Programmed cell death

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mitochondrial outer membrane - making them an integral part of mediating cell death by apoptosis. They do this by orchestrating the formation of pores within the membrane - essential to the release of cytochrome c. However, cytochrome c is only released if the mitochondrial membrane is compromised. Once cytochrome c is detected, the apoptosome complex is formed. This complex activates the executioner caspase which causes cell death. This killing of the cells may be essential as it prevents cellular overgrowth which can result in disease such as cancer. There are another two proteins worth mentioning that inhibit the release of cytochrome c in the mitochondria. Bcl-2 and Bcl-xl are anti-apoptotic and therefore prevent cell death. There is a potential mutation that can occur in that causes the overactivity of Bcl-2. It is the translocation between chromosomes 14 and 18. This over activity can result in the development of follicular lymphoma.

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biochemistry of these suicide pathways; some treading the path of "apoptosis", others following a more generalized pathway to deletion, but both usually being genetically and synthetically motivated. There is some evidence that certain symptoms of "apoptosis" such as endonuclease activation can be spuriously induced without engaging a genetic cascade, however, presumably true apoptosis and programmed cell death must be genetically mediated. It is also becoming clear that mitosis and apoptosis are toggled or linked in some way and that the balance achieved depends on signals received from appropriate growth or survival factors.

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is through fast ligan TNF-alpha binding or through a cytotoxic t-cell. The cytotoxic T-cell can attach itself to a membrane, facilitating the release of granzyme B. Granzyme B perforates the target cell membrane and in turn allows the release of perforin. Finally, perforin creates a pore in the membrane, and releases the caspases which leads to the activation of caspase 3. This initiator caspase may cause the cleaving of inactive caspase 3, causing it to become cleaved caspase 3. This is the final molecule needed to trigger cell death.

182: 780: 847:(Bcl-2-associated X protein) a larger percentage of interneurons survived compared to wild type mice. Together these findings indicate that programmed cell death in the CNS partly exploits Bax-mediated signaling and is independent of BDNF and the environment. Apoptotic mechanisms in the CNS are still not well understood, yet it is thought that apoptosis of interneurons is a self-autonomous process. 107:, was recognized as an alternative form of programmed cell death. It is hypothesized that necroptosis can serve as a cell-death backup to apoptosis when the apoptosis signaling is blocked by endogenous or exogenous factors such as viruses or mutations. Most recently, other types of regulated necrosis have been discovered as well, which share several signaling events with necroptosis and apoptosis. 895:, cerebellum, and spinal cord. However, PCD of neurons due to Bax deletion or Bcl-2 overexpression does not result in prominent morphological or behavioral abnormalities in mice. For example, mice overexpressing Bcl-2 have generally normal motor skills and vision and only show impairment in complex behaviors such as learning and anxiety. The normal behavioral 683: 281:

The extrinsic pathway involves specific receptor ligand interaction. Either the FAS ligand binds to the FAS receptor or the TNF-alpha ligand can bind to the TNF receptor. In both situations there is the activation of initiator caspase. The extrinsic pathway can be activated in two ways. The first way

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Programmed cell death can be reduced or eliminated in the developing nervous system by the targeted deletion of pro-apoptotic genes or by the overexpression of anti-apoptotic genes. The absence or reduction of PCD can cause serious anatomical malformations but can also result in minimal consequences

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is counterbalanced by the removal of neurons and their processes. During the development of the nervous system almost 50% of developing neurons are naturally removed by programmed cell death (PCD). PCD in the nervous system was first recognized in 1896 by John Beard. Since then several theories were

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tissue development, around eight years before "apoptosis" was coined. The term PCD has, however, been a source of confusion and Durand and Ramsey have developed the concept by providing mechanistic and evolutionary definitions. PCD has become the general terms that refers to all the different types

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and these mutations may cause cancer (see Figure). Several enzymatic pathways have evolved for repairing different kinds of DNA damage, and it has been found that in five well studied DNA repair pathways particular enzymes have a dual role, where one role is to participate in repair of a specific

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in 1892. Cajal presented the idea as an explanation for the "intelligent force" axons appear to take when finding their target but admitted that he had no empirical data. The theory gained more attraction when experimental manipulation of axon targets yielded death of all innervating neurons. This

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The neurotrophic theory is the leading hypothesis used to explain the role of programmed cell death in the developing nervous system. It postulates that in order to ensure optimal innervation of targets, a surplus of neurons is first produced which then compete for limited quantities of protective

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The intrinsic pathway is caused by cell damage such as DNA damage or UV exposure. This pathway takes place in the mitochondria and is mediated by sensors called Bcl sensors, and two proteins called BAX and BAK. These proteins are found in a majority of higher mammals as they are able to pierce the

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among other regions. At gestational weeks 19–23, PCD is observed in post-mitotic cells. The prevailing theory explaining this observation is the neurotrophic theory which states that PCD is required to optimize the connection between neurons and their afferent inputs and efferent targets. Another

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fragmentation. It is now thought that- in a developmental context- cells are induced to positively commit suicide whilst in a homeostatic context; the absence of certain survival factors may provide the impetus for suicide. There appears to be some variation in the morphology and indeed the

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and only a fraction survive while others die by programmed cell death. Furthermore, the theory states that predetermined factors regulate the amount of neurons that survive and the size of the innervating neuronal population directly correlates to the influence of their target field.

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class of damages and the second role is to induce apoptosis if the level of such DNA damage is beyond the cell’s repair capability. These dual role proteins tend to protect against development of cancer. Proteins that function in such a dual role for each repair process are: (1)

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Degterev, Alexei; Huang, Zhihong; Boyce, Michael; Li, Yaqiao; Jagtap, Prakash; Mizushima, Noboru; Cuny, Gregory D.; Mitchison, Timothy J.; Moskowitz, Michael A. (2005-07-01). "Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury".

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is the death of a cell caused by external factors such as trauma or infection and occurs in several different forms. Necrosis was long seen as a non-physiological process that occurs as a result of infection or injury, but in the 2000s, a form of programmed necrosis, called

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indicates that PCD may have an evolutionary significance in the development of the nervous system. In the nematode, PCD occurs in the first hour of development leading to the elimination of 12% of non-gonadal cells including neuronal lineages. Cell death in

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Bernstein C, Bernstein H, Payne CM, Garewal H. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat Res. 2002 Jun;511(2):145-78. doi: 10.1016/s1383-5742(02)00009-1. PMID:

835:. Transplanted cells died at the age of two weeks, the same age at which endogenous interneurons undergo apoptosis. Regardless of the size of the transplant, the fraction of cells undergoing apoptosis remained constant. Furthermore, disruption of 1310:

that can trigger cell suicide. It is not clear why apoptotic machinery is maintained in the extant unicellular organisms. This process has now been evolved to happen only when programmed. to cells (such as feedback from neighbors, stress or

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is a programmed form of necrosis, or inflammatory cell death. Conventionally, necrosis is associated with unprogrammed cell death resulting from cellular damage or infiltration by pathogens, in contrast to orderly, programmed cell death via

647:. Only natural forces on the cell are considered to be atrophic factors, whereas, for example, agents of mechanical or chemical abuse or lysis of the cell are considered not to be atrophic factors. Common types of atrophic factors are: 468:

to generate the cytosolic LC3-I. LC3-I is conjugated to phosphatidylethanolamine (PE) also in a ubiquitin-like reaction that requires Atg7 and Atg3. The lipidated form of LC3, known as LC3-II, is attached to the autophagosome membrane.

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is maintained by apoptotic machinery that appears to be independent of the environment. Supporting evidence came from an experiment where interneuron progenitors were either transplanted into the mouse neocortex or cultured

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There are two different potential pathways that may be followed when apoptosis is needed. There is the extrinsic pathway and the intrinsic pathway. Both pathways involve the use of caspases - crucial to cell death.

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developed the concept of target derived regulation which became the main tenet in the neurotrophic theory. Experiments that further supported this theory led to the identification of the first neurotrophic factor,

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exhibit extensive arborization followed by PCD in the retina while birds do not. Although synaptic refinement in vertebrate systems is largely dependent on PCD, other evolutionary mechanisms also play a role.

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that have gone awry during path finding. It is possible that PCD during the development of the nervous system serves different functions determined by the developmental stage, cell type, and even species.

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Dixon Scott J.; Lemberg Kathryn M.; Lamprecht Michael R.; Skouta Rachid; Zaitsev Eleina M.; Gleason Caroline E.; Patel Darpan N.; Bauer Andras J.; Cantley Alexandra M.; et al. (2012).

539:-independent programmed cell-death" or "necroptosis"), these alternative routes to death are as efficient as apoptosis and can function as either backup mechanisms or the main type of PCD. 915:

Learning about PCD in various species is essential in understanding the evolutionary basis and reason for apoptosis in development of the nervous system. During the development of the

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depending on the gene targeted, neuronal population, and stage of development. Excess progenitor cell proliferation that leads to gross brain abnormalities is often lethal, as seen in

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PCD in the developing nervous system has been observed in proliferating as well as post-mitotic cells. One theory suggests that PCD is an adaptive mechanism to regulate the number of

711:. In humans, PCD in progenitor cells starts at gestational week 7 and remains until the first trimester. This process of cell death has been identified in the germinal areas of the 732:

theory proposes that developmental PCD in the nervous system occurs in order to correct for errors in neurons that have migrated ectopically, innervated incorrect targets, or have

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Weltman, JK (February 8, 1987). "The 1986 Nobel Prize for Physiology or Medicine awarded for discovery of growth factors: Rita Levi-Montalcini, M.D., and Stanley Cohen, Ph.D.".

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The stalk is composed of dead cells that have undergone a type of PCD that shares many features of an autophagic cell-death: massive vacuoles forming inside cells, a degree of

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Plant cells undergo particular processes of PCD similar to autophagic cell death. However, some common features of PCD are highly conserved in both plants and metazoa.

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Fadini, GP; Menegazzo, L; Scattolini, V; Gintoli, M; Albiero, M; Avogaro, A (25 November 2015). "A perspective on NETosis in diabetes and cardiometabolic disorders".

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Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P (2014). "Regulated necrosis: the expanding network of non-apoptotic cell death pathways".

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Formigli, L; et al. (2000). "aponecrosis: morphological and biochemical exploration of a syncretic process of cell death sharing apoptosis and necrosis".

815:. Therefore, it is speculated that PCD in the PNS is dependent on the release of neurotrophic factors and thus follows the concept of the neurotrophic theory. 5373: 940:

and the other undergoes apoptosis. Furthermore, sex targeted cell death leads to different neuronal innervation of specific organs in males and females. In

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that removes the pieces of the dead cell. Instead of an immune response, the dying cell synthesizes substances to break itself down and places them in a

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and Bax (overexpression of Bcl-2 or deletion of Bax) produces an increase in the number of neurons in certain regions of the nervous system such as the

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in the central nervous system as well as the peripheral nervous system. However, there are a few differences between vertebrate species. For example,

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Kaczanowski S, Sajid M and Reece S E 2011 Evolution of apoptosis-like programmed cell death in unicellular protozoan parasites Parasites Vectors 4 44

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Rondi-Reig, L (2002). "To die or not to die, does it change the function? Behavior of transgenic mice reveals a role for developmental cell death".

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1358:, and when such cells are also defective in apoptosis they tend to survive even with excess DNA damage. Replication of DNA in such cells leads to 3699:

Martinou, JC (1994). "Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia".

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Lockshin RA, Williams CM (1964). "Programmed cell death—II. Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths".

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Buss, Robert R.; Sun, Woong; Oppenheim, Ronald W. (2006-07-21). "Adaptive Roles of Programmed Cell Death During Nervous System Development".

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Bursch W, Ellinger A, Gerner C, Fröhwein U, Schulte-Hermann R (2000). "Programmed cell death (PCD). Apoptosis, autophagic PCD, or others?".

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has additional significance: It permits the study of a developmental PCD path that does not depend on caspases characteristic of apoptosis.

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Mosinger, Ogilvie (1998). "Suppression of developmental retinal cell death but not of photoreceptor degeneration in Bax-deficient mice".

414:, p150 and Atg14-like protein or ultraviolet irradiation resistance-associated gene (UVRAG), is required for the induction of autophagy. 3755: 1295:

before the present, made it possible for certain eukaryotes and energy-producing prokaryotes to coexist and mutually benefit from their

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Fan, H (2001). "Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells".

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in PCD during development depends on the brain region and cell type. Knockout or inhibition of apoptotic protease activating factor 1 (

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Rubenstein, John; Pasko Rakic (2013). "Regulation of Neuronal Survival by Neurotrophins in the Developing Peripheral Nervous System".

2638: 5366: 5254: 2543: 1016:. Specific types of plant cells carry out unique cell-death programs. These have common features with animal apoptosis—for instance, 4033:

Rondi-Reig, L (2001). "Transgenic mice with neuronal overexpression of bcl-2 gene present navigation disabilities in a water task".

3650:"Protection of retinal ganglion cells from natural and axotomy-induced cell death in neonatal transgenic mice overexpressing bcl-2" 153:

PCD has been the subject of increasing attention and research efforts. This trend has been highlighted with the award of the 2002

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Oxidative stress or environmental insults can lead to DNA damage in replicating cells and this can result in apoptosis or cancer.

875:. The brainstem, spinal cord, and peripheral ganglia of these mice develop normally, however, suggesting that the involvement of 2761:

Neuronal cell death and some related regressive phenomena during neurogenesis: a selective historical review and progress report

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thickenings and programmed cell-death." The authors emphasize that the products of plant PCD play an important structural role.

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of an autophagy-related (Atg) gene product (mAtg13) and the scaffold protein FIP200. Class III PI3K complex, containing hVps34,

1655: 1436: 795:(CNS). In the PNS, innervation of the target is proportional to the amount of the target-released neurotrophic factors NGF and 594:

Aponecrosis is a hybrid of apoptosis and necrosis and refers to an incomplete apoptotic process that is completed by necrosis.

4530:"The PET1-CMS Mitochondrial Mutation in Sunflower Is Associated with Premature Programmed Cell Death and Cytochrome c Release" 1276:

and bacteria. Most of the time, invading bacteria are destroyed by the white blood cells; however, it is not uncommon for the

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is possible, but it remains controversial. Some categorize death in those organisms as unregulated apoptosis-like cell death.

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Kaczanowski, S. Apoptosis: its origin, history, maintenance and the medical implications for cancer and aging. Phys Biol 13,

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nervous system, PCD plays different roles in different species. The similarity of the asymmetric cell death mechanism in the

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Bonke M, Thitamadee S, Mähönen AP, Hauser MT, Helariutta Y (2003). "APL regulates vascular tissue identity in Arabidopsis".

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Lossi, L; Merighi, A (April 2003). "In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS".

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Besides the above two types of PCD, other pathways have been discovered. Called "non-apoptotic programmed cell-death" (or "

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Cook, B (1998). "Developmental neuronal death is not a universal phenomenon among cell types in the chick embryo retina".

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De la Rosa, EJ; De Pablo, F (October 23, 2000). "Cell death in early neural development: beyond the neurotrophic theory".

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by stimulating cell proliferation, BCL2 promoted cancer by stopping lymphoma cells from being able to kill themselves.

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bacteria, as well as a perilous step for the ancestors of mitochondria, which began to invade their proto-eukaryotic

907: 840: 779: 1163:. The structural role of the residues left by the dead cells is reminiscent of the products of PCD in plant tissue. 5607: 5602: 5450: 5320: 1355: 5532: 4734: 3742:

Zanjani, HS (1996). "Increased cerebellar Purkinje cell numbers in mice overexpressing a human bcl-2 transgene".

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Cowan, WN (2001). "Viktor Hamburger and Rita Levi-Montalcini: the path to the discovery of nerve growth factor".

883:), also results in malformations and increased embryonic lethality. Manipulation of apoptosis regulator proteins 31: 6104: 1072: 601: 17: 3007:

Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience

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Thomas SG, Franklin-Tong VE (2004). "Self-incompatibility triggers programmed cell death in Papaver pollen".

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Sulston, JE (1980). "The Caenorhabditis elegans male: postembryonic development of nongonadal structures".

3119:"Cell biology in neuroscience: Death of developing neurons: new insights and implications for connectivity" 6072: 6017: 5796: 5584: 1544: 1432: 2103: 843:(Bdnf), did not affect cell death. It has also been shown that in mice null for the proapoptotic factor 5765: 5521: 5209: 1416: 1396: 899:

of these mice suggest that an adaptive mechanism may be involved to compensate for the excess neurons.

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Lang, F; Lang, KS; Lang, PA; Huber, SM; Wieder, T (2006). "Mechanisms and significance of eryptosis".

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occurs in most parts of the nervous system during development. It has been observed before and during

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In contrast to invertebrates, the mechanism of programmed cell death is found to be more conserved in

527:-dependent autophagy, thereby functioning both as a pro-survival and as an anti-autophagic regulator. 390:

kinases, UNC-51-like kinase -1, -2, and -3 (ULK1, ULK2, UKL3), which play a similar role as the yeast

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1525: 997:", Martin Bonke and his colleagues had stated that one of the two long-distance transport systems in 788: 479:

are connected both positively and negatively, and extensive crosstalk exists between the two. During

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Doe, Cq (1985). "Development and segmental differences in the pattern of neuronal precursor cells".

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Kierszenbaum, A. L. & Tres, L. L. (ed Madelene Hyde) (ELSEVIER SAUNDERS, Philadelphia, 2012).

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Basic morphological and biochemical features of PCD have been conserved in both plant and animal

460:. The Atg12–Atg5 conjugate then interacts non-covalently with ATG16 to form a large complex. LC3/ 233: 1005:, consists of several cell-types "the differentiation of which involves deposition of elaborate 6062: 5961: 5718: 5330: 5290: 3787:"Overexpression of bcl-2 reduces sex differences in neuron number in the brain and spinal cord" 3074:

Oppenheim, Ronald (1989). "The neurotrophic theory and naturally occurring motorneuron death".

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The underlying idea that target cells secrete attractive or inducing factors and that their

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characteristic of metastatic cells is their altered expression of several apoptotic genes.

1384: 1044: 1040: 994: 747: 628:, an enzyme not involved in apoptosis, in response to infection by certain microorganisms. 496: 241: 199: 80:; the result is that the digits are separate. PCD serves fundamental functions during both 4154:

Sulston2, JE (1983). "The embryonic cell lineage of the nematode Caenorhabditis elegans".

3460:"Programmed cell death of developing mammalian neurons after genetic deletion of caspases" 3360:"Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9" 8: 5811: 5773: 5385: 5310: 5214: 5159: 4941: 1635: 1549: 1364: 1260:

step would have been risky for the primitive eukaryotic cells, which began to engulf the

768: 352: 245: 116: 4999: 4954: 4594: 4374: 3420: 3318: 3260: 2197: 2147: 2065: 1726: 682: 6119: 5064: 5019: 4913: 4886: 4853: 4705: 4679:"Dictyostelium cell death: early emergence and demise of highly polarized paddle cells" 4678: 4659: 4614: 4435: 4394: 4306: 4263: 4058: 4015: 3972: 3918: 3908: 3891: 3813: 3803: 3786: 3767: 3724: 3676: 3666: 3649: 3630: 3581: 3486: 3476: 3459: 3440: 3389: 3335: 3302: 3280: 3191: 3143: 3118: 3099: 2938: 2913:

Finlay, BL (1989). "Control of cell number in the developing mammalian visual system".

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and animals had differentiated. But, in addition to their place in the evolutionary

5979: 5942: 5923: 5259: 5244: 5229: 5048: 5003: 4958: 4908: 4898: 4857: 4837: 4784: 4743: 4700: 4692: 4643: 4618: 4598: 4581: 4551: 4543: 4500: 4492: 4443: 4427: 4378: 4361: 4290: 4247: 4212: 4163: 4128: 4085: 4042: 3999: 3976: 3954: 3913: 3903: 3845: 3808: 3798: 3751: 3708: 3671: 3661: 3634: 3612: 3585: 3563: 3522: 3481: 3471: 3444: 3424: 3393: 3371: 3330: 3322: 3264: 3218: 3195: 3179: 3175: 3138: 3130: 3103: 3083: 3038: 2969: 2942: 2922: 2879: 2836: 2798: 2731: 2723: 2679: 2671: 2582: 2539: 2504: 2467: 2426: 2418: 2391: 2371: 2275: 2201: 2161: 2151: 2069: 2012: 1978: 1935: 1882: 1799: 1789: 1760: 1730: 1277: 1273: 708: 73: 1910: 953:. Extensive studies performed on various vertebrates show that PCD of neurons and 5856: 5151: 5146: 4861: 4789: 4772: 4677:

Levraud JP, Adam M, Luciani MF, de Chastellier C, Blanton RL, Golstein P (2003).

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Programmed cell death in plants has a number of molecular similarities to animal

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integrity in humans. Cells that are deficient in DNA repair tend to accumulate

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Death of a cell mediated by intracellular program, often as part of development

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is involved in the regulation of apoptosis via its role in downregulating the

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10.1002/(sici)1096-9861(19961021)374:3<332::aid-cne2>3.0.co;2-2

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10.1002/(sici)1096-9861(19980622)396:1<12::aid-cne2>3.0.co;2-l

4259: 4251: 4224: 4175: 4140: 3927: 3763: 3720: 3685: 3626: 3536: 3436: 3385: 3230: 3134: 3095: 2934: 2727: 2287: 2175: 2156: 2081: 1752: 5994: 5919: 5861: 5728: 3849: 3303:"Intrinsically determined cell death of developing cortical interneurons" 2675: 1666: 1645: 1620: 1585: 1559: 1479:

The BCR-ABL oncogene has been found to be involved in the development of

1464: 1124: 1112: 1068: 1017: 950: 946:, PCD is essential in segmentation and specification during development. 868: 759: 755: 728: 588: 578: 565: 555: 237: 104: 5795: 4841: 4730:"Developmental cell death in dictyostelium does not require paracaspase" 4602: 4382: 3326: 2544:

10.1002/(sici)1097-4652(200001)182:1<41::aid-jcp5>3.0.co;2-7

1886: 1776:"Bacterial Programmed Cell Death and Multicellular Behavior in Bacteria" 978:, but it also has differences, the most obvious being the presence of a 6050: 5937: 5911: 5851: 5846: 5831: 5410: 5305: 5204: 5191: 5182: 4547: 4496: 4439: 1676: 1671: 1661: 1539: 1343: 1312: 1281: 1190: 1149: 1084: 942: 937: 929: 896: 716: 621: 607: 492: 418: 337: 257: 213: 136: 2236: 1828: 1773: 1177:

before the present. It seems that they emerged after the ancestors of

76:

in a developing human embryo occurs because cells between the fingers

5883: 5674: 5642: 5637: 5496: 5491: 5474: 5382: 5134: 3428: 2073: 1554: 1530: 1507: 1347: 1296: 1285: 1257: 1170: 1156: 1056: 1048: 1006: 979: 975: 872: 861: 857: 823: 808: 724: 664: 625: 584: 570: 500: 488: 484: 476: 472: 449: 387: 379: 356: 341: 329: 323: 319: 307: 303: 229: 204: 193: 186: 95: 91: 61: 57: 4431: 1939: 6027: 6009: 5971: 5888: 5733: 2375: 2255: 1650: 1580: 1420: 1359: 1307: 1238: 1222: 1133: 1103:

lands, interact with pollen and trigger PCD in incompatible (i.e.,

1029: 933: 920: 876: 832: 720: 465: 333: 315: 209: 143: 132: 99: 77: 5689: 4412:

Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999).

1735: 1710: 1694:

Srivastava, R. E. in Molecular Mechanisms (Humana Press, 2007).

911:

A conserved apoptotic pathway in nematodes, mammals and fruitflies

4727: 4411: 3943:"Behavioral visual acuity of wild type and bcl2 transgenic mouse" 2345: 2325: 1610: 1575: 1520: 1316: 1306:

and death, because mitochondria still retain their repertoire of

1211: 1199: 1189:, the fact that PCD has been observed in the humble, simple, six- 1092: 1025: 987: 962: 812: 644: 597: 574: 543: 536: 407: 348: 4676: 4326:"Programmed cell death in plants resembles apoptosis of animals" 2572: 2407:"Ferroptosis: An Iron-Dependent Form of Nonapoptotic Cell Death" 1241:

for this theory is the fact that mitochondria possess their own

1020:

degradation—but they also have their own peculiarities, such as

677: 232:

is the process of programmed cell death (PCD) that may occur in

6045: 5836: 5821: 5679: 5664: 5549: 5285: 5083:

http://iopscience.iop.org/article/10.1088/1478-3975/13/3/031001

3117:

Dekkers, MP; Nikoletopoulou, V; Barde, YA (November 11, 2013).

2360:

Kroemer G, Martin SJ (2005). "Caspase-independent cell death".

1480: 1351: 1234: 1169:

is a slime mold, part of a branch that might have emerged from

1100: 1096: 888: 610:

is another type of nonapoptotic cell death that is mediated by

383: 372: 360: 147: 120: 85: 1237:, which has since become widely accepted. The most convincing 1229:("living together inside") of larger eukaryotic cells. It was 818:

Programmed cell death in the CNS is not dependent on external

624:, an inflammatory type of cell death, is uniquely mediated by 5743: 5738: 5654: 5625: 5544: 5300: 4777:

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

3037:. Progress in Brain Research. Vol. 136. pp. 11–20. 1774:

Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R (2006).

1564: 1495: 1491: 1428: 1404: 1392: 1388: 1269: 1182: 1145: 1035:

Janneke Balk and Christopher J. Leaver, of the Department of

1002: 924: 884: 880: 733: 524: 520: 512: 457: 441: 429: 411: 322:

contents, abnormal protein aggregates, and excess or damaged

81: 49: 4823:"Cell death in parasitic protozoa: regulated or incidental?" 4463: 4358: 2181: 1111:, also found that the response involves rapid inhibition of 850: 5723: 5659: 5632: 5469: 5462: 5457: 2134: 1448: 1412: 1380: 1376: 1372: 1368: 1303: 1246: 1141: 954: 836: 804: 800: 774: 611: 577:

is another programmed form of necrosis that takes place in

516: 461: 453: 445: 437: 433: 421: 403: 399: 395: 391: 375: 128: 5129: 4885:

Szymon Kaczanowski; Mohammed Sajid; Sarah E Reece (2011).

3116: 695:

proposed to understand its biological significance during

487:

functions as a pro-survival mechanism, however, excessive

2127: 1859:

Histology and Cell Biology - An Introduction to Pathology

1452: 1408: 1400: 1242: 1055:

play the same key role in vascular plant PCD as in other

822:

but instead relies on intrinsically derived cues. In the

796: 546:, almost identical to apoptosis except in its induction; 508: 260: 5139: 127:

The first insight into the mechanism came from studying

1458: 216:

in a specific sequence prior to the destruction of the

68:, which usually confers advantage during an organism's 1350:

are two enzymatic processes essential for maintaining

783:

Cell death in the peripheral vs central nervous system

4026: 3004: 2826: 185:

Overview of signal transduction pathways involved in

4821:

Proto, W. R.; Coombs, G. H.; Mottram, J. C. (2012).

2956:

Yamaguchi, Yoshifumi; Miura, Masayuki (2015-02-23).

2130:"Do all programmed cell deaths occur via apoptosis?" 2128:

Schwartz LM, Smith SW, Jones ME, Osborne BA (1993).

1871: 1302:

Mitochondriate eukaryotic cells live poised between

1062: 936:

cells differentiate and one daughter cell becomes a

4578: 4323: 3110: 2615:(7th ed.). Wolters Kluwer Health. p. 94. 1132:has the peculiarity of either adopting a predatory 550:, a form of cell death exclusive to the epidermis; 371:A critical regulator of autophagy induction is the 267: 115:The concept of "programmed cell-death" was used by 5181: 4820: 2575:Nutrition, Metabolism, and Cardiovascular Diseases 382:and when not activated promotes it. Three related 5107: 5105: 5103: 5036: 4983: 3451: 2494: 2241:. New York: Cold Spring Harbor Laboratory Press. 1995: 1833:. New York: Cold Spring Harbor Laboratory Press. 6096: 5092: 5090: 4075: 3873:Investigative Ophthalmology & Visual Science 2863: 2104:"The Nobel Prize in Physiology or Medicine 2002" 1968: 1498:gene. Its role the disordered growth of tissue. 1319:activators that trigger the cell-death-inducing 1107:) pollen. The researchers, Steven G. Thomas and 902: 344:processes such as development, differentiation, 56:as a result of events inside of a cell, such as 5381: 5341:Strategies for engineered negligible senescence 3400: 2869: 1996:Durand and Ramsey, Pierre M. and Grant (2019). 1268:. This process is still evident today, between 5100: 4631: 3940: 3934: 2998: 2955: 2752: 1200:Evolutionary origin of mitochondrial apoptosis 993:In "APL regulates vascular tissue identity in 336:deprivation but has also been associated with 5781: 5367: 5167: 5114:Apoptosis, Cell Signaling, and Human Diseases 5087: 2822: 2820: 2359: 2051: 1291:One of these rare evolutionary events, about 1051:cells. Results of this research suggest that 1024:degradation triggered by the collapse of the 702: 678:Role in the development of the nervous system 542:Other forms of programmed cell death include 124:of cell death that have a genetic component. 5709: 4237: 4231: 3296: 3294: 1856: 639:An atrophic factor is a force that causes a 240:events lead to characteristic cell changes ( 4188:: CS1 maint: numeric names: authors list ( 3242: 3240: 3067: 3032: 2958:"Programmed Cell Death in Neurodevelopment" 2037:: CS1 maint: DOI inactive as of May 2024 ( 1330: 1210:The occurrence of programmed cell death in 1043:, carried out research on mutations in the 558:, an iron-dependent form of cell death and 146:. Unlike other cancer genes, which promote 5788: 5774: 5374: 5360: 5174: 5160: 5111: 4527: 4032: 3989: 2817: 2705: 2703: 2185:Annals of the New York Academy of Sciences 2045: 1631:Mitochondrial permeability transition pore 1284:to succeed, with the consequence known as 826:, a 4:1 ratio of excitatory to inhibitory 740: 600:is the process of cell-death generated by 208:: characterized by the formation of large 5255:Reliability theory of aging and longevity 4935: 4912: 4902: 4788: 4747: 4704: 4555: 4504: 4476: 4447: 3958: 3917: 3907: 3812: 3802: 3675: 3665: 3616: 3567: 3526: 3485: 3475: 3457: 3375: 3334: 3300: 3291: 3142: 3073: 3028: 3026: 2973: 2758: 2735: 2683: 2636:Chapter 10: All the Players on One Stage 2471: 2447: 2430: 2165: 2155: 1803: 1793: 1734: 851:Nervous system development in its absence 787:Different mechanisms regulate PCD in the 98:are both forms of programmed cell death. 4153: 4147: 3870: 3864: 3698: 3692: 3647: 3641: 3237: 3211:New England Regional Allergy Proceedings 2529: 2261: 1469: 1334: 932:occurs first in the nervous system when 906: 799:. Expression of neurotrophin receptors, 778: 775:Peripheral versus central nervous system 690:The initial expansion of the developing 681: 406:form a large complex with the mammalian 332:is generally activated by conditions of 180: 4770: 4118: 4112: 3741: 3735: 3598: 3592: 3508: 3502: 3246: 3208: 3202: 2784: 2782: 2780: 2778: 2776: 2774: 2772: 2770: 2709: 2700: 1688: 519:, also induce autophagy. Additionally, 14: 6097: 4939:(1996). "The birth of complex cells". 4324:Collazo C, Chacón O, Borrás O (2006). 4090:10.1146/annurev.neuro.29.051605.112800 3023: 2912: 2906: 2803:10.1146/annurev.neuro.29.051605.112800 2660:"Normal development of brain circuits" 2653: 2651: 1656:p53 upregulated modulator of apoptosis 119:& Williams in 1964 in relation to 5769: 5355: 5155: 3983: 3889: 3883: 3406: 3357: 3351: 3165: 3159: 2606: 2604: 2234: 1998:"The nature of programmed cell death" 1962: 1826: 464:is cleaved at its C terminus by ATG4 155:Nobel Prize in Physiology or Medicine 4280: 4274: 2788: 2767: 2610: 1852: 1850: 1708: 1570:BH3 interacting domain death agonist 1459:Programmed death of entire organisms 1327:is now crucial to all of our lives. 285: 276: 4773:"Programmed cell death in protists" 4202: 4196: 3835: 3829: 3784: 3778: 3549: 3543: 2657: 2648: 1323:cascade. As such, the cell suicide 1217:Biologists had long suspected that 1079:) as an important means to prevent 762:sensitivity was first put forth by 686:Dying cells in the proliferate zone 634: 378:, which when activated, suppresses 244:) and death. These changes include 74:differentiation of fingers and toes 24: 5528:Bcl-2 homologous antagonist killer 5200:Antagonistic pleiotropy hypothesis 3909:10.1523/JNEUROSCI.18-04-01428.1998 3838:Journal of Computational Neurology 3804:10.1523/JNEUROSCI.23-06-02357.2003 3744:Journal of Computational Neurology 3667:10.1523/JNEUROSCI.16-13-04186.1996 3477:10.1523/JNEUROSCI.21-13-04752.2001 2601: 2497:Antioxidants & Redox Signaling 2206:10.1111/j.1749-6632.2000.tb05594.x 2180:;and, for a more recent view, see 1861:. Philadelphia: ELSEVIER SAUNDERS. 969: 25: 6131: 5123: 4963:10.1038/scientificamerican0496-50 3301:Southwell, D.G. (November 2012). 1847: 1233:who from 1967 on championed this 1148:that will give birth to the next 1140:form or coalescing into a mobile 1118: 1063:PCD in pollen prevents inbreeding 841:brain derived neurotrophic factor 5608:Tumor necrosis factor receptor 2 5603:Tumor necrosis factor receptor 1 5451:Death-inducing signaling complex 5321:List of longest-living organisms 5135:International Cell Death Society 4283:Journal of Comparative Neurology 4240:Journal of Comparative Neurology 4205:Journal of Developmental Biology 3035:Changing Views of Cajal's Neuron 990:that ruptures as the cell dies. 268:Extrinsic Vs. Intrinsic Pathways 5533:Bcl-2-associated death promoter 5075: 5030: 4977: 4929: 4878: 4814: 4805: 4764: 4735:Journal of Biological Chemistry 4721: 4670: 4625: 4572: 4521: 4470: 4405: 4352: 4317: 4069: 2949: 2629: 2566: 2523: 2488: 2398: 2353: 2333: 2313: 2264:"Cell Biology International 17" 2228: 2121: 2096: 1144:-like form when dispersing the 32:Programmed cell death protein 1 4462:See also related articles in 3180:10.1146/annurev.neuro.24.1.551 2532:Journal of Cellular Physiology 2460:Cell Death and Differentiation 1989: 1917: 1865: 1857:Kierszenbaum, Abraham (2012). 1820: 1767: 1702: 1225:that had been incorporated as 530: 13: 1: 5130:Apoptosis and Cell Death Labs 4078:Annual Review of Neuroscience 4047:10.1016/s0306-4522(01)00050-1 4004:10.1016/s0361-9230(01)00639-6 3960:10.1016/s0042-6989(98)00169-2 3618:10.1016/s0092-8674(00)81733-x 3528:10.1016/s0092-8674(00)81732-8 3377:10.1016/s0092-8674(00)81476-2 3168:Annual Review of Neuroscience 3043:10.1016/s0079-6123(02)36004-7 2884:10.1016/s0301-0082(03)00051-0 2841:10.1016/s0166-2236(00)01628-3 2791:Annual Review of Neuroscience 1501: 903:Invertebrates and vertebrates 452:-like reaction that requires 5220:Free-radical theory of aging 4790:10.1016/j.bbamcr.2008.01.018 4217:10.1016/0012-1606(85)90445-2 4168:10.1016/0012-1606(83)90201-4 4133:10.1016/0012-1606(80)90352-8 3713:10.1016/0896-6273(94)90266-6 3088:10.1016/0166-2236(89)90021-0 2975:10.1016/j.devcel.2015.01.019 2927:10.1016/0301-0082(89)90017-8 2587:10.1016/j.numecd.2015.11.008 1983:10.1016/0022-1910(64)90034-4 1971:Journal of Insect Physiology 1795:10.1371/journal.pgen.0020135 1711:"Cell suicide for beginners" 1709:Raff, M (12 November 1998). 366: 310:process that results in the 294: 224: 131:, the product of a putative 7: 6073:Splanchnopleuric mesenchyme 6018:Splanchnopleuric mesenchyme 5797:Human embryonic development 5585:Tumor necrosis factor alpha 5112:Srivastava, Rakesh (2007). 4830:Nature Reviews Microbiology 2613:Histology: A Text and Atlas 1545:Apoptotic DNA fragmentation 1513: 1419:, the catalytic subunit of 1393:poly(ADP-ribose) polymerase 44:; sometimes referred to as 10: 6136: 5210:DNA damage theory of aging 4528:Balk J, Leaver CJ (2001). 3941:Gianfranceschi, L (1999). 3569:10.1016/j.cell.2005.03.016 3223:10.2500/108854187779045385 2423:10.1016/j.cell.2012.03.042 2268:Cell Biology International 1462: 1425:homologous recombinational 1417:non-homologous end joining 1397:nucleotide excision repair 1203: 1109:Vernonica E. Franklin-Tong 807:, is sufficient to induce 703:Role in neural development 614:through the activation of 142:often found in follicular 110: 64:. PCD is carried out in a 29: 6026: 6008: 5970: 5910: 5897: 5870: 5804: 5751:Apoptosis-inducing factor 5702: 5616: 5593: 5575: 5566: 5505: 5446: 5437: 5419: 5401: 5392: 5273: 5265:Stem cell theory of aging 5190: 5140:The Bcl-2 Family Database 2017:10.1007/s13752-018-0311-0 1526:Apoptosis-inducing factor 1288:by its resulting damage. 1115:growth, followed by PCD. 789:peripheral nervous system 6078:Somatopleuric mesenchyme 5990:Somatopleuric mesenchyme 5799:in the first three weeks 4477:Ito J, Fukuda H (2002). 2915:Progress in Neurobiology 2872:Progress in Neurobiology 1486: 1331:DNA damage and apoptosis 1315:), mitochondria release 1129:Dictyostelium discoideum 811:in the absence of their 503:. Several pro-apoptotic 394:, act downstream of the 202:or Type II cell-death. ( 176: 5240:Network theory of aging 5053:10.1126/science.1074592 5008:10.1126/science.1094884 4891:Parasites & Vectors 4684:Journal of Cell Biology 4648:10.1126/science.1080776 3992:Brain Research Bulletin 3896:Journal of Neuroscience 3791:Journal of Neuroscience 3654:Journal of Neuroscience 3464:Journal of Neuroscience 3269:10.1126/science.1236152 3076:Trends in Neurosciences 2829:Trends in Neurosciences 2716:Journal of Cell Biology 2664:Neuropsychopharmacology 2645:from PsychEducation.org 2509:10.1089/ars.2006.8.1183 2262:D. Bowen, Ivor (1993). 2235:Green, Douglas (2011). 2019:(inactive 2024-05-03). 1875:Nature Chemical Biology 1827:Green, Douglas (2011). 1032:elements of the xylem. 741:The neurotrophic theory 657:Diminished blood supply 302:, often referred to as 234:multicellular organisms 5962:Regional specification 5331:Regeneration (biology) 5291:Biological immortality 4904:10.1186/1756-3305-4-44 4749:10.1074/jbc.M312741200 4341:: 1–10. Archived from 4334:Biotecnología Aplicada 3458:Oppenheim, RW (2001). 2759:Oppenheim, RW (1981). 2611:Ross, Michael (2016). 2473:10.1038/sj.cdd.4401317 2280:10.1006/cbir.1993.1075 1682:Wallerian degeneration 1474: 1340: 1245:and are equipped with 1136:-like behavior in its 912: 793:central nervous system 784: 764:Santiago Ramon y Cajal 687: 587:is a form of suicidal 560:Wallerian degeneration 254:chromatin condensation 189: 6105:Programmed cell death 6068:Intraembryonic coelom 5250:Programmed cell death 5235:Negligible senescence 4697:10.1083/jcb.200212104 4465:The Plant Cell Online 4252:10.1002/cne.902260107 4156:Developmental Biology 4121:Developmental Biology 3135:10.1083/jcb.201306136 2728:10.1083/jcb.201306136 2157:10.1073/pnas.90.3.980 1927:Nat Rev Mol Cell Biol 1470:Clinical significance 1344:Repair of DNA damages 1338: 1204:Further information: 1181:and the ancestors of 1159:condensation, but no 910: 782: 685: 196:or Type I cell-death. 184: 38:Programmed cell death 30:For the protein, see 5336:Rejuvenation (aging) 3850:10.1002/cne.1055.abs 3648:Bonfanti, L (1996). 2710:Dekkers, MP (2013). 2676:10.1038/npp.2009.115 2108:The Nobel Foundation 1689:Notes and references 1385:base excision repair 1091:) has revealed that 1073:self-incompatibility 1045:mitochondrial genome 1041:University of Oxford 748:neurotrophic factors 660:Inadequate nutrition 318:degradation of bulk 88:tissue development. 6115:Cellular senescence 5311:Indefinite lifespan 5215:Evolution of ageing 5185:(biology of ageing) 5000:2004Sci...304..253D 4955:1996SciAm.274d..50D 4942:Scientific American 4842:10.1038/nrmicro2929 4771:Deponte, M (2008). 4603:10.1038/nature02540 4595:2004Natur.429..305T 4383:10.1038/nature02100 4375:2003Natur.426..181B 3599:Yoshida, H (1998). 3509:Cecconi, F (1998). 3421:1996Natur.384..368K 3327:10.1038/nature11523 3319:2012Natur.491..109S 3261:2013Sci...340...39D 2198:2000NYASA.926....1B 2148:1993PNAS...90..980S 2066:1988Natur.335..440V 1887:10.1038/nchembio711 1727:1998Natur.396..119R 1636:Mitotic catastrophe 1550:Autolysis (biology) 1365:DNA mismatch repair 982:and the lack of an 769:nerve growth factor 654:Loss of innervation 481:nutrient deficiency 72:. For example, the 5145:2009-02-21 at the 4548:10.1105/tpc.010116 4497:10.1105/tpc.006411 3890:White, FA (1998). 3009:. Academic Press. 2962:Developmental Cell 2641:2013-05-28 at the 1341: 1173:ancestors about a 1083:. Research on the 1081:self-fertilization 913: 893:trigeminal nucleus 785: 697:neural development 688: 651:Decreased workload 428:formation through 248:, cell shrinkage, 190: 66:biological process 6092: 6091: 6088: 6087: 5817:Oocyte activation 5763: 5762: 5759: 5758: 5698: 5697: 5562: 5561: 5558: 5557: 5386:signaling pathway 5349: 5348: 5326:Maximum life span 5281:Adaptive mutation 3660:(13): 4186–4194. 3470:(13): 4752–4760. 3415:(6607): 368–372. 3358:Kuida, K (1998). 3313:(7422): 109–115. 3016:978-0-12-397348-1 2248:978-0-87969-888-1 2005:Biological Theory 1840:978-0-87969-887-4 1293:two billion years 1161:DNA fragmentation 1071:, plants enforce 839:, a receptor for 791:(PNS) versus the 444:is conjugated to 346:neurodegenerative 286:Intrinsic Pathway 277:Extrinsic Pathway 167:H. Robert Horvitz 16:(Redirected from 6127: 5980:Surface ectoderm 5943:Primitive groove 5924:Primitive streak 5908: 5907: 5790: 5783: 5776: 5767: 5766: 5707: 5706: 5573: 5572: 5444: 5443: 5399: 5398: 5376: 5369: 5362: 5353: 5352: 5260:Selection shadow 5245:Plant senescence 5230:Immunosenescence 5176: 5169: 5162: 5153: 5152: 5118: 5117: 5109: 5098: 5094: 5085: 5079: 5073: 5072: 5034: 5028: 5027: 4981: 4975: 4974: 4933: 4927: 4926: 4916: 4906: 4882: 4876: 4875: 4873: 4872: 4866: 4860:. Archived from 4827: 4818: 4812: 4809: 4803: 4802: 4792: 4783:(7): 1396–1405. 4768: 4762: 4761: 4751: 4742:(12): 11489–94. 4725: 4719: 4718: 4708: 4674: 4668: 4667: 4629: 4623: 4622: 4576: 4570: 4569: 4559: 4525: 4519: 4518: 4508: 4474: 4468: 4461: 4451: 4409: 4403: 4402: 4356: 4350: 4349: 4347: 4330: 4321: 4315: 4314: 4278: 4272: 4271: 4235: 4229: 4228: 4200: 4194: 4193: 4187: 4179: 4151: 4145: 4144: 4116: 4110: 4109: 4073: 4067: 4066: 4030: 4024: 4023: 3987: 3981: 3980: 3962: 3938: 3932: 3931: 3921: 3911: 3902:(4): 1428–1439. 3887: 3881: 3880: 3868: 3862: 3861: 3833: 3827: 3826: 3816: 3806: 3797:(6): 2357–2362. 3785:Zup, SL (2003). 3782: 3776: 3775: 3739: 3733: 3732: 3707:(4): 1017–1030. 3696: 3690: 3689: 3679: 3669: 3645: 3639: 3638: 3620: 3596: 3590: 3589: 3571: 3547: 3541: 3540: 3530: 3506: 3500: 3499: 3489: 3479: 3455: 3449: 3448: 3429:10.1038/384368a0 3404: 3398: 3397: 3379: 3355: 3349: 3348: 3338: 3298: 3289: 3288: 3244: 3235: 3234: 3206: 3200: 3199: 3163: 3157: 3156: 3146: 3114: 3108: 3107: 3071: 3065: 3064: 3030: 3021: 3020: 3002: 2996: 2995: 2977: 2953: 2947: 2946: 2910: 2904: 2903: 2867: 2861: 2860: 2824: 2815: 2814: 2786: 2765: 2764: 2756: 2750: 2749: 2739: 2707: 2698: 2697: 2687: 2658:Tau, GZ (2009). 2655: 2646: 2633: 2627: 2626: 2608: 2599: 2598: 2570: 2564: 2563: 2527: 2521: 2520: 2503:(7–8): 1183–92. 2492: 2486: 2485: 2475: 2451: 2445: 2444: 2434: 2417:(5): 1060–1072. 2402: 2396: 2395: 2357: 2351: 2350: 2337: 2331: 2330: 2317: 2311: 2310: 2308: 2307: 2298:. Archived from 2259: 2253: 2252: 2232: 2226: 2225: 2179: 2169: 2159: 2125: 2119: 2118: 2116: 2115: 2100: 2094: 2093: 2074:10.1038/335440a0 2049: 2043: 2042: 2036: 2028: 2002: 1993: 1987: 1986: 1966: 1960: 1959: 1921: 1915: 1914: 1869: 1863: 1862: 1854: 1845: 1844: 1824: 1818: 1817: 1807: 1797: 1771: 1765: 1764: 1738: 1721:(6707): 119–22. 1706: 1278:chemical warfare 1262:energy-producing 1221:originated from 709:progenitor cells 635:Atrophic factors 440:-II) complexes. 46:cellular suicide 21: 6135: 6134: 6130: 6129: 6128: 6126: 6125: 6124: 6095: 6094: 6093: 6084: 6022: 6004: 5966: 5899: 5893: 5872: 5866: 5857:Inner cell mass 5800: 5794: 5764: 5755: 5694: 5612: 5589: 5554: 5540:Anti-apoptotic: 5501: 5433: 5415: 5388: 5380: 5350: 5345: 5269: 5186: 5180: 5147:Wayback Machine 5126: 5121: 5116:. Humana Press. 5110: 5101: 5095: 5088: 5080: 5076: 5047:(5579): 200–1. 5035: 5031: 4994:(5668): 253–7. 4982: 4978: 4934: 4930: 4883: 4879: 4870: 4868: 4864: 4825: 4819: 4815: 4810: 4806: 4769: 4765: 4726: 4722: 4675: 4671: 4630: 4626: 4589:(6989): 305–9. 4577: 4573: 4526: 4522: 4491:(12): 3201–11. 4475: 4471: 4432:10.2307/3870871 4410: 4406: 4369:(6963): 181–6. 4357: 4353: 4345: 4328: 4322: 4318: 4279: 4275: 4236: 4232: 4201: 4197: 4181: 4180: 4152: 4148: 4117: 4113: 4074: 4070: 4031: 4027: 3988: 3984: 3947:Vision Research 3939: 3935: 3888: 3884: 3869: 3865: 3834: 3830: 3783: 3779: 3740: 3736: 3697: 3693: 3646: 3642: 3597: 3593: 3550:Hao, Z (2005). 3548: 3544: 3507: 3503: 3456: 3452: 3405: 3401: 3356: 3352: 3299: 3292: 3255:(6128): 39–41. 3245: 3238: 3207: 3203: 3164: 3160: 3115: 3111: 3072: 3068: 3053: 3031: 3024: 3017: 3003: 2999: 2954: 2950: 2911: 2907: 2868: 2864: 2835:(10): 454–458. 2825: 2818: 2787: 2768: 2757: 2753: 2708: 2701: 2656: 2649: 2643:Wayback Machine 2634: 2630: 2623: 2609: 2602: 2571: 2567: 2528: 2524: 2493: 2489: 2452: 2448: 2403: 2399: 2363:Nature Medicine 2358: 2354: 2339: 2338: 2334: 2319: 2318: 2314: 2305: 2303: 2260: 2256: 2249: 2238:Means To An End 2233: 2229: 2126: 2122: 2113: 2111: 2102: 2101: 2097: 2060:(6189): 440–2. 2050: 2046: 2030: 2029: 2000: 1994: 1990: 1967: 1963: 1940:10.1038/nrm3737 1922: 1918: 1870: 1866: 1855: 1848: 1841: 1830:Means To An End 1825: 1821: 1772: 1768: 1707: 1703: 1691: 1686: 1535:Pseudoapoptosis 1516: 1504: 1489: 1477: 1472: 1467: 1461: 1333: 1208: 1202: 1121: 1065: 999:vascular plants 972: 970:In plant tissue 905: 853: 777: 743: 713:cerebral cortex 705: 680: 637: 533: 497:morphologically 369: 297: 288: 279: 270: 252:fragmentation, 227: 179: 171:John E. Sulston 113: 35: 28: 23: 22: 15: 12: 11: 5: 6133: 6123: 6122: 6117: 6112: 6107: 6090: 6089: 6086: 6085: 6083: 6082: 6081: 6080: 6075: 6070: 6060: 6055: 6054: 6053: 6048: 6038: 6036:Axial mesoderm 6032: 6030: 6024: 6023: 6021: 6020: 6014: 6012: 6006: 6005: 6003: 6002: 5997: 5992: 5987: 5982: 5976: 5974: 5968: 5967: 5965: 5964: 5959: 5958: 5957: 5947: 5946: 5945: 5940: 5934:Primitive node 5931: 5916: 5914: 5905: 5895: 5894: 5892: 5891: 5886: 5880: 5878: 5868: 5867: 5865: 5864: 5859: 5854: 5849: 5844: 5839: 5834: 5829: 5824: 5819: 5814: 5808: 5806: 5802: 5801: 5793: 5792: 5785: 5778: 5770: 5761: 5760: 5757: 5756: 5754: 5753: 5747: 5746: 5741: 5736: 5731: 5726: 5721: 5715: 5713: 5704: 5700: 5699: 5696: 5695: 5693: 5692: 5687: 5682: 5677: 5672: 5667: 5662: 5657: 5651: 5650: 5645: 5640: 5635: 5629: 5628: 5622: 5620: 5614: 5613: 5611: 5610: 5605: 5599: 5597: 5591: 5590: 5588: 5587: 5581: 5579: 5570: 5564: 5563: 5560: 5559: 5556: 5555: 5553: 5552: 5547: 5542: 5536: 5535: 5530: 5524: 5519: 5517:Pro-apoptotic: 5513: 5511: 5503: 5502: 5500: 5499: 5494: 5489: 5483: 5482: 5477: 5472: 5466: 5465: 5460: 5454: 5453: 5447: 5441: 5435: 5434: 5432: 5431: 5425: 5423: 5417: 5416: 5414: 5413: 5407: 5405: 5396: 5390: 5389: 5379: 5378: 5371: 5364: 5356: 5347: 5346: 5344: 5343: 5338: 5333: 5328: 5323: 5318: 5316:Life extension 5313: 5308: 5303: 5298: 5293: 5288: 5283: 5277: 5275: 5274:Related topics 5271: 5270: 5268: 5267: 5262: 5257: 5252: 5247: 5242: 5237: 5232: 5227: 5225:Hayflick limit 5222: 5217: 5212: 5207: 5202: 5196: 5194: 5188: 5187: 5179: 5178: 5171: 5164: 5156: 5150: 5149: 5137: 5132: 5125: 5124:External links 5122: 5120: 5119: 5099: 5086: 5074: 5029: 4976: 4928: 4877: 4813: 4804: 4763: 4720: 4691:(7): 1105–14. 4669: 4642:(5603): 56–7. 4624: 4571: 4542:(8): 1803–18. 4535:The Plant Cell 4520: 4484:The Plant Cell 4469: 4419:The Plant Cell 4404: 4351: 4348:on 2012-03-14. 4316: 4273: 4230: 4211:(1): 193–205. 4195: 4146: 4127:(2): 542–576. 4111: 4068: 4041:(1): 207–215. 4025: 3982: 3953:(3): 569–574. 3933: 3882: 3863: 3828: 3777: 3750:(3): 332–341. 3734: 3691: 3640: 3611:(6): 739–750. 3591: 3562:(4): 579–591. 3542: 3521:(6): 727–737. 3501: 3450: 3399: 3370:(3): 325–337. 3350: 3290: 3236: 3201: 3158: 3129:(3): 385–393. 3109: 3082:(7): 252–255. 3066: 3051: 3022: 3015: 2997: 2968:(4): 478–490. 2948: 2921:(3): 207–234. 2905: 2878:(5): 287–312. 2862: 2816: 2766: 2751: 2722:(3): 385–393. 2699: 2670:(1): 147–168. 2647: 2628: 2622:978-1451187427 2621: 2600: 2565: 2522: 2487: 2466:(2): 183–195. 2446: 2397: 2376:10.1038/nm1263 2352: 2332: 2312: 2274:(4): 365–380. 2254: 2247: 2227: 2120: 2095: 2044: 1988: 1977:(4): 643–649. 1961: 1934:(2): 135–147. 1916: 1881:(2): 112–119. 1864: 1846: 1839: 1819: 1766: 1700: 1699: 1698: 1695: 1690: 1687: 1685: 1684: 1679: 1674: 1669: 1664: 1659: 1653: 1648: 1643: 1638: 1633: 1628: 1623: 1618: 1616:Excitotoxicity 1613: 1608: 1606:Diablo homolog 1603: 1598: 1593: 1588: 1583: 1578: 1573: 1567: 1562: 1557: 1552: 1547: 1542: 1537: 1528: 1523: 1517: 1515: 1512: 1503: 1500: 1488: 1485: 1476: 1473: 1471: 1468: 1463:Main article: 1460: 1457: 1332: 1329: 1201: 1198: 1120: 1119:In slime molds 1117: 1089:Papaver rhoeas 1064: 1061: 1037:Plant Sciences 971: 968: 959:synaptogenesis 904: 901: 867:which develop 852: 849: 820:growth factors 776: 773: 742: 739: 704: 701: 692:nervous system 679: 676: 675: 674: 671: 668: 661: 658: 655: 652: 636: 633: 552:excitotoxicity 532: 529: 499:distinct from 368: 365: 312:autophagosomic 300:Macroautophagy 296: 293: 287: 284: 278: 275: 269: 266: 226: 223: 222: 221: 212:that eat away 197: 178: 175: 163:United Kingdom 159:Sydney Brenner 140:translocations 112: 109: 26: 18:Cellular aging 9: 6: 4: 3: 2: 6132: 6121: 6118: 6116: 6113: 6111: 6108: 6106: 6103: 6102: 6100: 6079: 6076: 6074: 6071: 6069: 6066: 6065: 6064: 6063:Lateral plate 6061: 6059: 6056: 6052: 6049: 6047: 6044: 6043: 6042: 6039: 6037: 6034: 6033: 6031: 6029: 6025: 6019: 6016: 6015: 6013: 6011: 6007: 6001: 5998: 5996: 5993: 5991: 5988: 5986: 5985:Neuroectoderm 5983: 5981: 5978: 5977: 5975: 5973: 5969: 5963: 5960: 5956: 5953: 5952: 5951: 5948: 5944: 5941: 5939: 5935: 5932: 5930: 5929:Primitive pit 5927: 5926: 5925: 5921: 5918: 5917: 5915: 5913: 5909: 5906: 5903: 5896: 5890: 5887: 5885: 5882: 5881: 5879: 5876: 5869: 5863: 5860: 5858: 5855: 5853: 5850: 5848: 5845: 5843: 5840: 5838: 5835: 5833: 5830: 5828: 5825: 5823: 5820: 5818: 5815: 5813: 5812:Fertilization 5810: 5809: 5807: 5803: 5798: 5791: 5786: 5784: 5779: 5777: 5772: 5771: 5768: 5752: 5749: 5748: 5745: 5742: 5740: 5737: 5735: 5732: 5730: 5727: 5725: 5722: 5720: 5717: 5716: 5714: 5712: 5711:Intracellular 5708: 5705: 5701: 5691: 5688: 5686: 5683: 5681: 5678: 5676: 5673: 5671: 5668: 5666: 5663: 5661: 5658: 5656: 5653: 5652: 5649: 5646: 5644: 5641: 5639: 5636: 5634: 5631: 5630: 5627: 5624: 5623: 5621: 5619: 5618:Intracellular 5615: 5609: 5606: 5604: 5601: 5600: 5598: 5596: 5592: 5586: 5583: 5582: 5580: 5578: 5574: 5571: 5569: 5565: 5551: 5548: 5546: 5543: 5541: 5538: 5537: 5534: 5531: 5529: 5525: 5523: 5520: 5518: 5515: 5514: 5512: 5510: 5509: 5504: 5498: 5495: 5493: 5490: 5488: 5485: 5484: 5481: 5478: 5476: 5473: 5471: 5468: 5467: 5464: 5461: 5459: 5456: 5455: 5452: 5449: 5448: 5445: 5442: 5440: 5439:Intracellular 5436: 5430: 5427: 5426: 5424: 5422: 5418: 5412: 5409: 5408: 5406: 5404: 5400: 5397: 5395: 5391: 5387: 5384: 5377: 5372: 5370: 5365: 5363: 5358: 5357: 5354: 5342: 5339: 5337: 5334: 5332: 5329: 5327: 5324: 5322: 5319: 5317: 5314: 5312: 5309: 5307: 5304: 5302: 5299: 5297: 5294: 5292: 5289: 5287: 5284: 5282: 5279: 5278: 5276: 5272: 5266: 5263: 5261: 5258: 5256: 5253: 5251: 5248: 5246: 5243: 5241: 5238: 5236: 5233: 5231: 5228: 5226: 5223: 5221: 5218: 5216: 5213: 5211: 5208: 5206: 5203: 5201: 5198: 5197: 5195: 5193: 5189: 5184: 5177: 5172: 5170: 5165: 5163: 5158: 5157: 5154: 5148: 5144: 5141: 5138: 5136: 5133: 5131: 5128: 5127: 5115: 5108: 5106: 5104: 5093: 5091: 5084: 5078: 5070: 5066: 5062: 5058: 5054: 5050: 5046: 5042: 5041: 5033: 5025: 5021: 5017: 5013: 5009: 5005: 5001: 4997: 4993: 4989: 4988: 4980: 4972: 4968: 4964: 4960: 4956: 4952: 4948: 4944: 4943: 4938: 4932: 4924: 4920: 4915: 4910: 4905: 4900: 4896: 4892: 4888: 4881: 4867:on 2016-03-03 4863: 4859: 4855: 4851: 4847: 4843: 4839: 4835: 4831: 4824: 4817: 4808: 4800: 4796: 4791: 4786: 4782: 4778: 4774: 4767: 4759: 4755: 4750: 4745: 4741: 4737: 4736: 4731: 4724: 4716: 4712: 4707: 4702: 4698: 4694: 4690: 4686: 4685: 4680: 4673: 4665: 4661: 4657: 4653: 4649: 4645: 4641: 4637: 4636: 4628: 4620: 4616: 4612: 4608: 4604: 4600: 4596: 4592: 4588: 4584: 4583: 4575: 4567: 4563: 4558: 4553: 4549: 4545: 4541: 4537: 4536: 4531: 4524: 4516: 4512: 4507: 4502: 4498: 4494: 4490: 4486: 4485: 4480: 4473: 4467: 4466: 4459: 4455: 4450: 4445: 4441: 4437: 4433: 4429: 4426:(3): 431–44. 4425: 4421: 4420: 4415: 4408: 4400: 4396: 4392: 4388: 4384: 4380: 4376: 4372: 4368: 4364: 4363: 4355: 4344: 4340: 4336: 4335: 4327: 4320: 4312: 4308: 4304: 4300: 4296: 4292: 4288: 4284: 4277: 4269: 4265: 4261: 4257: 4253: 4249: 4245: 4241: 4234: 4226: 4222: 4218: 4214: 4210: 4206: 4199: 4191: 4185: 4177: 4173: 4169: 4165: 4162:(1): 64–119. 4161: 4157: 4150: 4142: 4138: 4134: 4130: 4126: 4122: 4115: 4107: 4103: 4099: 4095: 4091: 4087: 4083: 4079: 4072: 4064: 4060: 4056: 4052: 4048: 4044: 4040: 4036: 4029: 4021: 4017: 4013: 4009: 4005: 4001: 3997: 3993: 3986: 3978: 3974: 3970: 3966: 3961: 3956: 3952: 3948: 3944: 3937: 3929: 3925: 3920: 3915: 3910: 3905: 3901: 3897: 3893: 3886: 3878: 3874: 3867: 3859: 3855: 3851: 3847: 3843: 3839: 3832: 3824: 3820: 3815: 3810: 3805: 3800: 3796: 3792: 3788: 3781: 3773: 3769: 3765: 3761: 3757: 3753: 3749: 3745: 3738: 3730: 3726: 3722: 3718: 3714: 3710: 3706: 3702: 3695: 3687: 3683: 3678: 3673: 3668: 3663: 3659: 3655: 3651: 3644: 3636: 3632: 3628: 3624: 3619: 3614: 3610: 3606: 3602: 3595: 3587: 3583: 3579: 3575: 3570: 3565: 3561: 3557: 3553: 3546: 3538: 3534: 3529: 3524: 3520: 3516: 3512: 3505: 3497: 3493: 3488: 3483: 3478: 3473: 3469: 3465: 3461: 3454: 3446: 3442: 3438: 3434: 3430: 3426: 3422: 3418: 3414: 3410: 3403: 3395: 3391: 3387: 3383: 3378: 3373: 3369: 3365: 3361: 3354: 3346: 3342: 3337: 3332: 3328: 3324: 3320: 3316: 3312: 3308: 3304: 3297: 3295: 3286: 3282: 3278: 3274: 3270: 3266: 3262: 3258: 3254: 3250: 3243: 3241: 3232: 3228: 3224: 3220: 3216: 3212: 3205: 3197: 3193: 3189: 3185: 3181: 3177: 3173: 3169: 3162: 3154: 3150: 3145: 3140: 3136: 3132: 3128: 3124: 3120: 3113: 3105: 3101: 3097: 3093: 3089: 3085: 3081: 3077: 3070: 3062: 3058: 3054: 3052:9780444508157 3048: 3044: 3040: 3036: 3029: 3027: 3018: 3012: 3008: 3001: 2993: 2989: 2985: 2981: 2976: 2971: 2967: 2963: 2959: 2952: 2944: 2940: 2936: 2932: 2928: 2924: 2920: 2916: 2909: 2901: 2897: 2893: 2889: 2885: 2881: 2877: 2873: 2866: 2858: 2854: 2850: 2846: 2842: 2838: 2834: 2830: 2823: 2821: 2812: 2808: 2804: 2800: 2796: 2792: 2785: 2783: 2781: 2779: 2777: 2775: 2773: 2771: 2762: 2755: 2747: 2743: 2738: 2733: 2729: 2725: 2721: 2717: 2713: 2706: 2704: 2695: 2691: 2686: 2681: 2677: 2673: 2669: 2665: 2661: 2654: 2652: 2644: 2640: 2637: 2632: 2624: 2618: 2614: 2607: 2605: 2596: 2592: 2588: 2584: 2580: 2576: 2569: 2561: 2557: 2553: 2549: 2545: 2541: 2537: 2533: 2526: 2518: 2514: 2510: 2506: 2502: 2498: 2491: 2483: 2479: 2474: 2469: 2465: 2461: 2457: 2450: 2442: 2438: 2433: 2428: 2424: 2420: 2416: 2412: 2408: 2401: 2393: 2389: 2385: 2381: 2377: 2373: 2370:(7): 725–30. 2369: 2365: 2364: 2356: 2348: 2347: 2342: 2336: 2328: 2327: 2322: 2316: 2302:on 2014-03-12 2301: 2297: 2293: 2289: 2285: 2281: 2277: 2273: 2269: 2265: 2258: 2250: 2244: 2240: 2239: 2231: 2223: 2219: 2215: 2211: 2207: 2203: 2199: 2195: 2191: 2187: 2186: 2177: 2173: 2168: 2163: 2158: 2153: 2149: 2145: 2141: 2137: 2136: 2131: 2124: 2109: 2105: 2099: 2091: 2087: 2083: 2079: 2075: 2071: 2067: 2063: 2059: 2055: 2048: 2040: 2034: 2026: 2022: 2018: 2014: 2010: 2006: 1999: 1992: 1984: 1980: 1976: 1972: 1965: 1957: 1953: 1949: 1945: 1941: 1937: 1933: 1929: 1928: 1920: 1912: 1908: 1904: 1900: 1896: 1892: 1888: 1884: 1880: 1876: 1868: 1860: 1853: 1851: 1842: 1836: 1832: 1831: 1823: 1815: 1811: 1806: 1801: 1796: 1791: 1787: 1783: 1782: 1781:PLOS Genetics 1777: 1770: 1762: 1758: 1754: 1750: 1746: 1742: 1737: 1736:10.1038/24055 1732: 1728: 1724: 1720: 1716: 1712: 1705: 1701: 1696: 1693: 1692: 1683: 1680: 1678: 1675: 1673: 1670: 1668: 1665: 1663: 1660: 1657: 1654: 1652: 1649: 1647: 1644: 1642: 1639: 1637: 1634: 1632: 1629: 1627: 1624: 1622: 1619: 1617: 1614: 1612: 1609: 1607: 1604: 1602: 1599: 1597: 1594: 1592: 1591:Cornification 1589: 1587: 1584: 1582: 1579: 1577: 1574: 1571: 1568: 1566: 1563: 1561: 1558: 1556: 1553: 1551: 1548: 1546: 1543: 1541: 1538: 1536: 1532: 1529: 1527: 1524: 1522: 1519: 1518: 1511: 1509: 1499: 1497: 1493: 1484: 1482: 1466: 1456: 1454: 1450: 1446: 1442: 1438: 1434: 1430: 1426: 1422: 1418: 1414: 1410: 1406: 1402: 1398: 1394: 1390: 1386: 1382: 1378: 1374: 1370: 1366: 1361: 1357: 1353: 1349: 1345: 1337: 1328: 1326: 1322: 1318: 1314: 1309: 1305: 1300: 1298: 1294: 1289: 1287: 1283: 1279: 1275: 1271: 1267: 1263: 1259: 1254: 1252: 1248: 1244: 1240: 1236: 1232: 1231:Lynn Margulis 1228: 1227:endosymbionts 1224: 1220: 1215: 1213: 1207: 1206:Symbiogenesis 1197: 1195: 1194:D. discoideum 1192: 1188: 1184: 1180: 1176: 1175:billion years 1172: 1168: 1167:D. discoideum 1164: 1162: 1158: 1153: 1151: 1147: 1143: 1139: 1135: 1131: 1130: 1126: 1116: 1114: 1110: 1106: 1102: 1099:on which the 1098: 1094: 1090: 1086: 1082: 1078: 1074: 1070: 1060: 1058: 1054: 1050: 1046: 1042: 1038: 1033: 1031: 1027: 1023: 1019: 1015: 1010: 1008: 1004: 1000: 996: 991: 989: 985: 984:immune system 981: 977: 967: 964: 960: 956: 952: 947: 945: 944: 939: 935: 931: 926: 922: 918: 909: 900: 898: 894: 890: 886: 882: 878: 874: 870: 866: 865:knockout mice 863: 859: 848: 846: 842: 838: 834: 829: 825: 821: 816: 814: 810: 806: 802: 798: 794: 790: 781: 772: 770: 765: 761: 757: 752: 749: 738: 735: 730: 726: 722: 718: 714: 710: 700: 698: 693: 684: 672: 669: 666: 662: 659: 656: 653: 650: 649: 648: 646: 642: 632: 629: 627: 623: 619: 617: 613: 609: 605: 603: 599: 595: 592: 590: 586: 582: 580: 576: 572: 567: 563: 561: 557: 553: 549: 548:cornification 545: 540: 538: 528: 526: 522: 518: 514: 510: 506: 502: 498: 494: 490: 486: 482: 478: 474: 470: 467: 463: 459: 455: 451: 447: 443: 439: 435: 431: 427: 426:autophagosome 423: 420: 415: 413: 409: 405: 401: 397: 393: 389: 385: 381: 377: 374: 364: 362: 358: 354: 350: 347: 343: 339: 338:physiological 335: 331: 327: 325: 321: 317: 313: 309: 305: 301: 292: 283: 274: 265: 262: 259: 255: 251: 247: 243: 239: 235: 231: 219: 215: 211: 207: 206: 201: 198: 195: 192: 191: 188: 183: 174: 172: 168: 164: 160: 156: 151: 149: 145: 141: 138: 135:activated by 134: 130: 125: 122: 118: 108: 106: 101: 97: 93: 89: 87: 83: 79: 75: 71: 67: 63: 59: 55: 51: 47: 43: 39: 33: 19: 6110:Mitochondria 6058:Intermediate 6000:Neural crest 5955:Gastrulation 5539: 5516: 5508:Bcl-2 family 5506: 5487:Cytochrome c 5429:Fas receptor 5296:CGK733 fraud 5249: 5113: 5077: 5044: 5038: 5032: 4991: 4985: 4979: 4946: 4940: 4931: 4894: 4890: 4880: 4869:. 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