Driving apoptosis-relevant proteins toward neural differentiation

Molecular Neurobiology

Volumn 46, Issue 2, 2012, Pages 316-331

  Solá, Susana ^a,b   Aranha, Márcia M ^a,c   Rodrigues, Cecília M P ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b Champalimaud Centre for the Unknown ^*  (Portugal)

^c CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

Author keywords

Apoptosis players; Cell fate; Neural differentiation; Stem cells

Indexed keywords

BECLIN 1; BIM PROTEIN; CASPASE; CASPASE 3; HISTONE ACETYLTRANSFERASE PCAF; PROTEIN BAD; PROTEIN BCL 2; PROTEIN BID; PROTEIN BNIP3; PROTEIN P53; PROTEIN P73; PROTEIN TYROSINE KINASE A; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR NANOG;

ACETYLATION; APOPTOSIS; ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL DEATH; CELL LOSS; CELL RENEWAL; DNA DAMAGE; EMBRYONIC STEM CELL; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NEDDYLATION; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SUMOYLATION; SYNAPTOGENESIS; UBIQUITINATION;

EID: 84868140124     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8289-2     Document Type: Article

References (180)

1. Ramon y Cajal S (1913) Degeneration and regeneration of the nervous system. Oxford University Press, London
2. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335
3. Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629-634 (Pubitemid 34141742)
4. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438 (Pubitemid 30127128)
5. Kempermann G, Gage FH (2000) Neurogenesis in the adult hippocampus. Novartis Found Symp 231:220-235
6. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, Thomson JA, Zhang SC (2010) Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci U S A 107:4335-4340
7. Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Sudhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature 476:220-223
8. Fernando P, Kelly JF, Balazsi K, Slack RS, Megeney LA (2002) Caspase 3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci U S A 99:11025-11030 (Pubitemid 34920873)
9. Fernando P, Brunette S, Megeney LA (2005) Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. FASEB J 19:1671-1673 (Pubitemid 41429525)
10. Fernando P, Megeney LA (2007) Is caspase-dependent apoptosis only cell differentiation taken to the extreme? FASEB J 21:8-17 (Pubitemid 46052541)
11. Stiewe T (2007) The p53 family in differentiation and tumorigenesis. Nat Rev Cancer 7:165-168
12. Ellis RE, Yuan JY, Horvitz HR (1991) Mechanisms and functions of cell death. Annu Rev Cell Biol 7:663-698
13. Reed JC (2002) Apoptosis-based therapies. Nat Rev Drug Discov 1:111-121 (Pubitemid 41646518)
14. Shi Y (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9:459-470 (Pubitemid 34273778)
15. Ashkenazi A (2002) Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2:420-430 (Pubitemid 37328939)
16. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501 (Pubitemid 28391865)
17. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH (2000) Pro-apoptotic cascade activates Bid, which oligomerizes Bak or Bax into pores that result in the release of cytochrome c. Cell Death Differ 7:1166-1173 (Pubitemid 32042223)
18. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312-1316 (Pubitemid 28406817)
19. Debatin KM, Krammer PH (2004) Death receptors in chemotherapy and cancer. Oncogene 23:2950-2966 (Pubitemid 38638855)
20. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99-163 (Pubitemid 46209992)
21. Sharpe JC, Arnoult D, Youle RJ (2004) Control of mitochondrial permeability by Bcl-2 family members. Biochim Biophys Acta 1644:107-113 (Pubitemid 38281267)
22. Miyashita T, Reed JC (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299
23. MichalakEM, Villunger A, Adams JM, Strasser A (2008) In several cell types tumour suppressor p53 induces apoptosis largely via PUMA but NOXA can contribute. Cell Death Differ 15:1019-1029 (Pubitemid 351712606)
24. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577-590 (Pubitemid 36385115)
25. Sot B, Freund SM, Fersht AR (2007) Comparative biophysical characterization of p53 with the pro-apoptotic Bak and the antiapoptotic Bcl-xL. J Biol Chem 282:29193-29200 (Pubitemid 350043367)
26. Galluzzi L, Morselli E, Kepp O, Vitale I, PintiM, Kroemer G (2011) Mitochondrial liaisons of p53. Antioxid Redox Signal 15:1691-1714
27. Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G (2012) Nonapoptotic functions of apoptosis-regulatory proteins. EMBO Rep 13:322-330
28. Vousden KH, Prives C (2009) Blinded by the light: the growing complexity of p53. Cell 137:413-431
29. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B, Reed JC (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805 (Pubitemid 24163411)
30. Cervantes RB, Stringer JR, Shao C, Tischfield JA, Stambrook PJ (2002) Embryonic stem cells and somatic cells differ in mutation frequency and type. Proc Natl Acad Sci U S A 99:3586-3590 (Pubitemid 34256391)
31. Aladjem MI, Spike BT, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, Wahl GM (1998) ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 8:145-155 (Pubitemid 28091572)
32. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, Xu Y (2005) p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 7:165-171 (Pubitemid 40268131)
33. Li M, He Y, Dubois W, Wu X, Shi J, Huang J (2012) Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol Cell 46:30-42
34. Tedeschi A, Di Giovanni S (2009) The non-apoptotic role of p53 in neuronal biology: enlightening the dark side of the moon. EMBO Rep 10:576-583
35. Qin H, Yu T, Qing T, Liu Y, Zhao Y, Cai J, Li J, Song Z, Qu X, Zhou P, Wu J, Ding M, Deng H (2007) Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. J Biol Chem 282:5842-5852 (Pubitemid 47093795)
36. Maimets T, Neganova I, Armstrong L, Lako M (2008) Activation of p53 by nutlin leads to rapid differentiation of human embryonic stem cells. Oncogene 27:5277-5287
37. Abdelalim EM, Tooyama I (2012) NPR-C protects embryonic stem cells from apoptosis by regulating p53 levels. Stem Cells Dev 21:1264-1271
38. Yang A, Kaghad M, Caput D, McKeon F (2002) On the shoulders of giants: p63, p73 and the rise of p53. Trends Genet 18:90-95 (Pubitemid 34127808)
39. Vousden KH, Lane DP (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8:275-283 (Pubitemid 46474662)
40. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713 (Pubitemid 29197649)
41. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, McKeon F (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718 (Pubitemid 29197650)
42. Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J, Vagner C, Bonnet H, Dikkes P, Sharpe A, McKeon F, Caput D (2000) p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404:99-103 (Pubitemid 30143141)
43. Nicotera P, Melino G (2005) Neurodevelopment on route p63. Neuron 48:707-709 (Pubitemid 41759418)
44. Fonseca MB, Nunes AF, Rodrigues CM (2012) c-Jun regulates the stability of anti-apoptotic deltaNp63 in amyloid-beta-induced apoptosis. J Alzheimers Dis 28:685-694
45. Jacobs WB, Govoni G, Ho D, Atwal JK, Barnabe-Heider F, Keyes WM, Mills AA, Miller FD, Kaplan DR (2005) p63 is an essential proapoptotic protein during neural development. Neuron 48:743-756 (Pubitemid 41759426)
46. Hernández-Acosta NC, Cabrera-Socorro A, Morlans MP, Delgado FJ, Suárez-Solá ML, Sottocornola R, Lu X, González-Gómez M, Meyer G (2011) Dynamic expression of the p53 family members p63 and p73 in the mouse and human telencephalon during development and in adulthood. Brain Res 1372:29-40
47. Holembowski L, Schulz R, Talos F, Scheel A, Wolff S, Dobbelstein M, Moll U (2011) While p73 is essential, p63 is completely dispensable for the development of the central nervous system. Cell Cycle 10:680-689
48. Donehower LA, HarveyM, Slagle BL,McArthurMJ,Montgomery CA Jr, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221
49. Armstrong JF, Kaufman MH, Harrison DJ, Clarke AR (1995) High-frequency developmental abnormalities in p53-deficient mice. Curr Biol 5:931-936
50. Sah VP, Attardi LD, Mulligan GJ, Williams BO, Bronson RT, Jacks T (1995) A subset of p53-deficient embryos exhibit exencephaly. Nat Genet 10:175-180
51. Louis JM, McFarland VW, May P, Mora PT (1988) The phosphoprotein p53 is down-regulated post-transcriptionally during embryogenesis in vertebrates. Biochim Biophys Acta 950:395-402
52. Rogel A, Popliker M, Webb CG, Oren M (1985) p53 cellular tumor antigen: analysis of mRNA levels in normal adult tissues, embryos, and tumors. Mol Cell Biol 5:2851-2855 (Pubitemid 15237110)
53. Schmid P, Lorenz A, Hameister H, Montenarh M (1991) Expression of p53 during mouse embryogenesis. Development 113:857-865 (Pubitemid 21900325)
54. Gottlieb E, Haffner R, King A, Asher G, Gruss P, Lonai P, Oren M (1997) Transgenic mouse model for studying the transcriptional activity of the p53 protein: age- and tissue-dependent changes in radiation-induced activation during embryogenesis. EMBO J 16:1381-1390 (Pubitemid 27136103)
55. Komarova EA, Chernov MV, Franks R, Wang K, Armin G, Zelnick CR, Chin DM, Bacus SS, Stark GR, Gudkov AV (1997) Transgenic mice with p53-responsive lacz: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J 16:1391-1400 (Pubitemid 27136104)
56. Hughes AL, Gollapudi L, Sladek TL, Neet KE (2000) Mediation of nerve growth factor-driven cell cycle arrest in PC12 cells by p53. Simultaneous differentiation and proliferation subsequent to p53 functional inactivation. J Biol Chem 275:37829-37837 (Pubitemid 32004900)
57. Montano X (1997) p53 associates with trk tyrosine kinase. Oncogene 15:245-256 (Pubitemid 27370871)
58. Poluha W, Schonhoff CM, Harrington KS, Lachyankar MB, Crosbie NE, Bulseco DA, Ross AH (1997) A novel, nerve growth factor-activated pathway involving nitric oxide, p53, and p21WAF1 regulates neuronal differentiation of PC12 cells. J Biol Chem 272:24002-24007 (Pubitemid 27410984)
59. Zhang J, Yan W, Chen X (2006) p53 is required for nerve growth factor-mediated differentiation of PC12 cells via regulation of trka levels. Cell Death Differ 13:2118-2128 (Pubitemid 44742695)
60. Browes C, Rowe J, Brown A, Montano X (2001) Analysis of trk A and p53 association. FEBS Lett 497:20-25 (Pubitemid 32480174)
61. Brynczka C, Labhart P, Merrick BA (2007) NGF-mediated transcriptional targets of p53 in PC12 neuronal differentiation. BMC Genomics 8:139
62. Di Giovanni S, Faden AI, Yakovlev A, Duke-Cohan JS, Finn T, Thouin M, Knoblach S, De Biase A, Bregman BS, Hoffman EP (2005) Neuronal plasticity after spinal cord injury: identification of a gene cluster driving neurite outgrowth. FASEB J 19:153-154 (Pubitemid 40069949)
63. Lee KH, Li M, Michalowski AM, Zhang X, Liao H, Chen L, Xu Y,Wu X, Huang J (2010) A genomewide study identifies the Wnt signaling pathway as a major target of p53 in murine embryonic stem cells. Proc Natl Acad Sci U S A 107:69-74
64. Di Giovanni S, Knights CD, Rao M, Yakovlev A, Beers J, Catania J, Avantaggiati ML, Faden AI (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25:4084-4096 (Pubitemid 44338749)
65. Tedeschi A, Nguyen T, Puttagunta R, Gaub P, Di Giovanni S (2009) A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth, and regeneration. Cell Death Differ 16:543-554
66. Helton ES, Chen X (2007) p53 modulation of the DNA damage response. J Cell Biochem 100:883-896
67. Aranha MM, Sola S, Low WC, Steer CJ, Rodrigues CM (2009) Caspases and p53 modulate FOXO3A/Id1 signaling during mouse neural stem cell differentiation. J Cell Biochem 107:748-758
68. Ostrakhovitch EA, Semenikhin OA (2011) p53-mediated regulation of neuronal differentiation via regulation of dual oxidase maturation factor 1. Neurosci Lett 494:80-85
69. Solá S, Xavier JM, Santos DM, Aranha MM, Morgado AL, Jepsen K, Rodrigues CM (2011) p53 interaction with JMJD3 results in its nuclear distribution during mouse neural stem cell differentiation. PLoS One 6:e18421
70. Krizhanovsky V, Lowe SW (2009) Stem cells: the promises and perils of p53. Nature 460:1085-1086
71. Armesilla-Diaz A, Bragado P, Del Valle I, Cuevas E, Lazaro I, Martin C, Cigudosa JC, Silva A (2009) p53 regulates the self-renewal and differentiation of neural precursors. Neuroscience 158:1378-1389
72. van Lookeren CM, Gill R (1998) Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: Comparison with expression of the cell cycle regulators p21Waf1/cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J Comp Neurol 397:181-198 (Pubitemid 28303354)
73. Meletis K, Wirta V, Hede SM, Nister M, Lundeberg J, Frisen J (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133:363-369 (Pubitemid 43210724)
74. Mori S, Matsuyama K, Mori F, Nakajima K (2001) Supraspinal sites that induce locomotion in the vertebrate central nervous system. Adv Neurol 87:25-40
75. Han MK, Song EK, Guo Y, Ou X, Mantel C, Broxmeyer HE (2008) Sirt1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell Stem Cell 2:241-251 (Pubitemid 351298591)
76. Gil-Perotin S, Marin-Husstege M, Li J, Soriano-Navarro M, Zindy F, Roussel MF, Garcia-Verdugo JM, Casaccia-Bonnefil P (2006) Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J Neurosci 26:1107-1116 (Pubitemid 43237042)
77. Gil-Perotin S, Haines JD, Kaur J, Marin-Husstege M, Spinetta MJ, Kim KH, Duran-Moreno M, Schallert T, Zindy F, Roussel MF, Garcia-Verdugo JM, Casaccia P (2011) Roles of p53 and p27 (Kip1) in the regulation of neurogenesis in the murine adult subventricular zone. Eur J Neurosci 34:1040-1052
78. Niu W, Zou Y, Shen C, Zhang CL (2011) Activation of postnatal neural stem cells requires nuclear receptor TLX. J Neurosci 31:13816-13828
79. Lavin MF, Gueven N (2006) The complexity of p53 stabilization and activation. Cell Death Differ 13:941-950
80. Ferecatu I, Rincheval V, Mignotte B, Vayssiere JL (2009) Tickets for p53 journey among organelles. Front Biosci 14:4214-4228
81. Sims RJ 3rd, Reinberg D (2008) Is there a code embedded in proteins that is based on post-translational modifications? Nat Rev Mol Cell Biol 9:815-820
82. Xu Y (2003) Regulation of p53 responses by post-translational modifications. Cell Death Differ 10:400-403 (Pubitemid 36626351)
83. Wong K, Zhang J, Awasthi S, Sharma A, Rogers L, Matlock EF, Van Lint C, Karpova T, McNally J, Harrod R (2004) Nerve growth factor receptor signaling induces histone acetyltransferase domain-dependent nuclear translocation of p300/CREB-binding protein-associated factor and hGCN5 acetyltransferases. J Biol Chem 279:55667-55674 (Pubitemid 40066571)
84. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, Quong AA, Zhang X, Beerman T, Pestell RG, Avantaggiati ML (2006) Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 173:533-544 (Pubitemid 43765200)
85. Brynczka C, Merrick BA (2007) Nerve growth factor potentiates p53 DNA binding but inhibits nitric oxide-induced apoptosis in neuronal PC12 cells. Neurochem Res 32:1573-1585 (Pubitemid 47094420)
86. Fabian Z, Vecsernyes M, Pap M, Szeberenyi J (2006) The effects of a mutant p53 protein on the proliferation and differentiation of PC12 rat phaeochromocytoma cells. J Cell Biochem 99:1431-1441
87. Scoumanne A, Chen X (2008) Protein methylation: a new mechanism of p53 tumor suppressor regulation. Histol Histopathol 23:1143-1149
88. Tsai WW, Nguyen TT, Shi Y, Barton MC (2008) p53-targeted LSD1 functions in repression of chromatin structure and transcription in vivo. Mol Cell Biol 28:5139-5146
89. Hudson CD, Morris PJ, Latchman DS, Budhram-Mahadeo VS (2005) Brn-3a transcription factor blocks p53-mediated activation of proapoptotic target genes Noxa and Bax in vitro and in vivo to determine cell fate. J Biol Chem 280:11851-11858 (Pubitemid 40418499)
90. Chen D, Zheng W, Lin A, Uyhazi K, Zhao H, Lin H (2012) Pumilio 1 suppresses multiple activators of p53 to safeguard spermatogenesis. Curr Biol 22:420-425
91. Murray-Zmijewski F, Slee EA, Lu X (2008) A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 9:702-712
92. Kaghad M, Bonnet H, Yang A, Creancier L, Biscan JC, Valent A, Minty A, Chalon P, Lelias JM, Dumont X, Ferrara P, McKeon F, Caput D (1997) Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90:809-819 (Pubitemid 27357971)
93. Muller M, Schilling T, Sayan AE, Kairat A, Lorenz K, Schulze-Bergkamen H, Oren M, Koch A, Tannapfel A, Stremmel W, Melino G, Krammer PH (2005) TAp73/delta Np73 influences apoptotic response, chemosensitivity and prognosis in hepatocellular carcinoma. Cell Death Differ 12:1564-1577 (Pubitemid 41679162)
94. Grob TJ, Novak U, Maisse C, Barcaroli D, Luthi AU, Pirnia F, Hugli B, Graber HU, De Laurenzi V, Fey MF, Melino G, Tobler A (2001) Human delta Np73 regulates a dominant negative feedback loop for TAp73 and p53. Cell Death Differ 8:1213-1223 (Pubitemid 34048476)
95. Tomasini R, Tsuchihara K, Wilhelm M, Fujitani M, Rufini A, Cheung CC, Khan F, Itie-Youten A, Wakeham A, Tsao MS, Iovanna JL, Squire J, Jurisica I, Kaplan D, Melino G, Jurisicova A, Mak TW (2008) TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev 22:2677-2691
96. De Laurenzi V, Raschella G, Barcaroli D, Annicchiarico-Petruzzelli M, Ranalli M, Catani MV, Tanno B, Costanzo A, Levrero M, Melino G (2000) Induction of neuronal differentiation by p73 in a neuroblastoma cell line. J Biol Chem 275:15226-15231 (Pubitemid 30337247)
97. Billon N, Terrinoni A, Jolicoeur C, McCarthy A, Richardson WD, Melino G, Raff M (2004) Roles for p53 and p73 during oligodendrocyte development. Development 131:1211-1220 (Pubitemid 38443876)
98. Talos F, Abraham A, Vaseva AV, Holembowski L, Tsirka SE, Scheel A, Bode D, Dobbelstein M, Bruck W, Moll UM (2010) p73 is an essential regulator of neural stem cell maintenance in embryonal and adult CNS neurogenesis. Cell Death Differ 17:1816-1829
99. Agostini M, Tucci P, Chen H, Knight RA, Bano D, Nicotera P, McKeon F, Melino G (2010) p73 regulates maintenance of neural stem cell. Biochem Biophys Res Commun 403:13-17
100. Fujitani M, Cancino GI, Dugani CB, Weaver IC, Gauthier-Fisher A, Paquin A, Mak TW, Wojtowicz MJ, Miller FD, Kaplan DR (2010) TAp73 acts via the bHLH Hey2 to promote long-term maintenance of neural precursors. Curr Biol 20:2058-2065
101. Gonzalez-Cano L, Herreros-Villanueva M, Fernandez-Alonso R, Ayuso-Sacido A, Meyer G, Garcia-Verdugo JM, Silva A, Marques MM, Marin MC (2010) p73 deficiency results in impaired self renewal and premature neuronal differentiation of mouse neural progenitors independently of p53. Cell Death Dis 1:e109
102. Agostini M, Tucci P, Steinert JR, Shalom-Feuerstein R, Rouleau M, Aberdam D, Forsythe ID, Young KW, Ventura A, Concepcion CP, Han YC, Candi E, Knight RA, Mak TW, Melino G (2011) MicroRNA-34a regulates neurite outgrowth, spinal morphology, and function. Proc Natl Acad Sci U S A 108:21099-21104
103. Agostini M, Tucci P, Killick R, Candi E, Sayan BS, di Val R, Cervo P, Nicotera P, McKeon F, Knight RA, Mak TW, Melino G (2011) Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proc Natl Acad Sci U S A 108:21093-21098
104. Li J, Yuan J (2008) Caspases in apoptosis and beyond. Oncogene 27:6194-6206
105. Yi CH, Yuan J (2009) The jekyll and hyde functions of caspases. Dev Cell 16:21-34
106. Dix MM, Simon GM, Cravatt BF (2008) Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 134:679-691
107. Mahrus S, Trinidad JC, Barkan DT, Sali A, Burlingame AL, Wells JA (2008) Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134:866-876
108. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J et al (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768-774
109. Sjakste N, Sjakste T (2007) Possible involvement of DNA strand breaks in regulation of cell differentiation. Eur J Histochem 51:81-94 (Pubitemid 351480291)
110. Larsen BD, Rampalli S, Burns LE, Brunette S, Dilworth FJ, Megeney LA (2010) Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks. Proc Natl Acad Sci U S A 107:4230-4235
111. Larsen BD, Megeney LA (2010) Parole terms for a killer: directing caspase3/CAD induced DNA strand breaks to coordinate changes in gene expression. Cell Cycle 9:2940-2945
112. Carlile GW, Smith DH, Wiedmann M (2004) Caspase-3 has a nonapoptotic function in erythroid maturation. Blood 103:4310-4316 (Pubitemid 38685378)
113. Zermati Y, Garrido C, Amsellem S, Fishelson S, Bouscary D, Valensi F, Varet B, Solary E, Hermine O (2001) Caspase activation is required for terminal erythroid differentiation. J Exp Med 193:247-254 (Pubitemid 32524456)
114. Radley JM, Scurfield G (1980) The mechanism of platelet release. Blood 56:996-999 (Pubitemid 11205051)
115. De Botton S, Sabri S, Daugas E, Zermati Y, Guidotti JE, Hermine O, Kroemer G, Vainchenker W, Debili N (2002) Platelet formation is the consequence of caspase activation within megakaryocytes. Blood 100:1310-1317 (Pubitemid 34864286)
116. Ishizaki Y, Jacobson MD, Raff MC (1998) A role for caspases in lens fiber differentiation. J Cell Biol 140:153-158 (Pubitemid 28070903)
117. Fujita J, Crane AM, Souza MK, Dejosez M, Kyba M, Flavell RA, Thomson JA, Zwaka TP (2008) Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell 2:595-601 (Pubitemid 351729216)
118. Janzen V, Fleming HE, Riedt T, Karlsson G, Riese MJ, Lo Celso C, Reynolds G, Milne CD, Paige CJ, Karlsson S, Woo M, Scadden DT (2008) Hematopoietic stem cell responsiveness to exogenous signals is limited by caspase-3. Cell Stem Cell 2:584-594 (Pubitemid 351751901)
119. Mogi M, Togari A (2003) Activation of caspases is required for osteoblastic differentiation. J Biol Chem 278:47477-47482 (Pubitemid 37523189)
120. Miura M, Chen XD, Allen MR, Bi Y, Gronthos S, Seo BM, Lakhani S, Flavell RA, Feng XH, Robey PG, Young M, Shi S (2004) A crucial role of caspase-3 in osteogenic differentiation of bone marrow stromal stem cells. J Clin Invest 114:1704-1713 (Pubitemid 40385526)
121. Li F, He Z, Shen J, Huang Q, Li W, Liu X, He Y, Wolf F, Li CY (2010) Apoptotic caspases regulate induction of ipscs from human fibroblasts. Cell Stem Cell 7:508-520
122. Crawford ED, Wells JA (2011) Caspase substrates and cellular remodeling. Annu Rev Biochem 80:1055-1087
123. Feinstein-Rotkopf Y, Arama E (2009) Can't live without them, can live with them: roles of caspases during vital cellular processes. Apoptosis 14:980-995
124. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51:283-290 (Pubitemid 44118716)
125. Huesmann GR, Clayton DF (2006) Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron 52:1061-1072 (Pubitemid 44909403)
126. Lu C, Fu W, Salvesen GS, Mattson MP (2002) Direct cleavage of AMPA receptor subunit GluR1 and suppression of AMPA currents by caspase-3: implications for synaptic plasticity and excitotoxic neuronal death. Neuromol Med 1:69-79 (Pubitemid 37021525)
127. Li Z, Jo J, Jia JM, Lo SC, Whitcomb DJ, Jiao S, Cho K, Sheng M (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141:859-871
128. Gulyaeva NV, Kudryashov IE, Kudryashova IV (2003) Caspase activity is essential for long-term potentiation. J Neurosci Res 73:853-864 (Pubitemid 37071740)
129. Jo J, Whitcomb DJ, Olsen KM, Kerrigan TL, Lo SC, Bru-Mercier G, Dickinson B, Scullion S, Sheng M, Collingridge G, Cho K (2011) Abeta(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3beta. Nat Neurosci 14:545-547
130. Kudryashova IV, Kudryashov IE, Gulyaeva NV (2006) Longterm potentiation in the hippocampus in conditions of inhibition of caspase-3: analysis of facilitation in paired-pulse stimulation. Neurosci Behav Physiol 36:817-824 (Pubitemid 44363712)
131. Miura M (2011) Apoptotic and non-apoptotic caspase functions in neural development. Neurochem Res 36:1253-1260
132. Fan Y, Bergmann A (2008) Distinct mechanisms of apoptosis-induced compensatory proliferation in proliferating and differentiating tissues in the Drosophila eye. Dev Cell 14:399-410
133. Rohn TT, Cusack SM, Kessinger SR, Oxford JT (2004) Caspase activation independent of cell death is required for proper cell dispersal and correct morphology in PC12 cells. Exp Cell Res 295:215-225 (Pubitemid 38407358)
134. Oomman S, Strahlendorf H, Dertien J, Strahlendorf J (2006) Bergmann glia utilize active caspase-3 for differentiation. Brain Res 1078:19-34
135. Campbell DS, Holt CE (2003) Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37:939-952 (Pubitemid 36401588)
136. Ohsawa S, Hamada S, Kuida K, Yoshida H, Igaki T, Miura M (2010) Maturation of the olfactory sensory neurons by Apaf-1/caspase-9-mediated caspase activity. Proc Natl Acad Sci U S A 107:13366-13371
137. Koto A, Kuranaga E, Miura M (2009) Temporal regulation of Drosophila IAP1 determines caspase functions in sensory organ development. J Cell Biol 187:219-231
138. Weber GF, Menko AS (2005) The canonical intrinsic mitochondrial death pathway has a non-apoptotic role in signaling lens cell differentiation. J Biol Chem 280:22135-22145 (Pubitemid 40827869)
139. Jiao S, Li Z (2011) Nonapoptotic function of Bad and Bax in long-term depression of synaptic transmission. Neuron 70:758-772
140. Ribeil JA, Zermati Y, Vandekerckhove J, Cathelin S, Kersual J, Dussiot M, Coulon S, Moura IC, Zeuner A, Kirkegaard-Sorensen T, Varet B, Solary E, Garrido C, Hermine O (2007) Hsp70 regulates erythropoiesis by preventing caspase-3-mediated cleavage of GATA-1. Nature 445:102-105 (Pubitemid 46067309)
141. Arama E, Agapite J, Steller H (2003) Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev Cell 4:687-697 (Pubitemid 36564899)
142. Plenchette S, Cathelin S, Rebe C, Launay S, Ladoire S, Sordet O, Ponnelle T, Debili N, Phan TH, Padua RA, Dubrez-Daloz L, Solary E (2004) Translocation of the inhibitor of apoptosis protein c-IAP1 from the nucleus to the Golgi in hematopoietic cells undergoing differentiation: a nuclear export signal-mediated event. Blood 104:2035-2043 (Pubitemid 39297854)
143. Kaplan Y, Gibbs-Bar L, Kalifa Y, Feinstein-Rotkopf Y, Arama E (2010) Gradients of a ubiquitin E3 ligase inhibitor and a caspase inhibitor determine differentiation or death in spermatids. Dev Cell 19:160-173
144. Arama E, Bader M, Rieckhof GE, Steller H (2007) A ubiquitin ligase complex regulates caspase activation during sperm differentiation in Drosophila. PLoS Biol 5:e251
145. Wright KM, Linhoff MW, Potts PR, Deshmukh M (2004) Decreased apoptosome activity with neuronal differentiation sets the threshold for strict IAP regulation of apoptosis. J Cell Biol 167:303-313 (Pubitemid 39435073)
146. Vyas S, Juin P, Hancock D, Suzuki Y, Takahashi R, Triller A, Evan G (2004) Differentiation-dependent sensitivity to apoptogenic factors in PC12 cells. J Biol Chem 279:30983-30993 (Pubitemid 39037757)
147. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K (2012) Stem cell marker (Nanog) and Stat-3 signaling promote microRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 31:149-160
148. Green DR, Evan GI (2002) A matter of life and death. Cancer Cell 1:19-30 (Pubitemid 41039172)
149. Lomonosova E, Chinnadurai G (2008) BH3-only proteins in apoptosis and beyond: an overview. Oncogene 27(Suppl 1):S2-S19
150. LeBrun DP, Warnke RA, Cleary ML (1993) Expression of Bcl-2 in fetal tissues suggests a role in morphogenesis. Am J Pathol 142:743-753 (Pubitemid 24063992)
151. Lu QL, Poulsom R,Wong L, Hanby AM (1993) Bcl-2 expression in adult and embryonic non-haematopoietic tissues. J Pathol 169:431-437 (Pubitemid 23128464)
152. Abe-Dohmae S, Harada N, Yamada K, Tanaka R (1993) Bcl-2 gene is highly expressed during neurogenesis in the central nervous system. Biochem Biophys Res Commun 191:915-921 (Pubitemid 23231577)
153. Merry DE, Veis DJ, Hickey WF, Korsmeyer SJ (1994) Bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120:301-311
154. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, Noda T, Kitamura Y, Kondoh H, Tsujimoto Y (1995) Bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res 55:354-359
155. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ (1993) Bcl-2- deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229-240 (Pubitemid 23320287)
156. Middleton G, Pinon LG, Wyatt S, Davies AM (1998) Bcl-2 accelerates the maturation of early sensory neurons. J Neurosci 18:3344-3350 (Pubitemid 28186026)
157. Bernier PJ, Parent A (1998) Bcl-2 protein as a marker of neuronal immaturity in postnatal primate brain. J Neurosci 18:2486-2497 (Pubitemid 28141797)
158. Zhang KZ, Westberg JA, Holtta E, Andersson LC (1996) Bcl2 regulates neural differentiation. Proc Natl Acad Sci U S A 93:4504-4508 (Pubitemid 26144316)
159. Wang S, Rosengren L, Hamberger A, Haglid K (2001) Antisense inhibition of Bcl-2 expression induces retinoic acid-mediated cell death during differentiation of human NT2N neurons. J Neurochem 76:1089-1098 (Pubitemid 32167383)
160. Niizuma H, Nakamura Y, Ozaki T, Nakanishi H, Ohira M, Isogai E, Kageyama H, Imaizumi M, Nakagawara A (2006) Bcl-2 is a key regulator for the retinoic acid-induced apoptotic cell death in neuroblastoma. Oncogene 25:5046-5055
161. Sato N, Hotta K, Waguri S, Nitatori T, Tohyama K, Tsujimoto Y, Uchiyama Y (1994) Neuronal differentiation of PC12 cells as a result of prevention of cell death by Bcl-2. J Neurobiol 25:1227-1234 (Pubitemid 24294763)
162. Suzuki A, Tsutomi Y (1998) Bcl-2 accelerates the neuronal differentiation: new evidence approaching to the biofunction of Bcl-2 in the neuronal system. Brain Res 801:59-66 (Pubitemid 28401646)
163. Eom DS, Choi WS, Oh YJ (2004) Bcl-2 enhances neurite extension via
164. Trouillas M, Saucourt C, Duval D, Gauthereau X, Thibault C, Dembele D, Feraud O, Menager J, Rallu M, Pradier L, Boeuf H (2008) Bcl-2, a transcriptional target of p38alpha, is critical for neuronal commitment of mouse embryonic stem cells. Cell Death Differ 15:1450-1459
165. Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, Lee CS, Adams LD, Gottlieb DI, Johnson EM Jr, Yu SP, Choi DW (2005) Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis 19:183-193 (Pubitemid 40544735)
166. Gonzalez-Garcia M, Garcia I, Ding L, O'Shea S, Boise LH, Thompson CB, Nunez G (1995) Bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc Natl Acad Sci U S A 92:4304-4308
167. Krajewska M, Mai JK, Zapata JM, Ashwell KW, Schendel SL, Reed JC, Krajewski S (2002) Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-x, Bax and Bak during development of murine nervous system. Cell Death Differ 9:145-157 (Pubitemid 34144774)
168. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S et al (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-1510
169. Parsadanian AS, Cheng Y, Keller-Peck CR, Holtzman DM, Snider WD (1998) Bcl-xL is an antiapoptotic regulator for postnatal CNS neurons. J Neurosci 18:1009-1019 (Pubitemid 28112923)
170. Liste I, Garcia-Garcia E, Martinez-Serrano A (2004) The generation of dopaminergic neurons by human neural stem cells is enhanced by Bcl-xL, both in vitro and in vivo. J Neurosci 24:10786-10795 (Pubitemid 39602390)
171. Shim JW, Koh HC, Chang MY, Roh E, Choi CY, Oh YJ, Son H, Lee YS, Studer L, Lee SH (2004) Enhanced in vitro midbrain dopamine neuron differentiation, dopaminergic function, neurite outgrowth, and 1-methyl-4-phenylpyridium resistance in mouse embryonic stem cells overexpressing Bcl-xL. J Neurosci 24:843-852 (Pubitemid 38146595)
172. Chang MY, Sun W, Ochiai W, Nakashima K, Kim SY, Park CH, Kang JS, Shim JW, Jo AY, Kang CS, Lee YS, Kim JS, Lee SH (2007) Bcl-xL/Bax proteins direct the fate of embryonic cortical precursor cells. Mol Cell Biol 27:4293-4305 (Pubitemid 46906554)
173. Savitt JM, Jang SS, MuW, Dawson VL, Dawson TM (2005) Bclx is required for proper development of the mouse substantia nigra. J Neurosci 25:6721-6728 (Pubitemid 41023139)
174. Liste I, Garcia-Garcia E, Bueno C, Martinez-Serrano A (2007) Bcl-xL modulates the differentiation of immortalized human neural stem cells. Cell Death Differ 14:1880-1892 (Pubitemid 350011664)
175. Sauvageot CM, Stiles CD (2002) Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12:244-249 (Pubitemid 34615748)
176. Vekrellis K, McCarthy MJ, Watson A, Whitfield J, Rubin LL, Ham J (1997) Bax promotes neuronal cell death and is down-regulated during the development of the nervous system. Development 124:1239-1249 (Pubitemid 27142077)
177. Guillemain I, Gaboyard S, Fontes G, Saunier M, Privat A, Patey G (2000) Differential expression of Bcl-2-related proteins in differentiating NT2 cells. Neuroreport 11:1421-1425 (Pubitemid 30365479)
178. Bunk E, König H-G, Bernas T, Engel T, Henshall D, Kirby B, Prehn J (2010) BH3-only proteins Bim and PUMA in the regulation of survival and neuronal differentiation of newly generated cells in the adult mouse hippocampus. Cell Death Dis 1:1-9
179. Waterhouse NJ, Sedelies KA, Browne KA, Wowk ME, Newbold A, Sutton VR, Clarke CJ, Oliaro J, Lindemann RK, Bird PI, Johnstone RW, Trapani JA (2005) A central role for Bid in granzyme B-induced apoptosis. J Biol Chem 280:4476-4482 (Pubitemid 40288613)
180. Wang T, Lee MH, Johnson T, Allie R, Hu L, Calabresi PA, Nath A (2010) Activated T-cells inhibit neurogenesis by releasing granzyme B: rescue by Kv1.3 blockers. J Neurosci 30:5020-5027