Gatekeeper Between Quiescence and Differentiation: p53 in Axonal Outgrowth and Neurogenesis

International Review of Neurobiology

Volumn 105, Issue , 2012, Pages 71-89

  Quadrato, Giorgia ^a   Di Giovanni, Simone ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Axonal regeneration; Cell cycle; Neural stem cells; Neurite outgrowth; Neurogenesis; P53

Indexed keywords

DNA; PROTEIN P53; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; AXONAL INJURY; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL FATE; CELL METABOLISM; CELL MIGRATION; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; DOWNSTREAM PROCESSING; EMBRYO DEVELOPMENT; HUMAN; MITOSIS; MOLECULAR MECHANICS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INJURY; NEURAL STEM CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; TUMOR SUPPRESSOR GENE;

EID: 84872369977     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-398309-1.00005-6     Document Type: Chapter

References (74)

1. Armesilla-Diaz A., Bragado P., Del Valle I., Cuevas E., Lazaro I., Martin C., et al. p53 regulates the self-renewal and differentiation of neural precursors. Neuroscience 2009, 158:1378-1389.
2. Armstrong J.F., Kaufman M.H., Harrison D.J., Clarke A.R. High-frequency developmental abnormalities in p53-deficient mice. Current Biology 1995, 5:931-936.
3. Avantaggiati M.L., Ogryzko V., Gardner K., Giordano A., Levine A.S., Kelly K. Recruitment of p300/CBP in p53-dependent signal pathways. Cell 1997, 89:1175-1184.
4. Baker S.J., Fearon E.R., Nigro J.M., Hamilton S.R., Preisinger A.C., Jessup J.M., et al. Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science 1989, 244:217-221.
5. Brooks C.L., Gu W. Ubiquitination, phosphorylation and acetylation: The molecular basis for p53 regulation. Current Opinion in Cell Biology 2003, 15:164-171.
6. Buss R.R., Oppenheim R.W. Role of programmed cell death in normal neuronal development and function. Anatomical Science International 2004, 79:191-197.
7. Cafferty W.B., Gardiner N.J., Das P., Qiu J., McMahon S.B., Thompson S.W. Conditioning injury-induced spinal axon regeneration fails in interleukin-6 knock-out mice. The Journal of Neuroscience 2004, 24:4432-4443.
8. Cafferty W.B., Gardiner N.J., Gavazzi I., Powell J., McMahon S.B., Heath J.K., et al. Leukemia inhibitory factor determines the growth status of injured adult sensory neurons. The Journal of Neuroscience 2001, 21:7161-7170.
9. Cicalese A., Bonizzi G., Pasi C.E., Faretta M., Ronzoni S., Giulini B., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 138:1083-1095.
10. Coutts A.S., Adams C.J., La Thangue N.B. p53 ubiquitination by Mdm2: A never ending tail?. DNA Repair 2009, 8:483-490.
11. Coutts A.S., Boulahbel H., Graham A., La Thangue N.B. Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Reports 2007, 8:84-90.
12. Croft D.R., Crighton D., Samuel M.S., Lourenco F.C., Munro J., Wood J., et al. p53-mediated transcriptional regulation and activation of the actin cytoskeleton regulatory RhoC to LIMK2 signaling pathway promotes cell survival. Cell Research 2011, 21:666-682.
13. Di Giovanni S. Regeneration following spinal cord injury, from experimental models to humans: Where are we?. Expert Opinion on Therapeutic Targets 2006, 10:363-376.
14. Di Giovanni S., Knights C.D., Rao M., Yakovlev A., Beers J., Catania J., et al. The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. The EMBO Journal 2006, 25:4084-4096.
15. Di Giovanni S., Rathore K. p53-dependent pathways in neurite outgrowth and axonal regeneration. Cell and Tissue Research 2012, 349:87-95.
16. Dziennis S., Alkayed N.J. Role of signal transducer and activator of transcription 3 in neuronal survival and regeneration. Reviews in the Neurosciences 2008, 19:341-361.
17. Eizenberg O., Faber-Elman A., Gottlieb E., Oren M., Rotter V., Schwartz M. p53 plays a regulatory role in differentiation and apoptosis of central nervous system-associated cells. Molecular and Cellular Biology 1996, 16:5178-5185.
18. El-Deiry W.S., Kern S.E., Pietenpol J.A., Kinzler K.W., Vogelstein B. Definition of a consensus binding site for p53. Nature Genetics 1992, 1:45-49.
19. Floriddia E., Nguyen T., Di Giovanni S. Chromatin immunoprecipitation from dorsal root ganglia tissue following axonal injury. Journal of Visualized Experiments 2011, 20(53). 10.3791/2803.
20. Floriddia E.M., Rathore K.I., Tedeschi A., Quadrato G., Wuttke A., Lueckmann J.M., Kigerl K.A., Popovich P.G., Di Giovanni S. p53 Regulates the Neuronal Intrinsic and Extrinsic Responses Affecting the Recovery of Motor Function following Spinal Cord Injury. Journal of Neuroscience 2012, 32(40):13956-13970. 10.1523/JNEUROSCI.1925-12.2012.
21. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Ferguson D.O., Zhu C., et al. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Molecular Cell 2000, 5:993-1002.
22. Gao Y., Ferguson D.O., Xie W., Manis J.P., Sekiguchi J., Frank K.M., et al. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 2000, 404:897-900.
23. Gaub P., Joshi Y., Wuttke A., Naumann U., Schnichels S., Heiduschka P., et al. The histone acetyltransferase p300 promotes intrinsic axonal regeneration. Brain 2011, 134:2134-2148.
24. Gaub P., Tedeschi A., Puttagunta R., Nguyen T., Schmandke A., Di Giovanni S. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death and Differentiation 2010, 17:1392-1408.
25. Gaub P., Tedeschi A., Puttagunta R., Nguyen T., Schmandke A., Di Giovanni S. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death and Differentiation 2010, 17:1392-1408.
26. Ghule P.N., Medina R., Lengner C.J., Mandeville M., Qiao M., Dominski Z., et al. Reprogramming the pluripotent cell cycle: Restoration of an abbreviated G1 phase in human induced pluripotent stem (iPS) cells. Journal of Cellular Physiology 2011, 226:1149-1156.
27. Gil-Perotin S., Marin-Husstege M., Li J., Soriano-Navarro M., Zindy F., Roussel M.F., et al. Loss of p53 induces changes in the behavior of subventricular zone cells: Implication for the genesis of glial tumors. The Journal of Neuroscience 2006, 26:1107-1116.
28. Gottlieb E., Haffner R., King A., Asher G., Gruss P., Lonai P., et al. Transgenic mouse model for studying the transcriptional activity of the p53 protein: Age- and tissue-dependent changes in radiation-induced activation during embryogenesis. The EMBO Journal 1997, 16:1381-1390.
29. Gregorian C., Nakashima J., Le Belle J., Ohab J., Kim R., Liu A., et al. Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. The Journal of Neuroscience 2009, 29:1874-1886.
30. Groszer M., Erickson R., Scripture-Adams D.D., Dougherty J.D., Le Belle J., Zack J.A., et al. PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:111-116.
31. Harms K., Nozell S., Chen X. The common and distinct target genes of the p53 family transcription factors. Cellular and Molecular Life Sciences 2004, 61:822-842.
32. Kippin T.E., Martens D.J., van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes & Development 2005, 19:756-767.
33. Komarova E.A., Chernov M.V., Franks R., Wang K., Armin G., Zelnick C.R., et al. Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. The EMBO Journal 1997, 16:1391-1400.
34. Koster M.I., Kim S., Mills A.A., DeMayo F.J., Roop D.R. p63 is the molecular switch for initiation of an epithelial stratification program. Genes & Development 2004, 18:126-131.
35. Kuan C.Y., Roth K.A., Flavell R.A., Rakic P. Mechanisms of programmed cell death in the developing brain. Trends in Neurosciences 2000, 23:291-297.
36. Lane D.P. Cancer. p53, guardian of the genome. Nature 1992, 358:15-16.
37. Lavin M.F., Gueven N. The complexity of p53 stabilization and activation. Cell Death and Differentiation 2006, 13:941-950.
38. Lill N.L., Grossman S.R., Ginsberg D., DeCaprio J., Livingston D.M. Binding and modulation of p53 by p300/CBP coactivators. Nature 1997, 387:823-827.
39. Lin J., Tang H., Jin X., Jia G., Hsieh J.T. p53 regulates Stat3 phosphorylation and DNA binding activity in human prostate cancer cells expressing constitutively active Stat3. Oncogene 2002, 21:3082-3088.
40. Liu L., Scolnick D.M., Trievel R.C., Zhang H.B., Marmorstein R., Halazonetis T.D., et al. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Molecular and Cellular Biology 1999, 19:1202-1209.
41. Louis J.M., McFarland V.W., May P., Mora P.T. The phosphoprotein p53 is down-regulated post-transcriptionally during embryogenesis in vertebrates. Biochimica et Biophysica Acta 1988, 950:395-402.
42. Ma X., Fei E., Fu C., Ren H., Wang G. Dysbindin-1, a schizophrenia-related protein, facilitates neurite outgrowth by promoting the transcriptional activity of p53. Molecular Psychiatry 2011, 16:1105-1116.
43. Macleod K.F., Hu Y., Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. The EMBO Journal 1996, 15:6178-6188.
44. Marion R.M., Strati K., Li H., Murga M., Blanco R., Ortega S., et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009, 460:1149-1153.
45. Meletis K., Wirta V., Hede S.M., Nister M., Lundeberg J., Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development (Cambridge, England) 2006, 133:363-369.
46. Miller F.D., Kaplan D.R. On Trk for retrograde signaling. Neuron 2001, 32:767-770.
47. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., et al. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301.
48. Murray-Zmijewski F., Slee E.A., Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nature Reviews. Molecular Cell Biology 2008, 9:702-712.
49. Paulson M., Pisharody S., Pan L., Guadagno S., Mui A.L., Levy D.E. Stat protein transactivation domains recruit p300/CBP through widely divergent sequences. Journal of Biological Chemistry 1999, 274:25343-25349.
50. Poluha W., Schonhoff C.M., Harrington K.S., Lachyankar M.B., Crosbie N.E., Bulseco D.A., et al. A novel, nerve growth factor-activated pathway involving nitric oxide, p53, and p21WAF1 regulates neuronal differentiation of PC12 cells. Journal of Biological Chemistry 1997, 272:24002-24007.
51. Pozniak C.D., Radinovic S., Yang A., McKeon F., Kaplan D.R., Miller F.D. An anti-apoptotic role for the p53 family member, p73, during developmental neuron death. Science 2000, 289:304-306.
52. Qin Q., Baudry M., Liao G., Noniyev A., Galeano J., Bi X. A novel function for p53: Regulation of growth cone motility through interaction with Rho kinase. The Journal of Neuroscience 2009, 29:5183-5192.
53. Qin Q., Liao G., Baudry M., Bi X. Role of calpain-mediated p53 truncation in semaphorin 3A-induced axonal growth regulation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:13883-13887.
54. Qiu J., Cafferty W.B., McMahon S.B., Thompson S.W. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. The Journal of Neuroscience 2005, 25:1645-1653.
55. Qiu J., Takagi Y., Harada J., Rodrigues N., Moskowitz M.A., Scadden D.T., et al. Regenerative response in ischemic brain restricted by p21cip1/waf1. The Journal of Experimental Medicine 2004, 199:937-945.
56. Riley T., Sontag E., Chen P., Levine A. Transcriptional control of human p53-regulated genes. Nature Reviews. Molecular Cell Biology 2008, 9:402-412.
57. Rogel A., Popliker M., Webb C.G., Oren M. p53 cellular tumor antigen: Analysis of mRNA levels in normal adult tissues, embryos, and tumors. Molecular and Cellular Biology 1985, 5:2851-2855.
58. Rowland B.D., Bernards R., Peeper D.S. The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nature Cell Biology 2005, 7:1074-1082.
59. Schmid P., Lorenz A., Hameister H., Montenarh M. Expression of p53 during mouse embryogenesis. Development (Cambridge, England) 1991, 113:857-865.
60. Schmidt H., Werner M., Heppenstall P.A., Henning M., More M.I., Kuhbandner S., et al. cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. The Journal of Cell Biology 2002, 159:489-498.
61. Schwaiger F.W., Hager G., Schmitt A.B., Horvat A., Streif R., Spitzer C., et al. Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). European Journal of Neuroscience 2000, 12:1165-1176.
62. Sola S., Xavier J.M., Santos D.M., Aranha M.M., Morgado A.L., Jepsen K., et al. p53 interaction with JMJD3 results in its nuclear distribution during mouse neural stem cell differentiation. PLoS One 2011, 6:e18421.
63. Tedeschi A., Di Giovanni S. The non-apoptotic role of p53 in neuronal biology: Enlightening the dark side of the moon. EMBO Reports 2009, 10:576-583.
64. Tedeschi A., Nguyen T., Puttagunta R., Gaub P., Di Giovanni S. A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth, and regeneration. Cell Death and Differentiation 2009, 16:543-554.
65. Tedeschi A., Nguyen T., Steele S.U., Feil S., Naumann U., Feil R., et al. The tumor suppressor p53 transcriptionally regulates cGKI expression during neuronal maturation and is required for cGMP-dependent growth cone collapse. The Journal of Neuroscience 2009, 29:15155-15160.
66. van Lookeren Campagne M., Gill R. 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. The Journal of Comparative Neurology 1998, 397:181-198.
67. Vogel K.S., Parada L.F. Sympathetic neuron survival and proliferation are prolonged by loss of p53 and neurofibromin. Molecular and Cellular Neurosciences 1998, 11:19-28.
68. Wang R., Cherukuri P., Luo J. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. Journal of Biological Chemistry 2005, 280:11528-11534.
69. Wong K., Zhang J., Awasthi S., Sharma A., Rogers L., Matlock E.F., et al. Nerve growth factor receptor signaling induces histone acetyltransferase domain-dependent nuclear translocation of p300/CREB-binding protein-associated factor and hGCN5 acetyltransferases. Journal of Biological Chemistry 2004, 279:55667-55674.
70. Yoon H.S., Chen X., Yang V.W. Kruppel-like factor 4 mediates p53-dependent G1/S cell cycle arrest in response to DNA damage. Journal of Biological Chemistry 2003, 278:2101-2105.
71. Zhang W., Geiman D.E., Shields J.M., Dang D.T., Mahatan C.S., Kaestner K.H., et al. The gut-enriched Kruppel-like factor (Kruppel-like factor 4) mediates the transactivating effect of p53 on the p21WAF1/Cip1 promoter. Journal of Biological Chemistry 2000, 275:18391-18398.
72. Zhang X.M., Li Q.M., Su D.J., Wang N., Shan Z.Y., Jin L.H., et al. RA induces the neural-like cells generated from epigenetic modified NIH/3T3 cells. Molecular Biology Reports 2010, 37:1197-1202.
73. Zheng H., Ying H., Yan H., Kimmelman A.C., Hiller D.J., Chen A.J., et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455:1129-1133.
74. Zhu Y., Mao X.O., Sun Y., Xia Z., Greenberg D.A. p38 Mitogen-activated protein kinase mediates hypoxic regulation of Mdm2 and p53 in neurons. Journal of Biological Chemistry 2002, 277:22909-22914.