p63 regulates adult neural precursor and newly born neuron survival to control hippocampal-dependent behavior

Journal of Neuroscience

Volumn 33, Issue 31, 2013, Pages 12569-12585

  Cancino, Gonzalo I ^a   Yiu, Adelaide P ^a   Fatt, Michael P ^a,b   Dugani, Chandrasagar B ^a,b   Flores, Elsa R ^c   Frankland, Paul W ^a,b   Josselyn, Sheena A ^a,b   Miller, Freda D ^a,b   Kaplan, David R ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CASPASE; CASPASE 3; CRE RECOMBINASE; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN P53; PROTEIN P63; PUMA PROTEIN; TRANSCRIPTION FACTOR SOX2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; COGNITION; CONTROLLED STUDY; EMBRYO; FEAR; FEMALE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NICK END LABELING; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPATIAL MEMORY; TASK PERFORMANCE;

ADULT STEM CELLS; ANIMALS; BROMODEOXYURIDINE; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL VENTRICLES; CONDITIONING (PSYCHOLOGY); CUES; EXPLORATORY BEHAVIOR; FEAR; HIPPOCAMPUS; INTERMEDIATE FILAMENT PROTEINS; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NESTIN; NEURAL STEM CELLS; NEUROGENESIS; PHOSPHOPROTEINS; PROTEINS; RNA, UNTRANSLATED; TAMOXIFEN; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84880780596     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1251-13.2013     Document Type: Article

References (50)

1. Arruda-Carvalho M, Sakaguchi M, Akers KG, Josselyn SA, Frankland PW (2011) Posttraining ablation of adult-generated neurons degrades previously acquired memories. J Neurosci 31:15113-15127. CrossRef Medline
2. Biernaskie JA, McKenzie IA, Toma JG, Miller FD (2006) Isolation of skinderived precursors (SKPs) and differentiation and enrichment of their Schwann cell progeny. Nat Protoc 1:2803-2812. CrossRef Medline
3. Brunner HG, Hamel BC, Van BokhovenH (2002) The p63 gene in EEC and other syndromes. J Med Genet 39:377-381. CrossRef Medline
4. Bunk EC, König HG, Bernas T, Engel T, Henshall DC, Kirby BP, Prehn JH (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:e15. CrossRef Medline
5. Cancino GI, Toledo EM, Leal NR, Hernandez DE, Yévenes LF, Inestrosa NC, Alvarez AR (2008) STI571 prevents apoptosis, tau phosphorylation and behavioural impairments induced by Alzheimer's beta-amyloid deposits. Brain 131:2425-2442. CrossRef Medline
6. Cancino GI, Miller FD, KaplanDR (2013) p73 haploinsufficiency causes tau hyperphosphorylation and tau kinase dysregulation in mouse models of aging and Alzheimer's disease. Neurobiol Aging 34:387-399. CrossRef Medline
7. de Hoz L, Martin SJ, Morris RG (2004) Forgetting, reminding, and remembering: the retrieval of lost spatial memory. PLoS Biol 2:E225. CrossRef Medline
8. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29:13532-13542. CrossRef Medline
9. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339-350. CrossRef Medline
10. Dötsch V, Bernassola F, Coutandin D, Candi E, Melino G (2010) p63 and p73, the ancestors of p53. Cold Spring Harb Perspect Biol 2:a004887. CrossRef Medline
11. Dugani CB, Paquin A, Fujitani M, Kaplan DR, Miller FD (2009) p63 antagonizes p53 to promote the survival of embryonic neural precursor cells. J Neurosci 29:6710-6721. CrossRef Medline
12. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P, Abrous DN, Piazza PV (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3:e1959. CrossRef Medline
13. Flores ER (2011) p73 is critical for the persistence of memory. Cell Death Differ 18:381-382. CrossRef Medline
14. Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, Silva AJ (2004) Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14:557-569. CrossRef Medline
15. 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. CrossRef Medline
16. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4:e5464. CrossRef Medline
17. 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. CrossRef Medline
18. Guo W, Allan AM, Zong R, Zhang L, Johnson EB, Schaller EG, Murthy AC, Goggin SL, Eisch AJ, Oostra BA, Nelson DL, Jin P, Zhao X (2011) Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat Med 17:559-565. CrossRef Medline
19. 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. CrossRef Medline
20. 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. CrossRef Medline
21. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161. CrossRef Medline
22. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1-7. CrossRef Medline
23. Keyes WM, Wu Y, Vogel H, Guo X, Lowe SW, Mills AA (2005) p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes Dev 19:1986-1999. CrossRef Medline
24. Kiernan MJ, Westbrook RF (1993) Effects of exposure to a to-be-shocked environment upon the rat's freezing response: evidence for facilitation, latent inhibition, and perceptual learning. Q J Exp Psychol B 46:271-288. Medline
25. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677. CrossRef Medline
26. Koster MI, Kim S, Roop DR (2005) p63 deficiency: a failure of lineage commitment or stem cell maintenance? J Investig Dermatol Symp Proc 10: 118-123. CrossRef Medline
27. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ, Greer CA, Mandyam CD, Eisch AJ (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci 27:12623-12629. CrossRef Medline
28. Liu D, Ou L, Clemenson GD Jr, Chao C, Lutske ME, Zambetti GP, Gage FH, Xu Y (2010) Puma is required for p53-induced depletion of adult stem cells. Nat Cell Biol 12:993-998. CrossRef Medline
29. Maei HR, Zaslavsky K, Teixeira CM, FranklandPW (2009) What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 3:4. CrossRef Medline
30. Malone CD, Hasan SM, Roome RB, Xiong J, Furlong M, Opferman JT, Vanderluit JL (2012) Mcl-1 regulates the survival of adult neural precursor cells. Mol Cell Neurosci 49:439-447. CrossRef Medline
31. Matus-Amat P, Higgins EA, Barrientos RM, Rudy JW (2004) The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 24:2431-2439. CrossRef Medline
32. Meletis K, Wirta V, Hede SM, Nistér M, Lundeberg J, Frisén J (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133: 363-369. CrossRef Medline
33. 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. CrossRef Medline
34. Mills AA, Qi Y, Bradley A (2002) Conditional inactivation of p63 by Cremediated excision. Genesis 32:138-141. CrossRef Medline
35. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702. CrossRef Medline
36. Moser E, Moser MB, Andersen P (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13:3916-3925. Medline
37. Moser MB, Moser EI (1998) Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci 18:7535-7542. Medline
38. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188-201. CrossRef Medline
39. Pozniak CD, Barnabé-Heider F, Rymar VV, Lee AF, Sadikot AF, Miller FD (2002) p73 is required for survival and maintenance of CNS neurons. J Neurosci 22:9800-9809. Medline
40. Rudy JW, Huff NC, Matus-Amat P (2004) Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev 28:675-685. CrossRef Medline
41. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 103:17501-17506. CrossRef Medline
42. Su X, Paris M, Gi YJ, Tsai KY, Cho MS, Lin YL, Biernaskie JA, Sinha S, Prives C, Pevny LH, Miller FD, Flores ER (2009) TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 5:64-75. CrossRef Medline
43. Sun Y, Zhang Y, Wang X, Blomgren K, Zhu C (2012) Apoptosis-inducing factor downregulation increased neuronal progenitor, but not stem cell, survival in the neonatal hippocampus after cerebral hypoxiaischemia. Mol Neurodegener 7:17. CrossRef Medline
44. Talos F, Abraham A, Vaseva AV, Holembowski L, Tsirka SE, Scheel A, Bode D, Dobbelstein M, Brück 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. CrossRef Medline
45. Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW (2006) Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci 26:7555-7564. CrossRef Medline
46. Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, Goffinet AM (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci U S A 106:16871-16876. CrossRef Medline
47. Westfall MD, Mays DJ, Sniezek JC, Pietenpol JA (2003) The Delta Np63 alpha phosphoprotein binds the p21 and 14-3-3 sigma promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Mol Cell Biol 23:2264-2276. CrossRef Medline
48. WetzelMK, Naska S, Laliberté CL, Rymar VV, FujitaniM, Biernaskie JA, Cole CJ, Lerch JP, Spring S, Wang SH, Frankland PW, Henkelman RM, Josselyn SA, Sadikot AF, Miller FD, KaplanDR (2008) p73 regulates neurodegeneration and phospho-tau accumulation during aging and Alzheimer's disease. Neuron 59:708-721. CrossRef Medline
49. Yang A, McKeon F (2000) P63 and P73: P53 mimics, menaces and more. Nat Rev Mol Cell Biol 1:199-207. CrossRef Medline
50. Yiu AP, Rashid AJ, Josselyn SA (2011) Increasing CREB function in the CA1 region of dorsal hippocampus rescues the spatial memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 36: 2169-2186. CrossRef Medline