RP58 controls neuron and astrocyte differentiation by downregulating the expression of Id1-4 genes in the developing cortex

EMBO Journal

Volumn 31, Issue 5, 2012, Pages 1190-1202

  Hirai, Shinobu ^a,b   Miwa, Akiko ^a   Ohtaka Maruyama, Chiaki ^a   Kasai, Masataka ^c   Okabe, Shigeo ^d   Hata, Yutaka ^b   Okado, Haruo ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

cell cycle control; cortical development; cyclin dependent kinase inhibitor; fate of NSCs; p57

Indexed keywords

BETA ACTIN; CELL PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; INHIBITOR OF DIFFERENTIATION PROTEIN; PROTEIN P57; PROTEIN RP58; PROTEIN TUJ1; TRANSCRIPTION FACTOR RP58; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROGENESIS; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE; CELL CYCLE REGULATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; CORTICOGENESIS; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GLIA CELL; ID1 GENE; ID2 GENE; ID3 GENE; ID4 GENE; KNOCKOUT MOUSE; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; P57 GENE; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; WILD TYPE;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CEREBRAL CORTEX; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; INHIBITOR OF DIFFERENTIATION PROTEINS; MICE; MICE, KNOCKOUT; NEURONS; REPRESSOR PROTEINS;

MUS;

EID: 84857995198     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.486     Document Type: Article

References (81)

1. Aoki K, Meng G, Suzuki K, Takashi T, Kameoka Y, Nakahara K, Ishida R, Kasai M (1998) RP58 associates with condensed chromatin and mediates a sequence-specific transcriptional repression. J Biol Chem 273: 26698-26704 (Pubitemid 28471685)
2. Baek SH, Kioussi C, Briata P, Wang D, Nguyen HD, Ohgi KA, Glass CK, Wynshaw-Boris A, Rose DW, Rosenfeld MG (2003) Regulated subset of G1 growth-control genes in response to derepression by the Wnt pathway. Proc Natl Acad Sci USA 100: 3245-3250 (Pubitemid 36356568)
3. Bedford L, Walker R, Kondo T, van Crüchten I, King ER, Sablitzky F (2005) Id4 is required for the correct timing of neural differentiation. Dev Biol 280: 386-395 (Pubitemid 40692139)
4. Berse M, Bounphengb M, Huanga X, Christyc B, Pollmanna C, Dubie W (2004) Ubiquitin-dependent degradation of Id1 and Id3 is mediated by the COP9 signalosome. J Mol Biol 343: 361-370 (Pubitemid 39296871)
5. Besson A, Dowdy SF, Roberts JM (2008) CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14: 159-169 (Pubitemid 351189186)
6. Burdon T, Smith A, Savatier P (2002) Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 12: 432-438 (Pubitemid 35239952)
7. Cai L, Morrow EM, Cepko CL (2000) Misexpression of basic helix-loop-helix genes in the murine cerebral cortex affects cell fate choices and neuronal survival. Development 127: 3021-3030 (Pubitemid 30611895)
8. Cánepa ET, Scassa ME, Ceruti JM, Marazita MC, Carcagno AL, Sirkin PF, Ogara MF (2007) INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 59: 419-426 (Pubitemid 47123998)
9. Canzoniere D, Farioli-Vecchioli S, Conti F, Ciotti MT, Tata AM, Augusti-Tocco G, Mattei E, Lakshmana MK, Krizhanovsky V, Reeves SA, Giovannoni R, Castano F, Servadio A, Ben-Arie N, Tirone F (2004) Dual control of neurogenesis by PC3 through cell cycle inhibition and induction of Math1. J Neurosci 24: 3355-3369 (Pubitemid 38451901)
10. Ciarapica R, Annibalid D, Raimondi L, Savino M, Nasi S, Rota R (2009) Targeting Id protein interactions by an engineered HLH domain induces human neuroblastoma cell differentiation. Oncogene 28: 1881-1891
11. Dahlquist KD, Salomonis N, Vranizan K, Lawlor SC, Conklin BR (2002) GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat Genet 31: 19-20
12. Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nature Rev Neuro 8: 438-450 (Pubitemid 46789227)
13. Doniger SW, Salomonis N, Dahlquist KD, Vranizan K, Lawlor SC, Conklin BR (2003) MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 4: R7
14. Dyer MA, Cepko CL (2000) p57 (Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development 127: 3593-3605
15. Ess KC (2010) Tuberous sclerosis complex: a brave new world? Curr Opin Neurol 23: 189-193
16. Favaro R, Valotta M, Ferri AL, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V (2009) Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci 12: 1248-1256
17. Friocourt G, Kanatani S, Tabata H, Yozu M, Takahashi T, Antypa M, Raguénès O, Chelly J, Férec C, Nakajima K, Parnavelas JG (2008) Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J Neurosci 28: 5794-5805
18. Fluckiger AC, Marcy G, Marchand M, Négre D, Cosset FL, Mitalipov S, Wolf D, Savatier P, Dehay C (2006) Cell cycle features of primate embryonic stem cells. Stem Cells 24: 547-556 (Pubitemid 44464758)
19. Fong S, Debs RJ, Desprez PY (2004) Id genes and proteins as promising targets in cancer therapy. Trends Mol Med 10: 387-392 (Pubitemid 39061140)
20. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J 20: 2536-2544 (Pubitemid 32452872)
21. Gui H, Li S, Matise MP (2007) A cell-autonomous requirement for Cip/Kip cyclin-kinase inhibitors in regulating neuronal cell cycle exit but not differentiation in the developing spinal cord. Dev Biol 301: 14-26 (Pubitemid 44958402)
22. Guillemot F (2007) Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83: 37-52
23. Hanawa H, Yamamoto M, Zhao H, Shimada T, Persons DA (2009) Optimized lentiviral vector design improves titer and transgene expression of vectors containing the chicken beta-globin locus HS4 insulator element. Mol Ther 17: 667-674
24. Iavarone A, Garg P, Lasorella A, Hsu J, Israel MA (1994) The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev 8: 1270-1284
25. Jen Y, Manova K, Benezra R (1996) Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn 207: 235-252 (Pubitemid 26378326)
26. Jen Y, Manova K, Benezra R (1997) Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev Dyn 208: 92-106 (Pubitemid 27030487)
27. Jeon HM, Jin X, Lee JS (2008) Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling. Genes Dev 22: 2028-2033
28. Joseph B, Hermanson O (2010) Molecular control of brain size: regulators of neural stem cell life, death and beyond. Exp Cell Res 316: 1415-1421
29. Jung S, Park RH, Kim S, Jeon YJ, Ham DS, Jung MY, Kim SS, Lee YD, Park CH, Suh-Kim H (2010) Id proteins facilitate self-renewal and proliferation of neural stem cells. Stem Cells Dev 19: 831-841
30. Katsimpardi L, Gaitanou M, Malnou CE, Lledo PM, Charneau P, Matsas R, Thomaidou D (2008) BM88/Cend1 expression levels are critical for proliferation and differentiation of subventricular zone-derived neural precursor cells. Stem Cells 26: 1796-1807
31. Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, Herman T, Ohgi KA, Lin C, Gleiberman A, Wang J, Brault V, Ruiz-Lozano P, Nguyen HD, Kemler R, Glass CK, Wynshaw-Boris A, Rosenfeld MG (2002) Identification of a Wnt/Dvl/β-Catenin → Pitx2 pathway mediating cell-type specific proliferation during development. Cell 111: 673-685 (Pubitemid 35441249)
32. Kuzontkoski PM, Mulligan-Kehoe MJ, Harris BT, Israel MA (2010) Inhibitor of DNA binding-4 promotes angiogenesis and growth of glioblastoma multiforme by elevating matrix GLA levels. Oncogene 29: 3793-3802
33. Langlands K, Yin X, Anand G, Prochownik EV (1997) Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J Biol Chem 272: 19785-19793 (Pubitemid 27340071)
34. Lasorella A, Stegmüller J, Guardavaccaro D, Liu G, Carro MS, Rothschild G, de la Torre-Ubieta L, Pagano M, Bonni A, Iavarone A (2006) Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442: 471-474 (Pubitemid 44264798)
35. Lasorella A, Uo T, Iavarone A (2001) Id proteins at the cross-road of development and cancer. Oncogene 20: 8326-8333 (Pubitemid 34121903)
36. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47: 353-364 (Pubitemid 41073877)
37. Lukaszewicz A, Savatier P, Cortay V, Kennedy H, Dehay C (2002) Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J Neurosci 22: 6610-6622 (Pubitemid 35386417)
38. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401: 670-677
39. Miller FD, Gauthier AS (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54: 357-369 (Pubitemid 46659814)
40. Nagata Y, Todokoro K (1994) Activation of helix-loop-helix proteins Id1, Id2 and Id3 during neural differentiation. Biochem Biophys Res Commun 199: 1355-1362 (Pubitemid 24174808)
41. Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T (2001) BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci USA 98: 5868-5873 (Pubitemid 32435734)
42. Napolioni V, Moavero R, Curatolo P (2009) Recent advances in neurobiology of tuberous sclerosis complex. Brain Dev 31: 104113
43. Neganova I, Lako M (2008) G1 to S phase cell cycle transition in somatic and embryonic stem cells. J Anat 213: 30-44 (Pubitemid 352044393)
44. Nguyen L, Besson A, Heng JI, Schuurmans C, Teboul L, Parras C, Philpott A, Roberts JM, Guillemot F (2006) p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev 20: 1511-1524 (Pubitemid 43830657)
45. Ohtaka-Maruyama C, Miwa A, Kawano H, Kasai M, Okado H (2007) Spatial and temporal expression of RP58, a novel zinc finger transcriptional repressor, in mouse brain. J Comp Neurol 502: 1098-1108 (Pubitemid 46806638)
46. INK4a expression during cellular senescence. Nature 409: 1067-1070
47. Okado H, Ohtaka-Maruyama C, Sugitani Y, Fukuda Y, Ishida R, Hirai S, Miwa A, Takahashi A, Aoki K, Mochida K, Suzuki O, Honda T, Nakajima K, Ogawa M, Terashima T, Matsuda J, Kawano H, Kasai M (2009) The transcriptional repressor RP58 is crucial for cell-division patterning and neuronal survival in the developing cortex. Dev Biol 331: 140-151
48. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, Wechsler-Reya RJ (2003) Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 100: 7331-7336 (Pubitemid 36706438)
49. Pagliuca A, Gallo P, De Luca P, Lania L (2000) Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res 60: 1376-1382 (Pubitemid 30152010)
50. Pan L, Sato S, Frederick JP, Sun XH, Zhuang Y (1999) Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol Cell Biol 19: 5969-5980 (Pubitemid 29399302)
51. Passiatore G, Gentilella A, Rom S, Pacifici M, Bergonzini V, Peruzzi F (2011) Induction of Id-1 by FGF-2 involves activity of EGR-1 and sensitizes neuroblastoma cells to cell death. J Cell Physiol 7: 1763-1770
52. Pateras IS, Apostolopoulou K, Niforou K, Kotsinas A, Gorgoulis VG (2009) p57KIP2: "Kip"ing the cell under control. Mol Cancer Res 27: 1902-1919
53. Pereira JD, Sansom SN, Smith J, Dobenecker MW, Tarakhovsky A, Livesey FJ (2010) Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci USA 107: 15957-15962
54. Perk J, Iavarone A, Benezra R (2005) Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 5: 603-614 (Pubitemid 41081386)
55. Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N, Kennedy H, Dehay C (2009) Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci USA 106: 21924-21929
56. Polleux F, Dehay C, Moraillon B, Kennedy H (1997) Regulation of neuroblast cell-cycle kinetics plays a crucial role in the generation of unique features of neocortical areas. J Neurosci 17: 7763-7783 (Pubitemid 27426215)
57. Prabhu S, Ignatova A, Park ST, Sun XH (1997) Regulation of expression of the cyclin dependent kinase inhibitor p21 by E2A and Id proteins. Mol Cell Biol 17: 5888-5896 (Pubitemid 27411095)
58. Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28: 69-80
59. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55: 165-177 (Pubitemid 46036463)
60. Kip2 to regulate cell cycle in neural cells. Mol Cell Biol 26: 4351-4361
61. Sakai K, Peraud A, Mainprize T, Nakayama J, Tsugu A, Hongo K, Kobayashi S, Rutka JT (2004) Inducible expression of p57KIP2 inhibits glioma cell motility and invasion. J Neurooncol 68: 217-223 (Pubitemid 38878255)
62. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9: 743-751
63. Sosunov AA, Wu X, Weiner HL, Mikell CB, Goodman RR, Crino PD, McKhann II GM (2008) Tuberous sclerosis: a primary pathology of astrocytes? Epilepsia 49: 53-62 (Pubitemid 351143766)
64. Sugitani Y, Nakai S, Minowa O, Nishi M, Jishage K, Kawano H, Mori K, Ogawa M, Noda T (2002) Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev 16: 1760-1765 (Pubitemid 34803892)
65. Sun XH, Copeland NG, Jenkins NA, Baltimore D (1991) Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 11: 5603-5611 (Pubitemid 21895327)
66. Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103: 865-872 (Pubitemid 32289300)
67. Takahashi A, Hirai S, Ohtaka-Maruyama C, Miwa A, Hata Y, Okabe S, Okado H (2008) Co-localization of a novel transcriptional repressor simiRP58 with RP58. Biochem Biophys Res Commun 368: 637-642
68. Takahashi T, Nowakowski RS, Caviness Jr VS (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15: 6046-6057
69. Tatard VM, Xiang C, Biegel JA, Dahmane N (2010) ZNF238 is expressed in postmitotic brain cells and inhibits brain tumor growth. Cancer Res 70: 1236-1246
70. KIP1 play a role in Id2-induced proliferation and tumorigenesis. Carcinogenesis 30: 1252-1259
71. Tsugu A, Sakai K, Dirks PB, Jung S, Weksberg R, Fei YL, Mondal S, Ivanchuk S, Ackerley C, Hamel PA, Rutka JT (2000) Expression of p57(KIP2) potently blocks the growth of human astrocytomas and induces cell senescence. Am J Pathol 157: 919-932 (Pubitemid 32109384)
72. Tury A, Mairet-Coello G, Dicicco-Bloom E (2011) The cyclin-dependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb Cortex 21: 1840-1856
73. Tzeng SF (2003) Inhibitors of DNA binding in neural cell proliferation and differentiation. Neurochem Res 28: 45-52
74. Tzeng SF, de Vellis J (1998) Id1, Id2, and Id3 gene expression in neural cells during development. Glia 24: 372-381
75. Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y (1997) High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol Cell Biol 17: 7317-7327 (Pubitemid 27505961)
76. Yates PR, Atherton GT, Deed RW, Norton JD, Sharrocks AD (1999) Id helix-loop-helix proteins inhibit nucleoprotein complex formation by the TCF ETS-domain transcription factors. EMBO J 18: 968-976 (Pubitemid 29082276)
77. Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S, Nishikawa S, Gruss P (1999) Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397: 702-706
78. Yokoyama S, Ito Y, Ueno-Kudoh H, Shimizu H, Uchibe K, Albini S, Mitsuoka K, Miyaki S, Kiso M, Nagai A, Hikata T, Osada T, Fukuda N, Yamashita S, Harada D, Mezzano V, Kasai M, Puri PL, Hayashizaki Y, Okado H et al (2009) A systems approach reveals that the myogenesis genome network is regulated by the transcriptional repressor RP58. Dev Cell 17: 836-848
79. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA (2004) Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131: 5441-5448 (Pubitemid 39562186)
80. Zeng W, Rushing EJ, Hartmann DP, Azumi N (2010) Increased inhibitor of differentiation 4 (Id4) expression in glioblastoma: a tissue microarray study. J Cancer 1: 1-5
81. INK4a expression by Id1 and E47 proteins in human diploId fibroblast. J Biol Chem 279: 31524-31532