Novel functions for cell cycle genes in nervous system development

Cell Cycle

Volumn 5, Issue 14, 2006, Pages 1506-1513

  McClellan, Kelly A ^a   Slack, Ruth S ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Cell cycle; Neurogenesis; Neuronal differentiation; Neuronal migration; Retinoblastoma

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN; CYCLIN D1; CYCLIN D2; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; GEMININ; PROTEIN; PROTEIN BMI 1; PROTEIN P107; PROTEIN P16INK4A; PROTEIN P57; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F3; UNCLASSIFIED DRUG;

APOPTOSIS; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; GENE FUNCTION; MEDICAL RESEARCH; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REGULATOR GENE; REVIEW;

EID: 33746268106     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.14.2980     Document Type: Review

References (74)

1. Angevine JB, Sidman RL. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 1961; 192:766-8.
2. McConnell SK. Development and decision-making in the mammalian cerebral cortex. Brain Res 1988; 472:1-23.
3. McConnell SK, Kaznowski CE. Cell cycle dependence of laminar determination in developing neocortex. Science 1991; 254:282-5.
4. Wald DK, McLoon SC. Immediate differentiation of ganglion cells following mitosis in the developing retina. Neuron 1995; 14:117-24.
5. Sanchez I, Dynlacht BD. New insights into cyclins, CDKs, and cell cycle control. Semin Cell Dev Biol 2005; 16:311-21.
6. Dimova DK, Dyson NJ. The E2F transcriptional network: Old acquaintances with new faces. Oncogene 2005; 24:2810-26.
7. Attwooll C, Lazzerini Denchi E, Helin K. The E2F family: Specific functions and overlapping interests. EMBO J 2004; 23:4709-16.
8. Classon M, Harlow E. The retinoblastoma tumour suppressor in development and cancer. Nat Rev Cancer 2002; 2:910-7.
9. Trimarchi JM, Lees JA. Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 2002; 3:11-20.
10. Nevins JR. The Rb/E2F pathway and cancer. Hum Mol Genet 2001; 10:699-703.
11. Vanderluit JL, Ferguson KL, Slack RS. Emerging roles for the Retinoblastoma gene family. In: Fanciulli M, ed. Rb and Tumorigenesis: Landes Bioscience, 2006:81-105.
12. Christensen J, Cloos P, Toftegaard U, Klinkenberg D, Bracken AP, Trinh E, Heeran M, Di Stefano L, Helin K. Characterization of E2F8, a novel E2F-like cell-cycle regulated repressor of E2F-activated transcription. Nucleic Acids Res 2005; 33:5458-70.
13. Maiti B, Li J, de Bruin A, Gordon F, Timmers C, Opavsky R, Patil K, Tuttle J, Cleghorn W, Leone G. Cloning and characterization of mouse E2F8, a novel mammalian E2F family member capable of blocking cellular proliferation. J Biol Chem 2005; 280:18211-20.
14. Markey M, Siddiqui H, Knudsen ES. Geminin is targeted for repression by the retinoblastoma tumor suppressor pathway through intragenic E2F sites. J Biol Chem 2004; 279:29255-62.
15. Yoshida K, Inoue I. Regulation of Geminin and Cdt1 expression by E2F transcription factors. Oncogene 2004; 23:3802-12.
16. Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A, te Riele H. Requirement for a functional Rb-1 gene in murine development. Nature 1992; 359:328-30.
17. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. Effects of an Rb mutation in the mouse. Nature 1992; 359:295-300.
18. Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH, Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 1992; 359:288-94.
19. Lee E, Hu N, Yuan SSF, Cox LA, Bradley A, Lee W, Herrup K. Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes and Dev 1994; 8:2008-21.
20. Morgenbesser SD, Williams BO, Jacks T, DePinho RA. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 1994; 371:72-4.
21. Maandag EC, van der Valk M, Vlaar M, Feltkamp C, O'Brien J, van Roon M, van der Lugt N, Berns A, te Riele H. Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J 1994; 13:4260-8.
22. Williams BO, Schmitt EM, Remington L, Bronson RT, Albert DM, Weinberg RA, Jacks T. Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO J 1994; 13:4251-9.
23. Lipinski MM, Macleod KF, Williams BO, Mullaney TL, Crowley D, Jacks T. Cell-autonomous and noncell-autonomous functions of the Rb tumor suppressor in developing central nervous system. EMBO J 2001; 20:3402-13.
24. Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 2003; 421:942-7.
25. de Bruin A, Maiti B, Jakoi L, Timmers C, Buerki R, Leone G. Identification and characterization of E2F7, a novel mammalian E2F family member capable of blocking cellular proliferation. J Biol Chem 2003; 278:42041-9.
26. Ferguson KL, Vanderluit JL, Hebert JM, McIntosh WC, Tibbo E, MacLaurin JG, Park DS, Wallace VA, Vooijs M, McConnell SK, Slack RS. Telencephalon- specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J 2002; 21:3337-46.
27. MacPherson D, Sage J, Crowley D, Trumpp A, Bronson RT, Jacks T. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol Cell Biol 2003; 23:1044-53.
28. Chen D, Livne-bar I, Vanderluit JL, Slack RS, Agochiya M, Bremner R. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 2004; 5:539-51.
29. Marino S, Hoogervoorst D, Brandner S, Berns A. Rb and p107 are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development 2003; 130:3359-68.
30. Robanus-Maandag E, Dekker M, van der Valk M, Carrozza ML, Jeanny JC, Dannenberg JH, Berns A, te Riele H. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev 1998; 12:1599-609.
31. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev 2004; 18:1681-94.
32. Vanderluit JL, Ferguson KL, Nikoletopoulou V, Parker M, Ruzhynsky V, Alexson T, McNamara SM, Park DS, Rudnicki M, Slack RS. p107 regulates neural precursor cells in the mammalian brain. J Cell Biol 2004; 166:853-63.
33. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 1999; 126:1927-35.
34. Kowalczyk A, Filipkowski RK, Rylski M, Wilczynski GM, Konopacki FA, Jaworski J, Ciemerych MA, Sicinski P, Kaczmarek L. The critical role of cyclin D2 in adult neurogenesis. J Cell Biol 2004; 167:209-13.
35. Cicero S, Herrup K. Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J Neurosci 2005; 25:9658-68.
36. Dhavan R, Tsai LH. A decade of CDK5. Nat Rev Mol Cell Biol 2001; 2:749-59.
37. Doetsch F, Verdugo JM, Caille I, Alvarez-Buylla A, Chao MV, Casaccia-Bonnefil P. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J Neurosci 2002; 22:2255-64.
38. Dyer MA, Cepko CL. p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development 2000; 127:3593-605.
39. Knoepfler PS, Cheng PF, Eisenman RN. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 2002; 16:2699-712.
40. Greene LA, Biswas SC, Liu DX. Cell cycle molecules and vertebrate neuron death: E2F at the hub. Cell Death Differ 2004; 11:49-60.
41. Smith PD, O'Hare MJ, Park DS. CDKs: Taking on a role as mediators of dopaminergic loss in Parkinson's disease. Trends Mol Med 2004; 10:445-51.
42. Becker EB, Bonni A. Beyond proliferation-cell cycle control of neuronal survival and differentiation in the developing mammalian brain. Semin Cell Dev Biol 2005; 16:439-48.
43. Joseph B, Wallen-Mackenzie A, Benoit G, Murata T, Joodmardi E, Okret S, Perlmann T. p57(Kip2) cooperates with Nurr1 in developing dopamine cells. Proc Natl Acad Sci USA 2003; 100:15619-24.
44. McGarry TJ, Kirschner MW. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998; 93:1043-53.
45. Luo L, Yang X, Takihara Y, Knoetgen H, Kessel M. The cell-cycle regulator geminin inhibits Hox function through direct and polycomb-mediated interactions. Nature 2004; 427:749-53.
46. Del Bene F, Tessmar-Raible K, Wittbrodt J. Direct interaction of geminin and Six3 in eye development. Nature 2004; 427:745-9.
47. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, Kroll KL. Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 2005; 19:1723-34.
48. Kroll KL, Salic AN, Evans LM, Kirschner MW. Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 1998; 125:3247-58.
49. Seo S, Richardson GA, Kroll KL. The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 2005; 132:105-15.
50. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol 2006; 8:17-26.
51. Ferguson KL, McClellan KA, Vanderluit JL, McIntosh WC, Schuurmans C, Polleux F, Slack RS. A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration. EMBO J 2005; 24:4381-91.
52. Morris EJ, Dyson NJ. Retinoblastoma protein partners. Adv Cancer Res 2001; 82:1-54.
53. Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005; 5:603-14.
54. Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 2000; 407:592-8.
55. Muller H, Bracken AP, Vernell R, Moroni MC, Christians F, Grassilli E, Prosperini E, Vigo E, Oliner JD, Helin K. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev 2001; 15:267-85.
56. Dimova DK, Stevaux O, Frolov MV, Dyson NJ. Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 2003; 17:2308-20.
57. Black EP, Hallstrom T, Dressman HK, West M, Nevins JR. Distinctions in the specificity of E2F function revealed by gene expression signatures. Proc Natl Acad Sci USA 2005; 102:15948-53.
58. Iwanaga R, Komori H, Ishida S, Okamura N, Nakayama K, Nakayama KI, Ohtani K. Identification of novel E2F1 target genes regulated in cell cycle-dependent and independent manners. Oncogene 2006; 25:1786-98.
59. Irie A, Yates EA, Turnbull JE, Holt CE. Specific heparan sulfate structures involved in retinal axon targeting. Development 2002; 129:61-70.
60. Iancu-Rubin C, Atweh GF. p27(Kip1) and stathmin share the stage for the first time. Trends Cell Biol 2005; 15:346-8.
61. Manitt C, Kennedy TE. Where the rubber meets the road: Netrin expression and function in developing and adult nervous systems. Prog Brain Res 2002; 137:425-42.
62. Huang Y, Rangwala F, Fulkerson PC, Ling B, Reed E, Cox AD, Kamholz J, Ratner N. Role of TC21/R-Ras2 in enhanced migration of neurofibromin-deficient Schwann cells. Oncogene 2004; 23:368-78.
63. Gad JM, Keeling SL, Wilks AF, Tan SS, Cooper HM. The expression patterns of guidance receptors, DCC and Neogenin, are spatially and temporally distinct throughout mouse embryogenesis. Dev Biol 1997; 192:258-73.
64. Benachenhou N, Massy I, Vacher J. Characterization and expression analyses of the mouse Wiskott-Aldrich syndrome protein (WASP) family member Wave1/Scar. Gene 2002; 290:131-40.
65. Rajagopalan S, Deitinghoff L, Davis D, Conrad S, Skutella T, Chedotal A, Mueller BK, Strittmatter SM. Neogenin mediates the action of repulsive guidance molecule. Nat Cell Biol 2004; 6:756-62.
66. Korey CA, Van Vactor D. From the growth cone surface to the cytoskeleton: One journey, many paths. J Neurobiol 2000; 44:184-93.
67. Cooper-Kuhn CM, Vroemen M, Brown J, Ye H, Thompson MA, Winkler J, Kuhn HG. Impaired adult neurogenesis in mice lacking the transcription factor E2F1. Mol Cell Neurosci 2002; 21:312-23.
68. Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 1995; 82:621-30.
69. Ferguson KL, Callaghan SM, MJ OH, Park DS, Slack RS. The Rb-CDK4/6 signaling pathway is critical in neural precursor cell cycle regulation. J Biol Chem 2000; 275:33593-600.
70. Kippin TE, Martens DJ, van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev 2005; 19:756-67.
71. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003; 425:962-7.
72. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev 2005; 19:1432-7.
73. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 2003; 3:895-902.
74. Konishi Y, Stegmuller J, Matsuda T, Bonni S, Bonni A. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 2004; 303:1026-30.