Mcl1 regulates the terminal mitosis of neural precursor cells in the mammalian brain through p27kip1

Development (Cambridge)

Volumn 140, Issue 15, 2013, Pages 3118-3127

  Mahmudul Hasan, S M ^a   Sheen, Ashley D ^a   Power, Angela M ^a   Langevin, Lisa Marie ^b   Xiong, Jieying ^a   Furlong, Michael ^a   Day, Kristine ^a   Schuurmans, Carol ^b   Opferman, Joseph T ^c   Vanderluit, Jacqueline L ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Bcl 2; Cdkn1b; Cell cycle; Mcl 1; Mouse; Neurogenesis

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; MONOCLONAL ANTIBODY KI 67; NESTIN; PROTEIN MCL 1; TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; GENE OVEREXPRESSION; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; MAMMAL; MITOSIS; MOUSE; NEOCORTEX; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

BCL-2; CDKN1B; CELL CYCLE; MCL-1; MOUSE; NEUROGENESIS;

ANIMALS; BRAIN; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOSIS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NEURAL STEM CELLS; NEUROGENESIS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84880267253     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.090910     Document Type: Article

References (68)

1. Adams, K. W. and Cooper, G. M. (2007). Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J. Biol. Chem. 282, 6192-6200.
2. Angevine, J. B., Jr and Sidman, R. L. (1961). Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766-768.
3. Arbour, N., Vanderluit, J. L., Le Grand, J. N., Jahani-Asl, A., Ruzhynsky, V. A., Cheung, E. C., Kelly, M. A., MacKenzie, A. E., Park, D. S., Opferman, J. T. et al. (2008). Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J. Neurosci. 28, 6068-6078.
4. Barton, K. M. and Levine, E. M. (2008). Expression patterns and cell cycle profiles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Dev. Dyn. 237, 672-682.
5. Cai, L., Hayes, N. L., Takahashi, T., Caviness, V. S., Jr and Nowakowski, R. S. (2002). Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior. J. Neurosci. Res. 69, 731- 744.
6. Casaccia-Bonnefil, P., Tikoo, R., Kiyokawa, H., Friedrich, V., Jr, Chao, M. V. and Koff, A. (1997). Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev. 11, 2335-2346.
7. Caviness, V. S., Jr, Goto, T., Tarui, T., Takahashi, T., Bhide, P. G. and Nowakowski, R. S. (2003). Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb. Cortex 13, 592-598.
8. Caviness, V. S., Jr, Nowakowski, R. S. and Bhide, P. G. (2009). Neocortical neurogenesis: morphogenetic gradients and beyond. Trends Neurosci. 32, 443-450.
9. Cicero, S. and Herrup, K. (2005). Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J. Neurosci. 25, 9658-9668.
10. Dehay, C. and Kennedy, H. (2007). Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8, 438-450.
11. Durand, B., Fero, M. L., Roberts, J. M. and Raff, M. C. (1998). p27Kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Curr. Biol. 8, 431-440.
12. Dyer, M. A. and Cepko, C. L. (2001). p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J. Neurosci. 21, 4259-4271.
13. Fero, M. L., Rivkin, M., Tasch, M., Porter, P., Carow, C. E., Firpo, E., Polyak, K., Tsai, L. H., Broudy, V., Perlmutter, R. M. et al. (1996). A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85, 733-744.
14. Fujise, K., Zhang, D., Liu, J. and Yeh, E. T. (2000). Regulation of apoptosis and cell cycle progression by MCL1. Differential role of proliferating cell nuclear antigen. J. Biol. Chem. 275, 39458-39465.
15. Gerdes, J., Lemke, H., Baisch, H., Wacker, H. H., Schwab, U. and Stein, H. (1984). Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710- 1715.
16. Goto, T., Mitsuhashi, T. and Takahashi, T. (2004). Altered patterns of neuron production in the p27 knockout mouse. Dev. Neurosci. 26, 208-217.
17. Götz, M. and Huttner, W. B. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
18. Greider, C., Chattopadhyay, A., Parkhurst, C. and Yang, E. (2002). BCL-x(L) and BCL2 delay Myc-induced cell cycle entry through elevation of p27 and inhibition of G1 cyclin-dependent kinases. Oncogene 21, 7765-7775.
19. Harley, M. E., Allan, L. A., Sanderson, H. S. and Clarke, P. R. (2010). Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest. EMBO J. 29, 2407-2420.
20. Haydar, T. F., Wang, F., Schwartz, M. L. and Rakic, P. (2000). Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 20, 5764-5774.
21. Hevner, R. F. (2007). Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development. J. Neuropathol. Exp. Neurol. 66, 101-109.
22. Hevner, R. F., Hodge, R. D., Daza, R. A. and Englund, C. (2006). Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci. Res. 55, 223-233.
23. Jamil, S., Sobouti, R., Hojabrpour, P., Raj, M., Kast, J. and Duronio, V. (2005). A proteolytic fragment of Mcl-1 exhibits nuclear localization and regulates cell growth by interaction with Cdk1. Biochem. J. 387, 659-667.
24. Ji, P., Jiang, H., Rekhtman, K., Bloom, J., Ichetovkin, M., Pagano, M. and Zhu, L. (2004). An Rb-Skp2-p27 pathway mediates acute cell cycle inhibition by Rb and is retained in a partial-penetrance Rb mutant. Mol. Cell 16, 47-58.
25. Joseph, B. and Hermanson, O. (2010). Molecular control of brain size: regulators of neural stem cell life, death and beyond. Exp. Cell Res. 316, 1415-1421.
26. Kawauchi, T., Chihama, K., Nabeshima, Y. and Hoshino, M. (2006). Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8, 17-26.
27. Kowalczyk, T., Pontious, A., Englund, C., Daza, R. A., Bedogni, F., Hodge, R., Attardo, A., Bell, C., Huttner, W. B. and Hevner, R. F. (2009). Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19, 2439-2450.
28. Kozopas, K. M., Yang, T., Buchan, H. L., Zhou, P. and Craig, R. W. (1993). MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. USA 90, 3516-3520.
29. Krajewski, S., Krajewska, M., Ehrmann, J., Sikorska, M., Lach, B., Chatten, J. and Reed, J. C. (1997). Immunohistochemical analysis of Bcl-2, Bcl-X, Mcl-1, and Bax in tumors of central and peripheral nervous system origin. Am. J. Pathol. 150, 805-814.
30. Langevin, L. M., Mattar, P., Scardigli, R., Roussigné, M., Logan, C., Blader, P. and Schuurmans, C. (2007). Validating in utero electroporation for the rapid analysis of gene regulatory elements in the murine telencephalon. Dev. Dyn. 236, 1273-1286.
31. Leone, D. P., Srinivasan, K., Chen, B., Alcamo, E. and McConnell, S. K. (2008). The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 18, 28-35.
32. Mairet-Coello, G., Tury, A., Van Buskirk, E., Robinson, K., Genestine, M. and DiCicco-Bloom, E. (2012). p57(KIP2) regulates radial glia and intermediate precursor cell cycle dynamics and lower layer neurogenesis in developing cerebral cortex. Development 139, 475-487.
33. Malone, C. D., Hasan, S. M., Roome, R. B., Xiong, J., Furlong, M., Opferman, J. T. and Vanderluit, J. L. (2012). Mcl-1 regulates the survival of adult neural precursor cells. Mol. Cell. Neurosci. 49, 439-447.
34. McConnell, S. K. and Kaznowski, C. E. (1991). Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282-285.
35. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
36. Mitsuhashi, T. and Takahashi, T. (2009). Genetic regulation of proliferation/differentiation characteristics of neural progenitor cells in the developing neocortex. Brain Dev. 31, 553-557.
37. Mitsuhashi, T., Aoki, Y., Eksioglu, Y. Z., Takahashi, T., Bhide, P. G., Reeves, S. A. and Caviness, V. S., Jr (2001). Overexpression of p27Kip1 lengthens the G1 phase in a mouse model that targets inducible gene expression to central nervous system progenitor cells. Proc. Natl. Acad. Sci. USA 98, 6435-6440.
38. Molyneaux, B. J., Arlotta, P., Menezes, J. R. and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437.
39. Montagnoli, A., Fiore, F., Eytan, E., Carrano, A. C., Draetta, G. F., Hershko, A. and Pagano, M. (1999). Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev. 13, 1181-1189.
40. Nguyen, L., Besson, A., Heng, J. I., Schuurmans, C., Teboul, L., Parras, C., Philpott, A., Roberts, J. M. and Guillemot, F. (2006a). p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20, 1511-1524.
41. Nguyen, L., Besson, A., Roberts, J. M. and Guillemot, F. (2006b). Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5, 2314-2318.
42. Nieto, M., Monuki, E. S., Tang, H., Imitola, J., Haubst, N., Khoury, S. J., Cunningham, J., Gotz, M. and Walsh, C. A. (2004). Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 479, 168-180.
43. Opferman, J. T., Letai, A., Beard, C., Sorcinelli, M. D., Ong, C. C. and Korsmeyer, S. J. (2003). Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426, 671-676.
44. Opferman, J. T., Iwasaki, H., Ong, C. C., Suh, H., Mizuno, S., Akashi, K. and Korsmeyer, S. J. (2005). Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307, 1101-1104.
45. Polleux, F., Dehay, C. and Kennedy, H. (1997). The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J. Comp. Neurol. 385, 95-116.
46. Reynolds, B. A., Tetzlaff, W. and Weiss, S. (1992). A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12, 4565-4574.
47. Reznikov, K. and van der Kooy, D. (1995). Variability and partial synchrony of the cell cycle in the germinal zone of the early embryonic cerebral cortex. J. Comp. Neurol. 360, 536-554.
48. Rinkenberger, J. L., Horning, S., Klocke, B., Roth, K. and Korsmeyer, S. J. (2000). Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14, 23-27.
49. Saito, T. and Nakatsuji, N. (2001). Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237-246.
50. Simpson, M. T., MacLaurin, J. G., Xu, D., Ferguson, K. L., Vanderluit, J. L., Davoli, M. A., Roy, S., Nicholson, D. W., Robertson, G. S., Park, D. S. et al. (2001). Caspase 3 deficiency rescues peripheral nervous system defect in retinoblastoma nullizygous mice. J. Neurosci. 21, 7089-7098.
51. Sitailo, L. A., Jerome-Morais, A. and Denning, M. F. (2009). Mcl-1 functions as major epidermal survival protein required for proper keratinocyte differentiation. J. Invest. Dermatol. 129, 1351-1360.
52. Takahashi, H. and Liu, F. C. (2006). Genetic patterning of the mammalian telencephalon by morphogenetic molecules and transcription factors. Birth Defects Res. C Embryo Today 78, 256-266.
53. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1993). Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J. Neurosci. 13, 820-833.
54. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1995). The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046-6057.
55. Takahashi, T., Goto, T., Miyama, S., Nowakowski, R. S. and Caviness, V. S., Jr (1999). Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19, 10357- 10371.
56. Tarui, T., Takahashi, T., Nowakowski, R. S., Hayes, N. L., Bhide, P. G. and Caviness, V. S. (2005). Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb. Cortex 15, 1343-1355.
57. Tropepe, V., Sibilia, M., Ciruna, B. G., Rossant, J., Wagner, E. F. and van der Kooy, D. (1999). Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208, 166-188.
58. Tury, A., Mairet-Coello, G. and DiCicco-Bloom, E. (2011). The cyclindependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb. Cortex 21, 1840-1856.
59. Tury, A., Mairet-Coello, G. and DiCicco-Bloom, E. (2012). The multiple roles of the cyclin-dependent kinase inhibitory protein p57(KIP2) in cerebral cortical neurogenesis. Dev. Neurobiol. 72, 821-842.
60. Vaccarino, F. M., Schwartz, M. L., Raballo, R., Nilsen, J., Rhee, J., Zhou, M., Doetschman, T., Coffin, J. D., Wyland, J. J. and Hung, Y. T. (1999). Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 2, 246-253.
61. Vairo, G., Soos, T. J., Upton, T. M., Zalvide, J., DeCaprio, J. A., Ewen, M. E., Koff, A. and Adams, J. M. (2000). Bcl-2 retards cell cycle entry through p27(Kip1), pRB relative p130, and altered E2F regulation. Mol. Cell. Biol. 20, 4745-4753.
62. Vanderluit, J. L., Ferguson, K. L., Nikoletopoulou, V., Parker, M., Ruzhynsky, V., Alexson, T., McNamara, S. M., Park, D. S., Rudnicki, M. and Slack, R. S. (2004). p107 regulates neural precursor cells in the mammalian brain. J. Cell Biol. 166, 853-863.
63. Vick, B., Weber, A., Urbanik, T., Maass, T., Teufel, A., Krammer, P. H., Opferman, J. T., Schuchmann, M., Galle, P. R. and Schulze-Bergkamen, H. (2009). Knockout of myeloid cell leukemia-1 induces liver damage and increases apoptosis susceptibility of murine hepatocytes. Hepatology 49, 627- 636.
64. Vlach, J., Hennecke, S. and Amati, B. (1997). Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16, 5334-5344.
65. Warr, M. R., Acoca, S., Liu, Z., Germain, M., Watson, M., Blanchette, M., Wing, S. S. and Shore, G. C. (2005). BH3-ligand regulates access of MCL-1 to its E3 ligase. FEBS Lett. 579, 5603-5608.
66. Ye, W., Mairet-Coello, G., Pasoreck, E. and Dicicco-Bloom, E. (2009). Patterns of p57Kip2 expression in embryonic rat brain suggest roles in progenitor cell cycle exit and neuronal differentiation. Dev. Neurobiol. 69, 1-21.
67. Zheng, Y. L., Li, B. S., Rudrabhatla, P., Shukla, V., Amin, N. D., Maric, D., Kesavapany, S., Kanungo, J., Pareek, T. K., Takahashi, S. et al. (2010). Phosphorylation of p27Kip1 at Thr187 by cyclin-dependent kinase 5 modulates neural stem cell differentiation. Mol. Biol. Cell 21, 3601-3614.
68. Zhong, Q., Gao, W., Du, F. and Wang, X. (2005). Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121, 1085-1095.