p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex

Genes and Development

Volumn 20, Issue 11, 2006, Pages 1511-1524

  Nguyen, Laurent ^a   Besson, Arnaud ^b   Heng, Julian Ik Tsen ^a   Schuurmans, Carol ^c   Teboul, Lydia ^a,e   Parras, Carlos ^a   Philpott, Anna ^d   Roberts, James M ^b   Guillemot, François ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Electroporation; Neurogenesis; Neurogenin; Radial migration; RhoA; RNA interference

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE P27; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; CDKN1B PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1B;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL MIGRATION; ELECTROPORATION; ENZYME ACTIVITY; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR GENETICS; MOUSE MUTANT; NERVE CELL; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL MOVEMENT; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE INHIBITOR P27; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; NEURONS;

EID: 33744816196     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.377106     Document Type: Article

References (55)

1. Abu Hatoum, O., Gross-Mesilaty, S., Breitschopf, K., Hoffman, A., Gonen, H., Ciechanover, A., and Bengal, E. 1998. Degradation of myogenic transcription factor MyoD by the ubiquitin pathway in vivo and in vitro: Regulation by specific DNA binding. Mol. Cell. Biol. 18: 5670-5677.
2. Bertrand, N., Castro, D.S., and Guillemot, F. 2002. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3: 517-530.
3. Besson, A., Gurian-West, M., Schmidt, A., Hall, A., and Roberts, J.M. 2004. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes & Dev. 18: 862-876.
4. Besson, A., Gurian-West, M., Chen, X., Kelly-Spratt, K.S., Kemp, C.J., and Roberts, J.M. 2006. A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes & Dev. 20: 47-64.
5. Bielas, S., Higginbotham, H., Koizumi, H., Tanaka, T., and Gleeson, J.G. 2004. Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu. Rev. Cell Dev. Biol. 20: 593-618.
6. Britz, O., Mattar, P., Nguyen, L., Langevin, L.-M., Zimmer, C., Alam, S., Guillemot, F., and Schuurmans, C. 2006. A role for proneural genes in the maturation of cortical progenitor cells. Cereb. Cortex (in press).
7. Carruthers, S., Mason, J., and Papalopulu, N. 2003. Depletion of the cell-cycle inhibitor p27(Xic1) impairs neuronal differentiation and increases the number of ElrC(+) progenitor cells in Xenopus tropicalis. Mech. Dev. 120: 607-616.
8. Casini, T. and Pelicci, P.G. 1999. A function of p21 during promyelocytic leukemia cell differentiation independent of CDK inhibition and cell cycle arrest. Oncogene 18: 3235-3243.
9. Cau, E., Gradwohl, G., Fode, C., and Guillemot, F. 1997. Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124: 1611-1621.
10. Caviness Jr., V.S., 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.
11. Diez-Juan, A. and Andres, V. 2003. Coordinate control of proliferation and migration by the p27Kip1/cyclin-dependent kinase/retinoblastoma pathway in vascular smooth muscle cells and fibroblasts. Circ. Res. 92: 402-410.
12. Doetsch, F., Verdugo, J.M., Caille, I., Alvarez-Buylla, A., Chao, M.V., and Casaccia-Bonnefil, P. 2002. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis. J. Neurosci. 22: 2255-2264.
13. Durand, B., Gao, F.B., and Raff, M. 1997. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J. 16: 306-317.
14. Elledge, S.J. and Harper, J.W. 1994. Cdk inhibitors: On the threshold of checkpoints and development. Curr. Opin. Cell Biol. 6: 847-852.
15. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R.A., Bulfone, A., Kowalczyk, T., and Hevner, R.F. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25: 247-251.
16. Farah, M.H., Olson, J.M., Sucic, H.B., Hume, R.I., Tapscott, S.J., and Turner, D.L. 2000. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127: 693-702.
17. Ferguson, K.L., McClellan, K.A., Vanderluit, J.L., McIntosh, W.C., Schuurmans, C., Polleux, F., and Slack, R.S. 2005. A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration. EMBO J. 24: 4381-4391.
18. 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.
19. Ge, W., He, F., Kim, K.J., Blanchi, B., Coskun, V., Nguyen, L., Wu, X., Zhao, J., Heng, J.I., Martinowich, K., et al. 2006. Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc. Natl. Acad. Sci. 103: 1319-1324.
20. Goto, T., Mitsuhashi, T., and Takahashi, T. 2004. Altered patterns of neuron production in the p27 knockout mouse. Dev. Neurosci. 26: 208-217.
21. Gradwohl, G., Fode, C., and Guillemot, F. 1996. Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180: 227-241.
22. Guillemot, F., Molnar, Z., Tarabykin, V., and Stoykova, A. 2006. Molecular mechanisms of cortical differentiation. Eur. J. Neurosci. 23: 857-868.
23. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, I.-T.K., Guerrier, S., Boutt, E., Peters, E., Barnes, A.P., Parras, C., et al. 2005. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48: 45-62.
24. Hoffman, L., Pratt, G., and Rechsteiner, M. 1992. Multiple forms of the 20 S multicatalytic and the 26 S ubiquitin/ATP-dependent proteases from rabbit reticulocyte lysate. J. Biol. Chem. 267: 22362-22368.
25. Kawaguchi, A., Ogawa, M., Saito, K., Matsuzaki, F., Okano, H., and Miyata, T. 2004. Differential expression of Pax6 and Ngn2 between pair-generated cortical neurons. J. Neurosci. Res. 78: 784-795.
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. Kholmanskikh, S.S., Dobrin, J.S., Wynshaw-Boris, A., Letourneau, P.C., and Ross, M.E. 2003. Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J. Neurosci. 23: 8673-8681.
28. Kiyokawa, H., Kineman, R.D., Manova-Todorova, K.O., Soares, V.C., Hoffman, E.S., Ono, M., Khanam, D., Hayday, A.C., Frohman, L.A., and Koff, A. 1996. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85: 721-732.
29. Laman, H., Funes, J.M., Ye, H., Henderson, S., Galinanes-Garcia, L., Hara, E., Knowles, P., McDonald, N., and Boshoff, C. 2005. Transforming activity of Fbxo7 is mediated specifically through regulation of cyclin D/cdk6. EMBO J. 24: 3104-3116.
30. Lee, E.Y., Chang, C.Y., Hu, N., Wang, Y.C., Lai, C.C., Herrup, K., Lee, W.H., and Bradley, A. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis [see comments]. Nature 359: 288-294.
31. Lukaszewicz, A., Savatier, P., Cortay, V., Giroud, P., Huissoud, C., Berland, M., Kennedy, H., and Dehay, C. 2005. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47: 353-364.
32. Luo, L. 2000. Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1: 173-180.
33. McAllister, S.S., Becker-Hapak, M., Pintucci, G., Pagano, M., and Dowdy, S.F. 2003. Novel p27(kip1) C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol. Cell. Biol. 23: 216-228.
34. Nakayama, K., Ishida, N., Shirane, M., Inomata, A., Inoue, T., Shishido, N., Horii, I., and Loh, D.Y. 1996. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85: 707-720.
35. Nieto, M., Schuurmans, C., Britz, O., and Guillemot, F. 2001. Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29: 401-413.
36. Ohnuma, S. and Harris, W.A. 2003. Neurogenesis and the cell cycle. Neuron 40: 199-208.
37. Ohnuma, S., Philpott, A., Wang, K., Holt, C.E., and Harris, W.A. 1999. p27Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. Cell 99: 499-510.
38. Reynaud, E.G., Leibovitch, M.P., Tintignac, L.A., Pelpel, K., Guillier, M., and Leibovitch, S.A. 2000. Stabilization of MyoD by direct binding to p57(Kip2). J. Biol. Chem. 275: 18767-18776.
39. Saito, T. and Nakatsuji, N. 2001. Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240: 237-246.
40. Schuurmans, C., Armant, O., Nieto, M., Stenman, J.M., Britz, O., Klenin, N., Seibt, J., Brown, C., Tang, H., Cunningham, J.M., et al. 2004. Sequential phases of neocortical fate specification involve Neurogenin-dependent and -independent pathways. EMBO J. 23: 2892-2902.
41. Sherr, C.J. and Roberts, J.M. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes & Dev. 13: 1501-1512.
42. Sidman, R.L. and Rakic, P. 1973. Neuronal migration, with special reference to developing human brain: A review. Brain Res. 62: 1-35.
43. Sriuranpong, V., Borges, M.W., Strock, C.L., Nakakura, E.K., Watkins, D.N., Blaumueller, C.M., Nelkin, B.D., and Ball, D.W. 2002. Notch signaling induces rapid degradation of achaete-scute homolog 1. Mol. Cell. Biol. 22: 3129-3139.
44. Steinman, R.A. 2002. Cell cycle regulators and hematopoiesis. Oncogene 21: 3403-3413.
45. Sun, J., Marx, S.O., Chen, H.J., Poon, M., Marks, A.R., and Rabbani, L.E. 2001. Role for p27(Kip1) in vascular smooth muscle cell migration. Circulation 103: 2967-2972.
46. Tanaka, H., Yamashita, T., Asada, M., Mizutani, S., Yoshikawa, H., and Tohyama, M. 2002. Cytoplasmic p21(Cip1/WAF1) regulates neurite remodeling by inhibiting Rho-kinase activity. J. Cell Biol. 158: 321-329.
47. 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.
48. Vernon, A.E. and Philpott, A. 2003. A single cdk inhibitor, p27Xic1, functions beyond cell cycle regulation to promote muscle differentiation in Xenopus. Development 130: 71-83.
49. Vernon, A.E., Devine, C., and Philpott, A. 2003. The cdk inhibitor p27Xic1 is required for differentiation of primary neurones in Xenopus. Development 130: 85-92.
50. Watanabe, H., Pan, Z.Q., Schreiber-Agus, N., DePinho, R.A., Hurwitz, J., and Xiong, Y. 1998. Suppression of cell transformation by the cyclin-dependent kinase inhibitor p57KIP2 requires binding to proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. 95: 1392-1397.
51. Welcker, M., Lukas, J., Strauss, M., and Bartek, J. 1998. p21WAF1/CIP1 mutants deficient in inhibiting cyclin-dependent kinases (CDKs) can promote assembly of active cyclin D/CDK4(6) complexes in human tumor cells. Cancer Res. 58: 5053-5056.
52. Wennerberg, K., Forget, M.A., Ellerbroek, S.M., Arthur, W.T., Burridge, K., Settleman, J., Der, C.J., and Hansen, S.H. 2003. Rnd proteins function as RhoA antagonists by activating p190 RhoGAP. Curr. Biol. 13: 1106-1115.
53. Zezula, J., Casaccia-Bonnefil, P., Ezhevsky, S.A., Osterhout, D.J., Levine, J.M., Dowdy, S.F., Chao, M.V., and Koff, A. 2001. p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep. 2: 27-34.
54. Zhang, P., Wong, C., Liu, D., Finegold, M., Harper, J.W., and Elledge, S.J. 1999. p21(CIP1) and p57(KIP2) control muscle differentiation at the myogenin step. Genes & Dev. 13: 213-224.
55. Zindy, F., Cunningham, J.J., Sherr, C.J., Jogal, S., Smeyne, R.J., and Roussel, M.F. 1999. Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc. Natl. Acad. Sci. 96: 13462-13467.