Protection of p27Kip1 mRNA by quaking RNA binding proteins promotes oligodendrocyte differentiation

Nature Neuroscience

Volumn 8, Issue 1, 2005, Pages 27-33

  Larocque, Daniel ^a,b   Galarneau, André ^a,b   Liu, Hsueh Ning ^b   Scott, Michelle ^c   Almazan, Guillermina ^b   Richard, Stéphane ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; MESSENGER RNA; RETROVIRUS VECTOR; RNA BINDING PROTEIN; CDKN1B PROTEIN, MOUSE; CDKN1B PROTEIN, RAT; CELL CYCLE PROTEIN; ISOPROTEIN; MYELIN BASIC PROTEIN; QK PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; BRAIN DEVELOPMENT; CELL CYCLE; CELL FATE; CELL MATURATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS CALLOSUM; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE TARGETING; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; RNA BINDING; STEM CELL; TELENCEPHALON; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; EMBRYO; GENETICS; METABOLISM; MOUSE MUTANT; MUTATION; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; RAT; RECESSIVE GENE; RNA STABILITY;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CORPUS CALLOSUM; CYCLIN-DEPENDENT KINASE INHIBITOR P27; EMBRYO; GENES, RECESSIVE; MICE; MICE, QUAKING; MUTATION; MYELIN BASIC PROTEINS; NEURONS; OLIGODENDROGLIA; PROTEIN ISOFORMS; RATS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; STEM CELLS; TELENCEPHALON; TUMOR SUPPRESSOR PROTEINS;

EID: 16644376235     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1359     Document Type: Article

References (48)

1. Sidman, R.L., Dickie, M.M. & Appel, S.H. Mutant mice (quaking and jimpy) with deficient myelination in the central nervous system. Science 144, 309-311 (1964).
2. Hogan, E.L. & Greenfield, S. Animal models of genetic disorders of myelin. in Myelin 489-534 (Plenum, New York, 1984).
3. Vernet, C. & Artzt, K. STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet. 13, 479-484 (1997).
4. Larocque, D. et al. Nuclear retention of MBP mRNAs in the Quaking viable mice. Neuron 36, 815-829 (2002).
5. Li, Z., Zhang, Y., Li, D. & Feng, Y. Destabilization and mislocalization of the myelin basic protein mRNAs in quaking dysmyelination lacking the Qk1 RNA-binding proteins. J. Neurosci. 20, 4944-4953 (2000).
6. Zhang, Y. & Feng, Y. Distinct molecular mechanisms lead to diminished myelin basic protein and 2′,3′-cyclic nucleotide 3′-phosphodiesterase in qk(v) dysmyelination. J. Neurochem. 77, 165-172 (2001).
7. Ebersole, T.A., Chen, Q., Justice, M.J. & Artzt, K. The quaking gene unites signal transduction and RNA binding in the developing nervous system. Nat. Genet. 12, 260-265 (1996).
8. Lorenzetti, D. et al. The neurological mutant quaking(viable) is Parkin deficient. Mamm. Genome 15, 210-217 (2004).
9. Hardy, R.J. et al. Neural cell type-specific expression of QKI proteins is altered in the quaking viable mutant mice. J. Neurosci. 16, 7941-7949 (1996).
10. Chen, T. & Richard, S. Structure-function analysis of Qk1: a lethal point mutation in mouse quaking prevents homodimerization. Mol. Cell. Biol. 18, 4863-4871 (1998).
11. Hardy, R.J. QKI expression is regulated during neuron-glial cell fate decisions. J. Neurosci. Res. 54, 46-57 (1998).
12. Rowitch, D.H. Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419 (2004).
13. Colognato, H. & French-Constant, C. Mechanisms of glial development. Curr. Opin. Neurobiol. 14, 37-44 (2004).
14. Ross, S.E., Greenberg, M.E. & Stiles, C.D. Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25 (2003).
15. Perrone-Bizzozero, N. & Bolognani, F. Role of HuD and other RNA-binding proteins in neural development and plasticity. J. Neurosci. Res. 68, 121-126 (2002).
16. Darnell, R.B. Paraneoplastic neurologic disorders: windows into neuronal function and tumor immunity. Arch. Neurol. 61, 30-32 (2004).
17. Jin, P. & Warren, S.T. New insights into fragile X syndrome: from molecules to neurobehaviors. Trends Biochem. Sci. 28, 152-158 (2003).
18. Okano, H., Imai, T. & Okabe, M. Musashi: a translational regulator of cell fate. J. Cell Sci. 115, 1355-1359 (2002).
19. Antic, D., Lu, N. & Keene, J.D. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13, 449-461 (1999).
20. Sherr, C.J. & Roberts, J.M. Positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512 (1999).
21. Casaccia-Bonnefil, P. et al. Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev. 11, 2335-2346 (1997).
22. Durand, B., Gao, F.B. & Raff, M. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J. 16, 306-317 (1997).
23. Dyer, M.A. & Cepko, C.L. p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J. Neurosci. 21, 4259-4271 (2001).
24. Friessen, A.J., Miskimins, W.K. & Miskimins, R. Cyclin-dependent kinase inhibitor p27kip1 is expressed at high levels in cells that express a myelinating phenotype. J. Neurosci. Res. 50, 373-382 (1997).
25. Tokumoto, Y.M., Apperly, J.A., Gao, F.B. & Raff, M.C. Posttranscriptional regulation of p18 and p27 Cdk inhibitor proteins and the timing of oligodendrocyte differentiation. Dev. Biol. 245, 224-234 (2002).
26. Trapp, B.D., Quarles, R.H. & Suzuki, K. Immunocytochemical studies of quaking mice support a role of the myelin-associated glycoprotein in forming and maintaining the periaxonal space and periaxonal cytoplasmic collar of myelinating schwann cells. J. Cell Biol. 99, 594-606 (1984).
27. Song, J., Goetz, B.D., Baas, P.W. & Duncan, I.D. Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol. Cell. Neurosci. 17, 624-636 (2001).
28. Dyer, M.A. & Cepko, C.L. Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2, 333-342 (2001).
29. Jan, E., Motzny, C.K., Graves, L.E. & Goodwin, E.B. The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J. 18, 258-269 (1999).
30. Lee, M.-H. & Schedl, T. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15, 2408-2420 (2001).
31. Saccomanno, L. et al. The STAR protein QKI-6 is a translational represser. Proc. Natl. Acad. Sci. USA 96, 12605-12610 (1999).
32. Li, Z. et al. Defective smooth muscle development in qkI-deficient mice. Dev. Growth Differ. 45, 449-462 (2003).
33. Cepko, C.L. et al. Lineage analysis using retroviral vectors. Methods 14, 393-406 (1998).
34. Gaiano, N., Kohtz, J.D., Turnbull, D.H. & Fishell, G. A method for rapid gain-of-function studies in the mouse embryonic nervous system. Nat. Neurosci. 2, 812-819 (1999).
35. Casaccia-Bonnefil, P. & Liu, A. Relationship between cell cycle molecules and onset of oligodendrocyte differentiation. J. Neurosci. Res. 72, 1-11 (2003).
36. Nagahara, H. et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4, 1449-1452 (1998).
37. Besson, A., Gurian-West, M., Schmidt, A., Hall, A. & Roberts, J.M. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18, 862-876 (2004).
38. Reed, S.I. Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover. Nat. Rev. Mol. Cell Biol. 4, 855-864 (2003).
39. Lee, M.H. & Schedl, T. Translation repression by GLD-1 protects its mRNA targets from nonsense mediated mRNA decay in C. elegans. Genes Dev. 18, 1047-1059 (2004).
40. Gopfert, U., Kullmann, M. & Hengst, L. Cell cycle-dependent translation of p27 involves a responsive element in its 5′-UTR that overlaps with a uORF. Hum. Mol. Genet. 12, 1767-1779 (2003).
41. Nery, S., Wichterle, H. & Fishell, G. Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540 (2001).
42. Lu, Q.R., Cai, L., Rowitch, D., Cepko, C.L. & Stiles, C.D. Ectopic expression of Olig1 promotes oligodendrocyte formation and reduces neuronal survival in developing mouse cortex. Nat. Neurosci. 4, 973-974 (2001).
43. Lee, M.H. et al. The brain-specific activator p35 allows Cdk5 to escape inhibition by p27Kip1 in neurons. Proc. Natl. Acad. Sci. USA 93, 3259-3263 (1996).
44. Tikoo, R. et al. Ectopic expression of p27Kip1 in oligodendrocyte progenitor cells results in cell-cycle growth arrest. J. Neurobiol. 36, 431-440 (1998).
45. Zhang, Y. et al. Tyrosine phosphorylation of QKI mediates developmental signals to regulate mRNA metabolism. EMBO J. 22, 1801-1810 (2003).
46. Almazan, G., Afar, D.E.H. & Bell, J.C. Phosphorylation and disruption of intermediate filament protein in oligodendrocyte precursor cultures treated with calyculin A. J. Neurosci. Res. 36, 163-172 (1993).
47. Pilotte, J., Larocque, D. & Richard, S. Nuclear translocation controlled by alternatively spliced isoforms inactivates the QUAKING apoptotic inducer. Genes Dev. 15, 845-858 (2001).
48. Fragoso, G. et al. Inhibition of p38 mitogen-activated protein kinase interferes with cell shape changes and gene expression associated with Schwann cell myelination. Exp. Neurol. 183, 34-46 (2003).