Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K

Journal of Cell Biology

Volumn 192, Issue 5, 2011, Pages 797-811

  Laursen, Lisbeth S ^a,b   Chan, Colin W ^c   FfrenchConstant, Charles ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; INTEGRIN; MESSENGER RNA; MYELIN BASIC PROTEIN; VERY LATE ACTIVATION ANTIGEN 6;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; MOUSE; MYELIN SHEATH; MYELINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RAT; RNA TRANSLATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD29; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN K; HUMANS; INTEGRIN ALPHA6BETA1; MOLECULAR SEQUENCE DATA; MYELIN BASIC PROTEINS; MYELIN SHEATH; OLIGODENDROGLIA; PROTEIN BIOSYNTHESIS; RATS; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 79952412205     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007014     Document Type: Article

References (52)

1. Ainger, K., D. Avossa, F. Morgan, S.J. Hill, C. Barry, E. Barbarese, and J.H. Carson. 1993. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J. Cell Biol. 123:431-441. doi:10.1083/jcb.123.2.431 (Pubitemid 23313966)
2. Ainger, K., D. Avossa, A.S. Diana, C. Barry, E. Barbarese, and J.H. Carson. 1997. Transport and localization elements in myelin basic protein mRNA. J. Cell Biol. 138:1077-1087. doi:10.1083/jcb.138.5.1077 (Pubitemid 27386457)
3. Barros, C.S., T. Nguyen, K.S. Spencer, A. Nishiyama, H. Colognato, and U. Müller. 2009. Beta1 integrins are required for normal CNS myelination and promote AKT-dependent myelin outgrowth. Development. 136:2717-2724. doi:10.1242/dev.038679
4. Biffiger, K., S. Bartsch, D. Montag, A. Aguzzi, M. Schachner, and U. Bartsch. 2000. Severe hypomyelination of the murine CNS in the absence of myelin-associated glycoprotein and fyn tyrosine kinase. J. Neurosci. 20:7430-7437.
5. Boggs, J.M. 2006. Myelin basic protein: a multifunctional protein. Cell. Mol. Life Sci. 63:1945-1961. doi:10.1007/s00018-006-6094-7 (Pubitemid 44359737)
6. Bomsztyk, K., O. Denisenko, and J. Ostrowski. 2004. hnRNP K: one protein multiple processes. Bioessays. 26:629-638. doi:10.1002/bies.20048 (Pubitemid 38758340)
7. Bottenstein, J.E., and G.H. Sato. 1979. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA. 76:514-517. doi:10.1073/pnas.76.1.514 (Pubitemid 9106659)
8. Buttery, P.C., and C. ffrench-Constant. 1999. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 14:199-212. doi:10.1006/mcne.1999.0781
9. Câmara, J., Z. Wang, C. Nunes-Fonseca, H.C. Friedman, M. Grove, D.L. Sherman, N.H. Komiyama, S.G. Grant, P.J. Brophy, A. Peterson, and C. ffrench-Constant. 2009. Integrin-mediated axoglial interactions initiate myelination in the central nervous system. J. Cell Biol. 185:699-712. doi:10.1083/jcb.200807010
10. Chang, A., W.W. Tourtellotte, R. Rudick, and B.D. Trapp. 2002. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346:165-173. doi:10.1056/NEJMoa010994 (Pubitemid 34438882)
11. Chicurel, M.E., R.H. Singer, C.J. Meyer, and D.E. Ingber. 1998. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature. 392:730-733. doi:10.1038/33719 (Pubitemid 28207796)
12. Chun, S.J., M.N. Rasband, R.L. Sidman, A.A. Habib, and T. Vartanian. 2003. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J. Cell Biol. 163:397-408. doi:10.1083/jcb.200304154 (Pubitemid 37363139)
13. Colognato, H., W. Baron, V. Avellana-Adalid, J.B. Relvas, A. Baron-Van Evercooren, E. Georges-Labouesse, and C. ffrench-Constant. 2002. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 4:833-841. doi:10.1038/ncb865
14. Colognato, H., S. Ramachandrappa, I.M. Olsen, and C. ffrench-Constant. 2004. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J. Cell Biol. 167:365-375. doi:10.1083/jcb. 200404076
15. de Hoog, C.L., L.J. Foster, and M. Mann. 2004. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell. 117:649-662. doi:10.1016/S0092-8674(04)00456-8 (Pubitemid 38692530)
16. Etienne-Manneville, S., and A. Hall. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell. 106:489-498. doi:10.1016/S0092-8674(01)00471-8 (Pubitemid 32786992)
17. Francone, V.P., M.J. Maggipinto, L.D. Kosturko, and E. Barbarese. 2007. The microtubule-associated protein tumor overexpressed gene/cytoskeleton- associated protein 5 is necessary for myelin basic protein expression in oligodendrocytes. J. Neurosci. 27:7654-7662. doi:10.1523/JNEUROSCI.0203-07.2007 (Pubitemid 47093802)
18. Frost, E.E., P.C. Buttery, R. Milner, and C. ffrench-Constant. 1999. Integrins mediate a neuronal survival signal for oligodendrocytes. Curr. Biol. 9:1251-1254. doi:10.1016/S0960-9822(99)80506-5
19. Hoek, K.S., G.J. Kidd, J.H. Carson, and R. Smith. 1998. hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. Biochemistry. 37:7021-7029. doi:10.1021/bi9800247 (Pubitemid 28228140)
20. Hughes, P.E., F. Diaz-Gonzalez, L. Leong, C. Wu, J.A. McDonald, S.J. Shattil, and M.H. Ginsberg. 1996. Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. J. Biol. Chem. 271:6571-6574. doi:10.1074/jbc.271.12.6571
21. Hüttelmaier, S., D. Zenklusen, M. Lederer, J. Dictenberg, M. Lorenz, X. Meng, G.J. Bassell, J. Condeelis, and R.H. Singer. 2005. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature. 438:512-515. doi:10.1038/nature04115 (Pubitemid 41742024)
22. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687. doi:10.1016/S0092-8674(02)00971-6 (Pubitemid 35283958)
23. Jung, M., E. Krämer, M. Grzenkowski, K. Tang, W. Blakemore, A. Aguzzi, K. Khazaie, K. Chlichlia, G. von Blankenfeld, H. Kettenmann, et al. 1995. Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur. J. Neurosci. 7:1245-1265. doi:10.1111/j.1460-9568.1995. tb01115.x
24. Kai, N., M. Mishina, and T. Yagi. 1997. Molecular cloning of Fyn-associated molecules in the mouse central nervous system. J. Neurosci. Res. 48:407-424. doi:10.1002/(SICI)1097-4547(19970601)48:5〈407::AIDJNR3〉3. 0.CO;2-I (Pubitemid 27240813)
25. Kippert, A., K. Trajkovic, L. Rajendran, J. Ries, and M. Simons. 2007. Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J. Neurosci. 27:3560-3570. doi:10.1523/JNEUROSCI.4926-06.2007 (Pubitemid 46515129)
26. Kosturko, L.D., M.J. Maggipinto, G. Korza, J.W. Lee, J.H. Carson, and E. Barbarese. 2006. Heterogeneous nuclear ribonucleoprotein (hnRNP) E1 binds to hnRNP A2 and inhibits translation of A2 response element mRNAs. Mol. Biol. Cell. 17:3521-3533. doi:10.1091/mbc.E05-10-0946 (Pubitemid 44156445)
27. Kwon, S., E. Barbarese, and J.H. Carson. 1999. The cis-acting RNA trafficking signal from myelin basic protein mRNA and its cognate trans-acting ligand hnRNP A2 enhance cap-dependent translation. J. Cell Biol. 147:247-256. doi:10.1083/jcb.147.2.247 (Pubitemid 29496335)
28. Laursen, L.S., C.W. Chan, and C. ffrench-Constant. 2009. An integrin-contactin complex regulates CNS myelination by differential Fyn phosphorylation. J. Neurosci. 29:9174-9185. doi:10.1523/JNEUROSCI.5942-08.2009
29. Lee, K.K., Y. de Repentigny, R. Saulnier, P. Rippstein, W.B. Macklin, and R. Kothary. 2006. Dominant-negative beta1 integrin mice have regionspecific myelin defects accompanied by alterations in MAPK activity. Glia. 53:836-844. doi:10.1002/glia.20343
30. Liang, X., N.A. Draghi, and M.D. Resh. 2004. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J. Neurosci. 24:7140-7149. doi:10.1523/JNEUROSCI.5319-03.2004 (Pubitemid 39096379)
31. Liu, Y., C. Gervasi, and B.G. Szaro. 2008. A crucial role for hnRNP K in axon development in Xenopus laevis. Development. 135:3125-3135. doi:10.1242/dev.022236
32. Lyons, D.A., S.G. Naylor, A. Scholze, and W.S. Talbot. 2009. Kif1b is essential for mRNA localization in oligodendrocytes and development of myelinated axons. Nat. Genet. 41:854-858. doi:10.1038/ng.376
33. McCarthy, K.D., and J. de Vellis. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85:890-902. doi:10.1083/jcb.85.3.890 (Pubitemid 10007455)
34. Messias, A.C., C. Harnisch, A. Ostareck-Lederer, M. Sattler, and D.H. Ostareck. 2006. The DICE-binding activity of KH domain 3 of hnRNP K is affected by c-Src-mediated tyrosine phosphorylation. J. Mol. Biol. 361:470-481. doi:10.1016/j.jmb.2006.06.025 (Pubitemid 44118333)
35. Milner, R., and C. ffrench-Constant. 1994. A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development. 120:3497-3506.
36. Min, Y., K. Kristiansen, J.M. Boggs, C. Husted, J.A. Zasadzinski, and J. Israelachvili. 2009. Interaction forces and adhesion of supported myelin lipid bilayers modulated by myelin basic protein. Proc. Natl. Acad. Sci. USA. 106:3154-3159. doi:10.1073/pnas.0813110106
37. Munro, T.P., R.J. Magee, G.J. Kidd, J.H. Carson, E. Barbarese, L.M. Smith, and R. Smith. 1999. Mutational analysis of a heterogeneous nuclear ribonucleoprotein A2 response element for RNA trafficking. J. Biol. Chem. 274:34389-34395. doi:10.1074/jbc.274.48.34389 (Pubitemid 129511783)
38. Olsen, I.M., and C. ffrench-Constant. 2005. Dynamic regulation of integrin activation by intracellular and extracellular signals controls oligodendrocyte morphology. BMC Biol. 3:25. doi:10.1186/1741-7007-3-25
39. Ostareck, D.H., A. Ostareck-Lederer, M. Wilm, B.J. Thiele, M. Mann, and M.W. Hentze. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell. 89:597-606. doi:10.1016/S0092-8674(00)80241-X (Pubitemid 27511770)
40. Ostareck, D.H., A. Ostareck-Lederer, I.N. Shatsky, and M.W. Hentze. 2001. Lipoxygenase mRNA silencing in erythroid differentiation: The 3′UTR regulatory complex controls 60S ribosomal subunit joining. Cell. 104:281-290. doi:10.1016/S0092-8674(01)00212-4 (Pubitemid 32174843)
41. Ostareck-Lederer, A., D.H. Ostareck, C. Cans, G. Neubauer, K. Bomsztyk, G. Superti-Furga, and M.W. Hentze. 2002. c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs. Mol. Cell. Biol. 22:4535-4543. doi:10.1128/MCB.22.13.4535-4543.2002 (Pubitemid 34620391)
42. Peritz, T., F. Zeng, T.J. Kannanayakal, K. Kilk, E. Eirí ksdóttir, U. Langel, and J. Eberwine. 2006. Immunoprecipitation of mRNA-protein complexes. Nat. Protoc. 1:577-580. doi:10.1038/nprot.2006.82
43. Raju, C.S., C. Göritz, Y. Nord, O. Hermanson, C. López-Iglesias, N. Visa, G. Castelo-Branco, and P. Percipalle. 2008. In cultured oligodendrocytes the A/B-type hnRNP CBF-A accompanies MBP mRNA bound to mRNA trafficking sequences. Mol. Biol. Cell. 19:3008-3019. doi:10.1091/mbc.E07- 10-1083
44. Relucio, J., I.D. Tzvetanova, W. Ao, S. Lindquist, and H. Colognato. 2009. Laminin alters fyn regulatory mechanisms and promotes oligodendrocyte development. J. Neurosci. 29:11794-11806. doi:10.1523/JNEUROSCI.0888-09.2009
45. Smart, F.M., G.M. Edelman, and P.W. Vanderklish. 2003. BDNF induces translocation of initiation factor 4E to mRNA granules: evidence for a role of synaptic microfilaments and integrins. Proc. Natl. Acad. Sci. USA. 100:14403-14408. doi:10.1073/pnas.2436349100 (Pubitemid 37499249)
46. Thiele, B.J., A. Doller, T. Kähne, R. Pregla, R. Hetzer, and V. Regitz-Zagrosek. 2004. RNA-binding proteins heterogeneous nuclear ribonucleoprotein A1, E1, and K are involved in post-transcriptional control of collagen I and III synthesis. Circ. Res. 95:1058-1066. doi:10.1161/01.RES. 0000149166.33833.08 (Pubitemid 39557892)
47. Thisted, T., D.L. Lyakhov, and S.A. Liebhaber. 2001. Optimized RNA targets of two closely related triple KH domain proteins, heterogeneous nuclear ribonucleoprotein K and alphaCP-2KL, suggest distinct modes of RNA recognition. J. Biol. Chem. 276:17484-17496. doi:10.1074/jbc.M010594200
48. Trajkovic, K., A.S. Dhaunchak, J.T. Goncalves, D. Wenzel, A. Schneider, G. Bunt, K.A. Nave, and M. Simons. 2006. Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J. Cell Biol. 172:937-948. doi:10.1083/jcb.200509022
49. Umemori, H., S. Sato, T. Yagi, S. Aizawa, and T. Yamamoto. 1994. Initial events of myelination involve Fyn tyrosine kinase signalling. Nature. 367:572-576. doi:10.1038/367572a0 (Pubitemid 24055518)
50. Wang, Z., H. Colognato, and C. ffrench-Constant. 2007. Contrasting effects of mitogenic growth factors on myelination in neuron-oligodendrocyte cocultures. Glia. 55:537-545. doi:10.1002/glia.20480
51. White, R., C. Gonsior, E.M. Krämer-Albers, N. Stöhr, S. Hüttelmaier, and J. Trotter. 2008. Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J. Cell Biol. 181:579-586. doi:10.1083/jcb.200706164 (Pubitemid 351717505)
52. Yu, W., A. Datta, P. Leroy, L.E. O'Brien, G. Mak, T.S. Jou, K.S. Matlin, K.E. Mostov, and M.M. Zegers. 2005. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell. 16:433-445. doi:10.1091/mbc.E04-05-0435 (Pubitemid 40165545)