β1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination

Journal of Cell Biology

Volumn 177, Issue 6, 2007, Pages 1063-1075

  Nodari, Alessandro ^a   Zambroni, Desirée ^a   Quattrini, Angelo ^a   Court, Felipe A ^a   D'Urso, Alessandra ^a   Recchia, Alessandra ^b   Tybulewicz, Victor L J ^c   Wrabetz, Lawrence ^a   Feltri, M Laura ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; RAC1 PROTEIN; LAMININ; NEUROPEPTIDE; RAC PROTEIN; RAC1 PROTEIN, MOUSE; RAC1 PROTEIN, RAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ELONGATION; CELL MIGRATION; CELL SELECTION; CONTROLLED STUDY; CYTOPLASM; LAMELLAR BODY; MOUSE; MYELINATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; TRANSGENIC MOUSE; ANIMAL; CELL MOTION; CELL SURFACE; CYTOLOGY; METABOLISM; MYELIN SHEATH; PHYSIOLOGY; RAT;

MUS MUSCULUS;

ANIMALS; ANTIGENS, CD29; AXONS; CELL MOVEMENT; CELL SURFACE EXTENSIONS; LAMININ; MICE; MICE, TRANSGENIC; MYELIN SHEATH; NEUROPEPTIDES; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RATS; SCHWANN CELLS;

EID: 34250740938     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200610014     Document Type: Article

References (60)

1. Benard, V., B.P. Bohl, and G.M. Bokoch. 1999. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274:13198-13204.
2. Benninger, Y., T. Thurnerr, J. Pereira, S. Krause, X. Wu, A. Chrostek-Grashoff, D. Herzog, K.-A. Nave, R.J.M. Franklin, D. Meijer, et al. 2007. Essential and distinct codes for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J. Cell. Biol. 177: 1051-1061.
3. Bolis, A., S. Coviello, S. Bussini, G. Dina, C. Pardini, S.C. Previtali, M. Malaguti, P. Morana, U. Del Carro, M.L. Feltri, et al. 2005. Loss of Mtmr2 phosphatase in Schwann cells but not in motor neurons causes Charcot-Marie-Tooth type 4B1 neuropathy with myelin outfoldings. J. Neurosci. 25:8567-8577.
4. Bradley, W.G., and M. Jenkison. 1973. Abnormalities of peripheral nerves in murine muscular dystrophy. J. Neurol. Sci. 18:227-247.
5. Bunge, R.P., M.B. Bunge, and C.F. Eldridge. 1986. Linkage between axonal ensheathment and basal lamina production by Schwann cells. Annu. Rev. Neurosci. 9:305-328.
6. Colognato, H., C. ffrench-Constant, and M.L. Feltri. 2005. Human diseases reveal novel roles for neural laminins. Trends Neurosci. 28:480-486.
7. Cosgaya, J.M., J.R. Chan, and E.M. Shooter. 2002. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science. 298:1245-1248.
8. Cox, E.A., S.K. Sastry, and A. Huttenlocher. 2001. Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol. Biol. Cell. 12:265-277.
9. Del Pozo, M.A., L.S. Price, N.B. Alderson, X.D. Ren, and M.A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008-2014.
10. Del Pozo, M.A., W.B. Kiosses, N.B. Alderson, N. Meller, K.M. Hahn, and M.A. Schwartz. 2002. Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat. Cell Biol. 4:232-239.
11. Del Pozo, M.A., N.B. Alderson, W.B. Kiosses, H.H. Chiang, R.G. Anderson, and M.A. Schwartz. 2004. Integrins regulate Rac targeting by internalization of membrane domains. Science. 303:839-842.
12. Einheber, S., T. Milner, F. Giancotti, and J. Salzer. 1993. Axonal regulation of Schwann cell integrin expression suggests a role for α6β4 in myelination. J. Cell Biol. 123:1223-1236.
13. Feltri, M.L., and L. Wrabetz. 2005. Laminins and their receptors in Schwann cells and hereditary neuropathies. J. Peripher. Nerv. Syst. 10:128-143.
14. Feltri, M.L., S.S. Scherer, R. Nemni, J. Kamholz, H. Vogelbacker, M.O. Scott, N. Canal, V. Quaranta, and L. Wrabetz. 1994. β4 integrin expression in myelinating Schwann cells is polarized, developmentally regulated and axonally dependent. Development. 120:1287-1301.
15. Feltri, M.L., M. D'Antonio, S. Previtali, M. Fasolini, A. Messing, and L. Wrabetz. 1999. P0-Cre transgenic mice for inactivation of adhesion molecules in Schwann cells. Ann. N. Y. Acad. Sci. 883:116-123.
16. Feltri, M.L., D. Graus Porta, S.C. Previtali, A. Nodari, B. Migliavacca, A. Cassetti, A. Littlewood-Evans, L.F. Reichardt, A. Messing, A. Quattrini, et al. 2002. Conditional disruption of β1 integrin in Schwann cells impedes interactions with axons. J. Cell Biol. 156:199-209.
17. Fernandez-Valle, C., L. Gwynn, P.M. Wood, S. Carbonetto, and M.B. Bunge. 1994. Anti-beta 1 integrin antibody inhibits Schwann cell myelination. J. Neurobiol. 25:1207-1226.
18. Fernandez-Valle, C., Y. Tang, J. Ricard, A. Rodenas-Ruano, A. Taylor, E. Hackler, J. Biggerstaff, and J. Iacovelli. 2002. Paxillin binds schwannomin and regulates its density-dependent localization and effect on cell morphology. Nat. Genet. 31:354-362.
19. Gao, Y., J.B. Dickerson, F. Guo, J. Zheng, and Y. Zengh. 2004. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA. 101:7618-7623.
20. Gatto, C.L., B.J. Walker, and S. Lambert. 2003. Local ERM activation and dynamic growth cones at Schwann cell tips implicated in efficient formation of nodes of Ranvier. J. Cell Biol. 162:489-498.
21. Giagulli, C., E. Scarpini, L. Ottoboni, S. Narumiya, E.C. Butcher, G. Constantin, and C. Laudanna. 2004. RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity. 20:25-35.
22. Grove, M., N.H. Komiyama, K.A. Nave, S.G. Grant, D.L. Sherman, and P.J. Brophy. 2007. FAK is required for axonal sorting by Schwann cells. J. Cell Biol. 176:277-282.
23. Haataja, L., J. Groffen, and N. Heisterkamp. 1997. Characterization of RAC3, a novel member of the Rho family. J. Biol. Chem. 272:20384-20388.
24. Hall, A. 2005. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33:891-895.
25. Hall, A., H.F. Paterson, P. Adamson, and A.J. Ridley. 1993. Cellular responses regulated by rho-related small GTP-binding proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340:267-271.
26. Hirsch, E., L. Barberis, M. Brancaccio, O. Azzolino, D. Xu, J.M. Kyriakis, L. Silengo, F.G. Giancotti, G. Tarone, R. Fassler, and F. Altruda. 2002. Defective Rac-mediated proliferation and survival after targeted mutation of the β1 integrin cytodomain. J. Cell Biol. 157:481-492.
27. Jessen, K.R., and R. Mirsky. 2005. The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci. 6:671-682.
28. Jirsova, K., P. Sodaar, V. Mandys, and P.R. Bar. 1997. Cold jet: a method to obtain pure Schwann cell cultures without the need for cytotoxic, apoptosis-inducing drug treatment. J. Neurosci. Methods. 78:133-137.
29. Kaempchen, K., K. Mielke, T. Utermark, S. Langmesser, and C.O. Hanemann. 2003. Upregulation of the Rac1/JNK signaling pathway in primary human schwannoma cells. Hum. Mol. Genet. 12:1211-1221.
30. Kissil, J.L., E.W. Wilker, K.C. Johnson, M.S. Eckman, M.B. Yaffe, and T. Jacks. 2003. Merlin, the product of the Nf2 tumor suppressor gene, is an inhibitor of the p21-activated kinase, Pak1. Mol. Cell. 12:841-849.
31. Kleitman, N., P.M. Wood, and R.P. Bunge. 1991. Tissue culture methods for the study of myelination. In Culturing Nerve Cells. Bradford, Cambridge, MA. 337-377.
32. Laforest, S., J. Milanini, F. Parat, J. Thimonier, and M. Lehmann. 2005. Evidences that beta1 integrin and Rac1 are involved in the overriding effect of laminin on myelin-associated glycoprotein inhibitory activity on neuronal cells. Mol. Cell. Neurosci. 30:418-428.
33. 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.
34. Melendez-Vasquez, C.V., S. Einheber, and J.L. Salzer. 2004. Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J. Neurosci. 24:3953-3963.
35. Miao, H., S. Li, Y.L. Hu, S. Yuan, Y. Zhao, B.P. Chen, W. Puzon-McLaughlin, T. Tarui, J.Y. Shyy, Y. Takada, et al. 2002. Differential regulation of Rho GTPases by β1 and β3 integrins: the role of an extracellular domain of integrin in intracellular signaling. J. Cell Sci. 115:2199-2206.
36. Michailov, G.V., M.W. Sereda, B.G. Brinkmann, T.M. Fischer, B. Haug, C. Birchmeier, L. Role, C. Lai, M.H. Schwab, and K.A. Nave. 2004. Axonal neuregulin-1 regulates myelin sheath thickness. Science. 304:700-703.
37. Nakai, Y., Y. Zheng, M. MacCollin, and N. Ratner. 2006. Temporal control of Rac in Schwann cell-axon interaction is disrupted in NF2-mutant schwannoma cells. J. Neurosci. 26:3390-3395.
38. Nakamura, F. 2001. Biochemical, electron microscopic and immunohistological observations of cationic detergent-extracted cells: detection and improved preservation of microextensions and ultramicroextensions. BMC Cell Biol. 2:10.
39. Nobes, C.D., and A. Hall. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:53-62.
40. Occhi, S., D. Zambroni, U. Del Carro, S. Amadio, K. Campbell, F. Saito, Z. Chen, S. Strickland, E. Sirkowski, S. Scherer, et al. 2005. Both laminin and Schwann cell dystroglycan are necessary for proper clustering of sodium channels at nodes of Ranvier. J. Neurosci. 25:9418-9427.
41. Ojakian, G.K., and R. Schwimmer. 1994. Regulation of epithelial cell surface polarity reversal by beta 1 integrins. J. Cell Sci. 107:561-576.
42. Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K.M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793-802.
43. Parkinson, D., Z. Dong, H. Bunting, J. Whitfield, C. Meier, H. Marie, R. Mirsky, and K.R. Jessen. 2001. Transforming growth factor β (TGFβ) mediates Schwann cell death in vitro and in vivo: examination of c-Jun activation, interactions with survival signals, and the relationship of TGFβ-mediated death to Schwann cell differentiation. J. Neurosci. 21:8572-8585.
44. Saito, F., S.A. Moore, R. Barresi, M.D. Henry, A. Messing, S.E. Ross-Barta, R.D. Cohn, R.A. Williamson, K.A. Sluka, D.L. Sherman, et al. 2003. Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization. Neuron. 38:747-758.
45. Sepp, K.J., and V.J. Auld. 2003. RhoA and Rac1 GTPases mediate the dynamic rearrangement of actin in peripheral glia. Development. 130:1825-1835.
46. Shaw, R.J., J.G. Paez, M. Curto, A. Yaktine, W.M. Pruitt, I. Saotome, J.P. O'Bryan, V. Gupta, N. Ratner, C.J. Der, et al. 2001. The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev. Cell. 1:63-72.
47. Sherman, D.L., and P.J. Brophy. 2005. Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 6:683-690.
48. Stephens, L.E., J.E. Sonne, M.L. Fitzgerald, and C.H. Damsky. 1993. Targeted deletion of β1 integrins in F9 embryonal carcinoma cells affects morphological differentiation but not tissue-specific gene expression. J. Cell Biol. 123:1607-1620.
49. Stirling, C.A. 1975. Abnormalities in Schwann cell sheaths in spinal nerve roots of dystrophic mice. J. Anat. 119:169-180.
50. Suzuki-Inoue, K., Y. Yatomi, N. Asazuma, M. Kainoh, T. Tanaka, K. Satoh, and Y. Ozaki. 2001. Rac, a small guanosine triphosphate-binding protein, and p21-activated kinase are activated during platelet spreading on collagen-coated surfaces: roles of integrin α2β1. Blood. 98:3708-3716.
51. Taveggia, C., G. Zanazzi, A. Petrylak, H. Yano, J. Rosenbluth, S. Einheber, X. Xu, R.M. Esper, J.A. Loeb, P. Shrager, et al. 2005. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron. 47:681-694.
52. Terashima, T., H. Yasuda, M. Terada, S. Kogawa, K. Maeda, M. Haneda, A. Kashiwagi, and R. Kikkawa. 2001. Expression of Rho-family GTPases (Rac, cdc42, RhoA) and their association with p-21 activated kinase in adult rat peripheral nerve. J. Neurochem. 77:986-993.
53. Tsiper, M.V., and P.D. Yurchenco. 2002. Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J. Cell Sci. 115:1005-1015.
54. Walmsley, M.J., S.K. Ooi, L.F. Reynolds, S.H. Smith, S. Ruf, A. Mathiot, L. Vanes, D.A. Williams, M.P. Cancro, and V.L. Tybulewicz. 2003. Critical roles for Rac1 and Rac2 GTPases in B cell development and signaling. Science. 302:459-462.
55. Webster, H.D., R. Martin, and M.F. O'Connell. 1973. The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscopic study. Dev. Biol. 32:401-416.
56. Wrabetz, L., M. Feltri, A. Quattrini, D. Inperiale, S. Previtali, M. D'Antonio, R. Martini, X. Yin, B. Trapp, L. Zhou, et al. 2000. P0 overexpression causes congenital hypomyelination of peripheral nerve. J. Cell Biol. 148:1021-1033.
57. Yamauchi, J., Y. Miyamoto, A. Tanoue, E.M. Shooter, and J.R. Chan. 2005. Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc. Natl. Acad. Sci. USA. 102:14889-14894.
58. Yang, D., J. Bierman, Y.S. Tarumi, Y.P. Zhong, R. Rangwala, T.M. Proctor, Y. Miyagoe-Suzuki, S. Takeda, J.H. Miner, L.S. Sherman, et al. 2005. Coordinate control of axon defasciculation and myelination by laminin-2 and -8. J. Cell Biol. 168:655-666.
59. 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. 2005a. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell. 16:433-445.
60. Yu, W.M., M.L. Feltri, L. Wrabetz, S. Strickland, and Z.L. Chen. 2005b. Schwann cell-specific ablation of laminin gamma1 causes apoptosis and prevents proliferation. J. Neurosci. 25:4463-4472.