N-WASp is required for Schwann cell cytoskeletal dynamics, normal myelin gene expression and peripheral nerve myelination

Development

Volumn 138, Issue 7, 2011, Pages 1329-1337

  Jin, Fuzi ^a,b   Dong, Baoxia ^a,b   Georgiou, John ^c   Jiang, Qiuhong ^b   Zhang, Jinyi ^b   Bharioke, Arjun ^b,g   Qiu, Frank ^b   Lommel, Silvia ^d   Laura Feltri, M ^e   Wrabetz, Lawrence ^e   Roder, John C ^c   Eyer, Joel ^f   Chen, Xiequn ^a   Peterson, Alan C ^f   Siminovitch, Katherine A ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF BONN   (Germany)

^e SAN RAFFAELE HOSPITAL   (Italy)

^f UNIVERSITÉ D'ANGERS   (France)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Mouse; Myelination; N WASp (Wasl); Schwann cells

Indexed keywords

MYELIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CYTOSKELETON; GENE EXPRESSION; IN VITRO STUDY; MOTOR DYSFUNCTION; MOUSE; MYELINATION; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; SCHWANN CELL;

ANIMALS; AXONS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOSKELETON; FLUORESCENT ANTIBODY TECHNIQUE; GAIT; GENE EXPRESSION; MICE; MICE, KNOCKOUT; MYELIN SHEATH; PERIPHERAL NERVES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHWANN CELLS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

ANIMALIA; MUS;

EID: 79955159546     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.058677     Document Type: Article

References (42)

1. Bacon, C., Lakics, V., Machesky, L. and Rumsby, M. (2007). N-WASP regulates extension of filopodia and processes by oligodendrocyte progenitors, oligodendrocytes, and Schwann cells-implications for axon ensheathment at myelination. Glia 55, 844-858.
2. Badour, K., Zhang, J., Shi, F, Leng, Y., Collins, M. and Siminovitch, K. A. (2004). Fyn and PTP-PEST-mediated regulation of Wiskott-Aldrich syndrome protein (WASp) tyrosine phosphorylation is required for coupling T cell antigen receptor engagement to WASp effector function and T cell activation. J. Exp. Med. 199, 99-112.
3. Benninger, Y., Thurnherr, T., Pereira, J. A., Krause, S., Wu, X., Chrostek-Grashoff, A., Herzog, D., Nave, K. A., Franklin, R. J., Meijer, D. et al. (2007). Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J. Cell Biol. 177, 1051-1061.
4. Bray, G., Perkins, S., Peterson, A. and Aguayo, A. (1977). Schwann cell multiplication deficit in nerve roots of newborn dystrophic mice. J. Neurol. Sci. 32, 203-212.
5. Brown, M. J. and Asbury, A. K. (1981). Schwann cell proliferation in the postnatal mouse: timing and topography. Exp. Neurol. 74, 170-186.
6. Bunge, R. P., Bunge, M. B. and Bates, M. (1989). Movements of the Schwann cell nucleus implicate progression of inner (axons related) Schwann cell process during myelination. J. Cell Biol. 109, 273-284.
7. Eldrige, C. F., Bunge, M. B., Bunge, R. P. and Wood, P. M. (1987). Differentiation of axon-related Schwann cells in vitro. I. Ascorbic acid regulates basal lamina assembly and myelin formation. J. Cell Biol. 105, 1023-1034.
8. Feltri, M. L., D'Antonio, M., Previtali, S., Fasolini, M., Messing, A. and Wrabetz, L. (1999a). P0-Cre transgenic mice for inactivation of adhesion molecules in Schwann cells. Ann. N. Y. Acad. Sci. 883, 116-123.
9. Feltri, M. L., D'Antonio, M., Quattrini, A., Numerato, R., Arona, M., Previtali, S., Chiu, S. Y., Messing, A. and Wrabetz, L. (1999b). A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur. J. Neurosci. 11, 1577-1586.
10. Feltri, M. L., Porta, D. G., Previtali, S. C., Nodari, A., Migliavacca, B., Cassetti, A., Littlewood-Evans, A., Reichardt, L. F., Messing, A., Quattrini, A. et al. (2002). Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J. Cell Biol. 156, 199-209.
11. Feltri, M. L., Suter, U. and Relvas, J. B. (2008). The function of RhoGTPases in axon ensheathment and myelination. Glia 56, 1508-1517.
12. Fernandez-Valle, C., Gorman, D., Gomez, A. M. and Bunge, M. B. (1997). Actin plays a role in both changes in cell shape and gene expression associated with Schwann cell myelination. J. Neurosci. 17, 241-250.
13. Ferrai, C., Naum-Onganía, G., Longobardi, E., Palazzolo, M., Disanza, A., Diaz, V. M., Crippa, M. P., Scita, G. and Blasi, F. (2009). Induction of HoxB transcription by retinoic acid requires actin polymerization. Mol. Biol. Cell 20, 3543-3551.
14. Gatto, C. L., Walker, B. J. and Lambert, S. (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.
15. Ghislain, J. and Charnay, P. (2006). Control of myelination in Schwann cells: a Krox20 cis-regulatory element integrates Oct6, Brn2 and Sox10 activities. EMBO Rep. 7, 52-58.
16. Gieni, R. S. and Hendzel, M. J. (2009). Actin dynamics and functions in the interphase nucleus: moving toward an understanding of nuclear polymeric actin. Biochem. Cell Biol. 87, 283-306.
17. Grove, M., Komiyama, N. H., Nave, K. A., Grant, S. G., Sherman, D. L. and Brophy, P. J. (2007). FAK is required for axonal sorting by Schwann cells. J. Cell Biol. 176, 277-282.
18. Honkanen, H., Lahti, O., Nissinen, M., Myllylä, R. M., Kangas, S., Päiväläinen, S., Alanne, M. H., Peltonen, S., Peltonen, J. and Heape, A. M. (2007). Isolation, purification and expansion of myelination-competent, neonatal mouse Schwann cells. Eur. J. Neurosci. 26, 953-964.
19. Jessen, K. R., Brennan, A., Morgan, L., Mirsky, R., Kent, A., Hashimoto, Y. and Gavrilovic, J. (1994). The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12, 509-527.
20. Kim, H. J., DiBernardo, A. B., Sloane, J. A., Rasband, M. N., Solomon, D., Kosaras, B., Kwak, S. P. and Vartanian, T. K. (2006). WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination. J. Neurosci. 26, 5849-5859.
21. Lemke, G. and Chao, M. (1988). Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 102, 499-504.
22. Lommel, S., Benesch, S., Rottner, K., Franz, T., Wehland, J. and Kuhn, R. (2001). Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASp-defective cells. EMBO Rep. 2, 850-857.
23. Lommel, S., Benesch, S., Rohde, M., Wehland, J. and Rottner, K. (2004). Enterohaemorrhagic and enteropathogenic Escherichia coli use different mechanisms for actin pedestal formation that converge on N-WASP. Cell. Microbiol. 6, 243-254.
24. Melendez-Vasquez, C. V., Einheber, S. and Salzer, J. L. (2004). Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J. Neurosci. 24, 3953-3963.
25. Nave, K. A. (2010). Myelination and the trophic support of long axons. Nat. Rev. Neurosci. 11, 275-283.
26. Nodari, A., Zambroni, D., Quattrini, A., Court, F. A., D'Urso, A., Recchia, A., Tybulewicz, V. L., Wrabetz, L. and Feltri, M. L. (2007). Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J. Cell Biol. 177, 1063-1075.
27. Novak, A., Guo, C., Yang, W., Nagy, A. and Lobe, C. G. (2000). Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28, 147-155.
28. Ory, S. and Gasman, S. (2010). Rho GTPases and exocytosis: what are the molecular links? Semin. Cell Dev. Biol. 22, 27-32.
29. Päiväläinen, S., Nissinen, M., Honkanen, H., Lahti, O., Kangas, S. M., Peltonen, J., Peltonen, S. and Heape, A. M. (2008). Myelination in mouse dorsal root ganglion/Schwann cell cocultures. Mol. Cell. Neurosci. 37, 568-578.
30. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29, 9.
31. Rajasekharan, S., Baker, K. A., Horn, K. E., Jarjour, A. A., Antel, J. P. and Kennedy, T. E. (2009). Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA. Development 136, 415-426.
32. Svaren, J. and Meijer, D. (2008). The molecular machinery of myelin gene transcription in Schwann cells. Glia 56, 1541-1551.
33. Taylor, M. D., Sadhukhan, S., Kottangada, P., Ramgopal, A., Sarkar, K., D'Silva, S., Selvakumar, A., Candotti, F. and Vyas, Y. M. (2010). Nuclear role of WASp in pathogenesis of dysregulated TH1 immunity in human Wiskott-Aldrich syndrome. Sci. Transl. Med. 2, 37ra44.
34. Tsuchiya, D., Kitamura, Y., Takata, K., Sugisaki, T., Taniguchi, T., Uemura, K., Miki, H., Takenawa, T. and Shimohama, S. (2006). Developmental expression of neural Wiskott-Aldrich syndrome protein (N-WASP) and WASP family verprolin-homologous protein (WAVE)-related proteins in postnatal rat cerebral cortex and hippocampus. Neurosci. Res. 56, 459-469.
35. Wanner, I. B., Mahoney, J., Jessen, K. R., Wood, P. M., Bates, M. and Bunge, M. B. (2006). Invariant mantling of growth cones by Schwann cell precursors characterize growing peripheral nerve fronts. Glia 54, 424-438.
36. Webster, H. (1984). Development of peripheral nerve fibers. In Peripheral Neuropathy (ed. P. T. Dyck, E. H. Lambert and R. Bunges), pp. 329-359. Philadelphia, PA: W. B. Saunders.
37. Webster, H. D. (1971). The geometry of peripheral myelin sheaths during their formation and growth in rat-sciatic nerves. J. Cell Biol. 48, 348-367.
38. Webster, H. D., Martin, R. and O'Connell, M. F. (1973). The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscopic study. Dev. Biol. 32, 401-416.
39. Wegner, A. M., Nebhan, C. A., Hu, L., Majumdar, D., Meier, K. M., Weaver, A. M. and Webb, D. J. (2008). N-WASp and the Arp2/3 complex are critical regulators of actin in the development of dendritic spines and synapses. J. Biol. Chem. 283, 15912-15920.
40. Wood, P., Moya, F., Eldridge, C., Owens, G., Ranscht, B., Schachner, M., Bunge, M. and Bunge, R. (1990). Studies of the initiation of myelination by Schwann cells. Ann. N. Y. Acad. Sci. 605, 1-14.
41. Woodhoo, A. and Sommer, L. (2008). Development of the Schwann cell lineage: from the neural crest to the myelinated nerve. Glia 56, 1481-1490.
42. Woodhoo, A., Alonso, M. B., Droggiti, A., Turmaine, M., D'Antonio, M., Parkinson, D. B., Wilton, D. K., Al-Shawi, R., Simons, P., Shen, J. et al. (2009). Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat. Neurosci. 12, 839-847.