N-WASP regulates extension of filopodia and processes by oligodendrocyte progenitors, oligodendrocytes, and Schwann cells - Implications for axon ensheathment at myelination

GLIA

Volumn 55, Issue 8, 2007, Pages 844-858

  Bacon, Claire ^a   Lakics, Viktor ^b   Machesky, Laura ^c   Rumsby, Martin ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b ELI LILLY AND COMPANY   (United States)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Axon ensheathment; Differentiation; Motility; Myelination; Oligodendrocytes; Schwann cells; WASP WAVE proteins

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; FILOPODIUM; MYELINATION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SCHWANN CELL;

ACTINS; ANIMALS; CARBAZOLES; CELL LINE; COCULTURE TECHNIQUES; CORTACTIN; GANGLIA, SPINAL; GENE EXPRESSION; MICROSCOPY, ELECTRON, SCANNING; MYELIN SHEATH; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; OPTIC NERVE; PROPANOLAMINES; PSEUDOPODIA; RATS; SCHWANN CELLS; STEM CELLS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 34249105474     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20505     Document Type: Article

References (83)

1. Asou H, Hamada K, Sakota T. 1995. Visualization of a single myelination process of an oligodendrocyte in culture by video microscopy. Cell Struct Funct 20:59-70.
2. Begum R, Nur-E-Kamal MSA, Zaman MA. 2004. The role of RhoGT-Pases in the regulation of the rearrangement of actin cytoskeleton and cell movement. Exp Mol Med 36:358-366.
3. Bretschneider T, Diez S, Anderson K, Heuser J, Clarke M, Muller-Taubenberger A, Kohler J, Gerisch G. 2004. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol 14:1-10.
4. Bunge RP, Bunge MB, Bates M. 1989. Movements of the Schwann cell nucleus implicate progression of the inner (axon related) Schwann cell process during myelination. J Cell Biol 109:273-284.
5. Chen S, Velardez MO, Warot X, Yu ZX, Miller SJ, Cros D, Corfas G. 2006. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 26:3079-3086.
6. Chernousov MA, Rothblum K, Stahl RC, Evans A, Prentiss L, Carey DJ. 2006. Glypican-1 and α4(V) collagen are required for Schwann cell myelination. J Neurosci 26:508-517.
7. Chun SJ, Rasband MN, Sidman RL, Habib AA, Vartanian T. 2003. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol 163:397-408.
8. Daly RJ. 2004. Cortactin signalling and dynamic actin networks. Biochem J 382:13-25.
9. Dawson J, Hotchin N, Lax S, Rumsby M. 2003. Lysophosphatidic acid induces process retraction in CG-4 line oligodendrocytes and oligodendrocyte precursor cells but not in differentiated oligodendrocytes. J Neurochem 87:947-957.
10. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793.
11. Etienne-Manneville S. 2004. Actin and microtubules in cell motility: Which one is in control? Traffic 5:470-477.
12. Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL Jr, Colman DR. 1995. Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherent junctions. J Cell Biol 129:189-202.
13. Feltri ML, Graus PD, Previtali SC, Nodari A, Migliavacca B, Cassetti A, Littlewood-Evans A, Reichardt LF, Messing A, Quattrini A, Mueller U, Wrabetz L. 2002. Conditional disruption of β 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156:199-209.
14. Fernandez-Valle C, Gwynn L, Wood PR, Carbonetto S, Bunge MB. 1994. Anti-β1 integrin antibody inhibits Schwann cell myelination. J Neurobiol 25:1207-1226.
15. Fernandez-Valle C, Gorman D, Gomez AM, Bunge MB. 1997. Actin plays a role in both changes in cell shape and gene expression associated with Schwann cell myelination. J Neurosci 17:241-250.
16. Garratt AN, Britsch S, Birchmeier C. 2000. Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 22:987-996.
17. Hall A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
18. Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, Trapp BD. 1999. Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival. J Cell Biol 146:1173-1183.
19. Horwitz AR, Parsons JT. 1999. Cell migration-movin' on. Science 286:1102-1103.
20. Ibarra N, Polliti A, Insali RH. 2005. Regulation of actin assembly by SCAR/WAVE proteins. Biochem Soc Trans 33:1243-1246.
21. Innocenti M, Zucconi A, Disanza A, Frittoli E, Areces LB, Steffen A, Stradai T, Di Fiore PP, France-Carlier M, Scita G. 2004. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat Cell Biol 6:319-327.
22. Kempiak SJ, Yamaguchi H, Sarmiento C, Sidani M, Ghosh M, Eddy RJ, Desmarais V, Way M, Condeelis J, Segali JE. 2005. A neural Wiskott-Aldrich Syndrome protein-mediated pathway for localized activation of actin polymerization that is regulated by cortactin. J Biol Chem 280:5836-5842.
23. Kim HJ, DiBernardo AB, Sloane JA, Rasband MN, Solomon D, Kosaras B, Kwak SP, Vartanian TK. 2006. WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination. J Neurosci 26:5849-5859.
24. Kovacs EM, Makar RS, Gertler FB. 2006. Tuba stimulates intracellular N-WASP-dependent actin assembly. J Cell Sci 119:2715-2726.
25. Kowalski JR, Egile C, Gil S, Snapper SB, Li R, Thomas SM. 2005. Cortactin regulates cell migration through activation of N-WASP. J Cell Sci 118:79-87.
26. Kunda P, Craig G, Dominguez V, Baum B. 2003. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr Biol 13:1867-1875.
27. Letourneau PC, Roche FK, Shattuck TA, Lemmon V, Takeichi M. 1991. Interactions of Schwann cells with neurites and with other Schwann cells involve the calcium-dependent adhesion molecule, N-cadherin. J Neurobiol 22:707-720.
28. Lunn KF, Baas PW, Duncan ID. 1997. Microtubule organization and stability in the oligodendrocyte. J Neurosci 17:4921-4932.
29. Machesky LM. 2002. Sharks' teeth and dunes. Nature 417:494-497.
30. Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J Cell Biol 127:107-115.
31. Machesky LM, Insali RH. 1998. Scar1 and the related Wiskott-Aldrich syndrome protein WASP regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 8:1347-1356.
32. Machesky LM, Insali RH. 1999. Signalling to actin dynamics. J Cell Biol 146:267-272.
33. Machesky LM, Mullins RD, Higgs HN, Kaiser DA, Blanchoin L, May RC, Hall ME, Pollard TD. 1999. Scar, a WASP-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 96:3739-3744.
34. Melendez-Vasquez CV, Einheber S, Salzer JL. 2004. Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J Neurosci 24:3953-3963.
35. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA. 2004. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703.
36. Miki H, Sasaki T, Takai Y, Takenawa T. 1998a. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASR Nature 391:93-96.
37. Miki H, Suetsugu S, Takenawa T. 1998b. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J 17:6932-6941.
38. Miki H, Takenawa T. 2003. Regulation of actin dynamics by WASP family proteins. J Biochem (Tokyo) 134:309-313.
39. Miki H, Yamaguchi H, Suetsugu S, Takenawa T. 2000. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408:732-735.
40. Millard TH, Sharp SJ, Machesky LM. 2004. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380:1-17.
41. Mitchison TJ, Cramer LP. 1996. Actin-based cell motility and cell locomotion. Cell 84:371-379.
42. Moreau V, Madania RP, Martin RP, Winsor B. 1996. The Saccharomyces cerevisiae actin-related protein Arp2 is involved in the actin cytoskeleton. J Cell Biol 134:117-132.
43. Mullins RD, Heuser JA, Pollard TD. 1998a. The interaction of Arp2/3 complex with actin: Nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95:6181-6186.
44. Mullins RD, Kelleher JF, Xu J, Pollard TD. 1998b. Arp2/3 complex from Acanthamoeba binds profilin and cross links actin filaments. Mol Biol Cell 9:841-852.
45. Mullins RD, Stafford WF, Pollard TD. 1997. Structure, subunit topology, and actin binding activity of the Arp 2/3 complex from Acanthamoeba. J Cell Biol 136:331-343.
46. Oh LYS, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW. 1999. Matrix metalloproteinase-9/Gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 19:8464-8475.
47. Oikawa T, Yamaguchi H, Itoh T, Kato M, Ijuin T, Yamazaki D, Suetsugu S, Takenawa T. 2004. PtdIns(3, 4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat Cell Biol 6:420-426.
48. Owens GC, Boyd CJ. 1991. Expressing antisense PoRNA in Schwann cells perturbs myelination. Development 112:639-649.
49. Payne HR, Hemperly JJ, Lemmon V. 1996. N-cadherin expression and function in cultured oligodendrocytes. Dev Brain Res 97:9-15.
50. Peters A, Palay SL, Webster H. 1976. The fine structure of the nervous system: the neurons and supporting cells. Philadelphia: W.B. Saunders.
51. Peterson JR, Bickford LC, Morgan D, Kim AS, Ouerfelli O, Kirschner MW, Rosen MK. 2004. Chemical inhibition of N-WASP by stabilisation of a native autoinhibited conformation. Nat Struct Mol Biol 11:747-755.
52. Peterson JR, Golemis EA. 2004. Autoinhibited proteins as promising drug targets. J Cell Biochem 93:68-73.
53. Peterson JR, Lokey RS, Mitchison TJ, Kirschner MW. 2001. A chemical inhibitor of N-WASP reveals a new mechanism for targeting protein interactions. Proc Natl Acad Sci USA 98:10624-10629.
54. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
55. Quarles RH. 2002. Myelin sheaths: Glycoproteins involved in their formation, maintenance and degeneration. Cell Mol Life Sci 59:1851-1871.
56. Ridley AJ. 1994. Membrane ruffling and signal transduction. Bioessays 16:321-327.
57. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599-609.
58. Rumsby M, Afsari F, Stark M, Hughson E. 2003. Microfilament and microtubule organisation and dynamics in process extension by central glia-4 oligodendrocytes: Evidence for a microtubule organising center. Glia 42:118-129.
59. Rumsby MG, Crang AJ. 1977. The myelin sheath-a structural examination. Cell Surf Rev 4:247-362.
60. Sagane K, Hayakawa K, Kai J, Hirohashi T, Takahashi E, Miyamoto N, Ino M, Oki T, Yamazaki K, Nagasu T. 2005. Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neurosci 6:33.
61. Saito F, Moore SA, Barresi R, Henry MD, Messing A, Ross-Barta SE, Cohn RD, Williamson RA, Sluka KA, Sherman DL, Brophy PJ, Schmeizer JD, Low PA, Wrabetz L, Feltri ML, Campbell KP. 2003. Unique role of dystroglycan in peripheral nerve myelination, nodal structure and sodium channel stabilisation. Neuron 38:747-758.
62. Schnadelbach O, Ozen I, Blaschuk OW, Gour BJ, Meyer RL, Fawcett JW. 2001. N-Cadherin is involved in axon-oligodendrocyte contact and myelination. Mol Cell Neurosci 17:1084-1093.
63. Sheetz MP, Felsenfeld DP, Galbraith CG. 1998. Cell migration: Regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol 8:51-54.
64. Sherman DL, Brophy PJ. 2005. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683-690.
65. Simpson PB, Armstrong RC. 1999. Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration. Glia 26:22-35.
66. Small JV, Stradai T, Vignai E, Rottner K. 2002. The Lamellipodium: Where motility begins. Trends Cell Biol 12:112-120.
67. Song J, Carson JH, Barbarese E, Li FY, Duncan ID. 2003. RNA transport in oligodendrocytes from the taiep mutant rat. Mol Cell Neurosci 24:926-938.
68. Song J, Goetz BD, Baas PW, Duncan ID. 2001. Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol Cell Neurosci 17:624-636.
69. Stovold CF, Millard TH, Machesky LM. 2005. Inclusion of Scar/ WAVE3 in a similar complex to Scar/WAVE1 and 2. BMC Cell Biol 6:11.
70. Stradal T, Rottner K, Disanza A, Confalonieri S, Innocenti M, Scita G. 2004. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol 14:303-311.
71. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T. 2003. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5:595-609.
72. Svitkina TM, Borisy GG. 1999. Apr2/3 complex and actin depolymerising factor/cofilin in dendritic organisation and treadmilling of actin filament array in lamellipodia. J Cell Biol 145:1009-1026.
73. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG. 2003. Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160:409-421.
74. Takenawa T, Miki H. 2001. WASP and WAVE family proteins: Key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114:1801-1809.
75. Uhm JH, Dooley NP, Oh LYS, Yong VW. 1998. Oligodendrocytes utilise a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 22:53-63.
76. Urano T, Liu J, Zhang P, Fan Y, Egile C, Li R, Mueller SC, Zhan X. 2001. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3:259-266.
77. Wanner I, Wood P. 2002. N-cadherin mediates axon-aligned process growth and cell-cell interaction in rat Schwann cells. J Neurosci 22:4066-4079.
78. Weaver AM, Young ME, Lee WL, Cooper JA. 2003. Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol 15:23-30.
79. Whitmore AV, Lindsten T, Raff MC, Thompson CB. 2003. The proapoptotic proteins Bax and Bak are not involved in Wallerian degeneration. Cell Death Diff 10:260-261.
80. Wittmann T, Bokoch GM, Waterman-Storer CM. 2003. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J Cell Biol 161:845-851.
81. Yamagishi A, Masuda M, Ohki T, Onishi H, Mochizuki N. 2004. A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J Biol Chem 279:14929-14936.
82. Yamazaki D, Fujiwara T, Suetsugu S, Takenawa T. 2005. A novel function of WAVE in lamellipodia: WAVE1 is required for stabilization of lamellipodial protrusions during cell spreading. Genes Cells 10:381-392
83. Yin X, Crawford TO, Griffin JW, Tu P, Lee VM, Li C, Roder J, Trapp BD. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18:1953-1962.