CNS Myelin Wrapping Is Driven by Actin Disassembly

Developmental Cell

Volumn 34, Issue 2, 2015, Pages 152-167

  Zuchero, J Bradley ^a   Fu, Meng meng ^a   Sloan, Steven A ^a   Ibrahim, Adiljan ^a   Olson, Andrew ^a   Zaremba, Anita ^b   Dugas, Jason C ^c,f   Wienbar, Sophia ^a   Caprariello, Andrew V ^b   Kantor, Christopher ^b   Leonoudakus, Dmitri ^c   Lariosa Willingham, Karen ^c   Kronenberg, Golo ^d   Gertz, Karen ^d   Soderling, Scott H ^e   Miller, Robert H ^b,g   Barres, Ben A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Myelin Repair Foundation   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f RIGEL PHARMACEUTICALS INC   (United States)

^g GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; MYELIN; MYELIN BASIC PROTEIN; ACTIN; CFL1 PROTEIN, MOUSE; COFILIN 1; GELSOLIN; MBP PROTEIN, MOUSE; SMALL INTERFERING RNA;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MALE; MOUSE; MYELIN SHEATH; MYELINATION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHWANN CELL; SPINAL GANGLION; UPREGULATION; WHITE MATTER; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; CELL MOTION; EMBRYOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; OPTIC NERVE; PHYSIOLOGY; RAT; RNA INTERFERENCE; SPRAGUE DAWLEY RAT;

MAMMALIA; VERTEBRATA;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; AXONS; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; COFILIN 1; GELSOLIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN BASIC PROTEIN; MYELIN SHEATH; OLIGODENDROGLIA; OPTIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84938066482     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.06.011     Document Type: Article

References (46)

1. Aggarwal S., Yurlova L., Snaidero N., Reetz C., Frey S., Zimmermann J., Pähler G., Janshoff A., Friedrichs J., Müller D.J., et al. A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev. Cell 2011, 21:445-456.
2. Baryłko B., Dobrowolski Z. Ca2+-calmodulin-dependent regulation of F-actin-myelin basic protein interaction. Eur. J. Cell Biol. 1984, 35:327-335.
3. Bauer N.G., Richter-Landsberg C., Ffrench-Constant C. Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 2009, 57:1691-1705.
4. Bercury K.K., Macklin W.B. Dynamics and mechanisms of CNS myelination. Dev. Cell 2015, 32:447-458.
5. Boggs J.M., Rangaraj G. Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin. Biochemistry 2000, 39:7799-7806.
6. Dangata Y.Y., Kaufman M.H. Myelinogenesis in the optic nerve of (C57BL x CBA) F1 hybrid mice: a morphometric analysis. Eur. J. Morphol. 1997, 35:3-17.
7. Doerflinger N.H., Macklin W.B., Popko B. Inducible site-specific recombination in myelinating cells. Genesis 2003, 35:63-72.
8. Dugas J.C., Emery B. Purification of oligodendrocyte precursor cells from rat cortices by immunopanning. Cold Spring Harb. Protoc. 2013, 2013:745-758.
9. Emery B., Dugas J.C. Purification of oligodendrocyte lineage cells from mouse cortices by immunopanning. Cold Spring Harb. Protoc. 2013, 2013:854-868.
10. Fletcher D.A., Mullins R.D. Cell mechanics and the cytoskeleton. Nature 2010, 463:485-492.
11. Fox M.A., Afshari F.S., Alexander J.K., Colello R.J., Fuss B. Growth conelike sensorimotor structures are characteristic features of postmigratory, premyelinating oligodendrocytes. Glia 2006, 53:563-566.
12. Gálvez-Santisteban M., Rodríguez-Fraticelli A.E., Bryant D.M., Vergarajauregui S., Yasuda T., Bañón-Rodríguez I., Bernascone I., Datta A., Spivak N., Young K., et al. Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat. Cell Biol. 2012, 14:838-849.
13. Goebbels S., Oltrogge J.H., Kemper R., Heilmann I., Bormuth I., Wolfer S., Wichert S.P., Möbius W., Liu X., Lappe-Siefke C., et al. Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J. Neurosci. 2010, 30:8953-8964.
14. Gould R.M., Dawson R.M. Incorporation of newly formed lecithin into peripheral nerve myelin. J. Cell Biol. 1976, 68:480-496.
15. Hildebrand C., Remahl S., Persson H., Bjartmar C. Myelinated nerve fibres in the CNS. Prog. Neurobiol. 1993, 40:319-384.
16. Hilpelä P., Vartiainen M.K., Lappalainen P. Regulation of the actin cytoskeleton by PI(4,5)P2 and PI(3,4,5)P3. Curr. Top. Microbiol. Immunol. 2004, 282:117-163.
17. Jin F., Dong B., Georgiou J., Jiang Q., Zhang J., Bharioke A., Qiu F., Lommel S., Feltri M.L., Wrabetz L., et al. N-WASp is required for Schwann cell cytoskeletal dynamics, normal myelin gene expression and peripheral nerve myelination. Development 2011, 138:1329-1337.
18. Kim H.-J., DiBernardo A.B., Sloane J.A., Rasband M.N., Solomon D., Kosaras B., Kwak S.P., Vartanian T.K. WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination. J. Neurosci. 2006, 26:5849-5859.
19. Kim I.H., Racz B., Wang H., Burianek L., Weinberg R., Yasuda R., Wetsel W.C., Soderling S.H. Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J. Neurosci. 2013, 33:6081-6092.
20. Kronenberg G., Gertz K., Baldinger T., Kirste I., Eckart S., Yildirim F., Ji S., Heuser I., Schröck H., Hörtnagl H., et al. Impact of actin filament stabilization on adult hippocampal and olfactory bulb neurogenesis. J. Neurosci. 2010, 30:3419-3431.
21. Lappe-Siefke C., Goebbels S., Gravel M., Nicksch E., Lee J., Braun P.E., Griffiths I.R., Nave K.-A. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 2003, 33:366-374.
22. Liu A., Muggironi M., Marin-Husstege M., Casaccia-Bonnefil P. Oligodendrocyte process outgrowth in vitro is modulated by epigenetic regulation of cytoskeletal severing proteins. Glia 2003, 44:264-274.
23. Matthews M.A., Duncan D. A quantitative study of morphological changes accompanying the initiation and progress of myelin production in the dorsal funiculus of the rat spinal cord. J. Comp. Neurol. 1971, 142:1-22.
24. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
25. Nawaz S., Kippert A., Saab A.S., Werner H.B., Lang T., Nave K.-A., Simons M. Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J. Neurosci. 2009, 29:4794-4807.
26. Nawaz S., Schweitzer J., Jahn O., Werner H.B. Molecular evolution of myelin basic protein, an abundant structural myelin component. Glia 2013, 61:1364-1377.
27. Nolen B.J., Tomasevic N., Russell A., Pierce D.W., Jia Z., McCormick C.D., Hartman J., Sakowicz R., Pollard T.D. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 2009, 460:1031-1034.
28. Novak N., Bar V., Sabanay H., Frechter S., Jaegle M., Snapper S.B., Meijer D., Peles E. N-WASP is required for membrane wrapping and myelination by Schwann cells. J. Cell Biol. 2011, 192:243-250.
29. Paluch E.K., Raz E. The role and regulation of blebs in cell migration. Curr. Opin. Cell Biol. 2013, 25:582-590.
30. Readhead C., Popko B., Takahashi N., Shine H.D., Saavedra R.A., Sidman R.L., Hood L. Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype. Cell 1987, 48:703-712.
31. Rosenbluth J. Central myelin in the mouse mutant shiverer. J. Comp. Neurol. 1980, 194:639-648.
32. Schüller U., Heine V.M., Mao J., Kho A.T., Dillon A.K., Han Y.-G., Huillard E., Sun T., Ligon A.H., Qian Y., et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008, 14:123-134.
33. Shine H.D., Readhead C., Popko B., Hood L., Sidman R.L. Morphometric analysis of normal, mutant, and transgenic CNS: correlation of myelin basic protein expression to myelinogenesis. J. Neurochem. 1992, 58:342-349.
34. Snaidero N., Möbius W., Czopka T., Hekking L.H.P., Mathisen C., Verkleij D., Goebbels S., Edgar J., Merkler D., Lyons D.A., et al. Myelin membrane wrapping of CNS axons by PI(3,4,5)P3-dependent polarized growth at the inner tongue. Cell 2014, 156:277-290.
35. Song J., Goetz B.D., Baas P.W., Duncan I.D. Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol. Cell. Neurosci. 2001, 17:624-636.
36. Thurnherr T., Benninger Y., Wu X., Chrostek A., Krause S.M., Nave K.-A., Franklin R.J.M., Brakebusch C., Suter U., Relvas J.B. Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J. Neurosci. 2006, 26:10110-10119.
37. Trapp B.D., Andrews S.B., Wong A., O'Connell M., Griffin J.W. Co-localization of the myelin-associated glycoprotein and the microfilament components, F-actin and spectrin, in Schwann cells of myelinated nerve fibres. J. Neurocytol. 1989, 18:47-60.
38. Wang H., Tewari A., Einheber S., Salzer J.L., Melendez-Vasquez C.V. Myosin II has distinct functions in PNS and CNS myelin sheath formation. J. Cell Biol. 2008, 182:1171-1184.
39. Watkins T.A., Emery B., Mulinyawe S., Barres B.A. Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 2008, 60:555-569.
40. Wilson R., Brophy P.J. Role for the oligodendrocyte cytoskeleton in myelination. J. Neurosci. Res. 1989, 22:439-448.
41. Witke W., Sharpe A.H., Hartwig J.H., Azuma T., Stossel T.P., Kwiatkowski D.J. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell 1995, 81:41-51.
42. Wu C., Asokan S.B., Berginski M.E., Haynes E.M., Sharpless N.E., Griffith J.D., Gomez S.M., Bear J.E. Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 2012, 148:973-987.
43. Yae K., Keng V.W., Koike M., Yusa K., Kouno M., Uno Y., Kondoh G., Gotow T., Uchiyama Y., Horie K., Takeda J. Sleeping beauty transposon-based phenotypic analysis of mice: lack of Arpc3 results in defective trophoblast outgrowth. Mol. Cell. Biol. 2006, 26:6185-6196.
44. Yang Q., Zhang X.-F., Pollard T.D., Forscher P. Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow. J. Cell Biol. 2012, 197:939-956.
45. Zhang Y., Chen K., Sloan S.A., Bennett M.L., Scholze A.R., O'Keeffe S., Phatnani H.P., Guarnieri P., Caneda C., Ruderisch N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 2014, 34:11929-11947.
46. Zuchero J.B. Purification of dorsal root ganglion neurons from rat by immunopanning. Cold Spring Harb. Protoc. 2014, 2014:826-838.