Dystroglycan promotes filopodial formation and process branching in differentiating oligodendroglia

Journal of Neurochemistry

Volumn 120, Issue 6, 2012, Pages 928-947

  Eyermann, Christopher ^a   Czaplinski, Kevin ^a   Colognato, Holly ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Dystroglycan; FAK; Laminin; Oligodendrocyte; Outgrowth; Process branching

Indexed keywords

DYSTROGLYCAN; FOCAL ADHESION KINASE; GREEN FLUORESCENT PROTEIN; LAMININ; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FILOPODIUM; MOUSE; MYELINATED NERVE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ACTINS; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; DYSTROGLYCANS; FOCAL ADHESION KINASE 1; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; INTERFERON-BETA; LAMININ; OLIGODENDROGLIA; PHOSPHORIC DIESTER HYDROLASES; PSEUDOPODIA; RATS; RNA, SMALL INTERFERING; STATISTICS, NONPARAMETRIC; STEM CELLS; TIME FACTORS; TRANSFECTION;

MUS;

EID: 84857913607     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07600.x     Document Type: Article

References (51)

1. Barresi R. and Campbell K. P. (2006) Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207. (Pubitemid 43210689)
2. Barros C. S., Nguyen T., Spencer K. S., Nishiyama A., Colognato H. and Muller U. (2009) Beta1 integrins are required for normal CNS myelination and promote AKT-dependent myelin outgrowth. Development 136, 2717-2724.
3. Batchelor C. L., Higginson J. R., Chen Y. J., Vanni C., Eva A. and Winder S. J. (2007) Recruitment of Dbl by ezrin and dystroglycan drives membrane proximal Cdc42 activation and filopodia formation. Cell Cycle 6, 353-363.
4. Bauer N. G., Richter-Landsberg C. and ffrench-Constant C. (2009) Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 57, 1691-1705.
5. Beggs H. E., Schahin-Reed D., Zang K., Goebbels S., Nave K. A., Gorski J., Jones K. R., Sretavan D. and Reichardt L. F. (2003) FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501-514. (Pubitemid 37494700)
6. Benninger Y., Colognato H., Thurnherr T., Franklin R. J., Leone D. P., Atanasoski S., Nave K. A., ffrench-Constant C., Suter U. and Relvas J. B. (2006) Beta1-integrin signaling mediates premyelinating oligodendrocyte survival but is not required for CNS myelination and remyelination. J. Neurosci. 26, 7665-7673. (Pubitemid 44315186)
7. Berti C., Bartesaghi L., Ghidinelli M., Zambroni D., Figlia G., Chen Z. L., Quattrini A., Wrabetz L. and Feltri M. L. (2011) Non-redundant function of dystroglycan and beta1 integrins in radial sorting of axons. Development 138, 4025-4037.
8. Bottenstein J. E. and Sato G. H. (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA. 76, 541-517.
9. Buttery P. C. and ffrench-Constant C. (1999) Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 14, 199-212.
10. Camara J., Wang Z., Nunes-Fonseca C. et al. (2009) Integrin-mediated axoglial interactions initiate myelination in the central nervous system. J. Cell Biol. 185, 699-712.
11. Cavaldesi M., Macchia G., Barca S., Defilippi P., Tarone G. and Petrucci T. C. (1999) Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J. Neurochem. 72, 1648-1655. (Pubitemid 29140840)
12. Chen Y. J., Spence H. J., Cameron J. M., Jess T., Ilsley J. L. and Winder S. J. (2003) Direct interaction of beta-dystroglycan with F-actin. Biochem. J. 375, 329-337.
13. Chun S. J., Rasband M. N., Sidman R. L., Habib A. A. and Vartanian T. (2003) Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J. Cell Biol. 163, 397-408. (Pubitemid 37363139)
14. Clement E., Mercuri E., Godfrey C. et al. (2008) Brain involvement in muscular dystrophies with defective dystroglycan glycosylation. Ann. Neurol. 64, 573-582.
15. Colognato H., Baron W., Avellana-Adalid V., Relvas J. B., Baron-Van Evercooren A., Georges-Labouesse E. and ffrench-Constant C. (2002) CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 4, 833-841. (Pubitemid 35331357)
16. Colognato H., Galvin J., Wang Z., Relucio J., Nguyen T., Harrison D., Yurchenco P. D. and ffrench-Constant C. (2007) Identification of dystroglycan as a second laminin receptor in oligodendrocytes, with a role in myelination. Development 134, 1723-1736. (Pubitemid 46796569)
17. Court F. A., Hewitt J. E., Davies K., Patton B. L., Uncini A., Wrabetz L. and Feltri M. L. (2009) A laminin-2, dystroglycan, utrophin axis is required for compartmentalization and elongation of myelin segments. J. Neurosci. 29, 3908-3919.
18. Dent E. W., Kwiatkowski A. V., Mebane L. M. et al. (2007) Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9, 1347-1359. (Pubitemid 350201748)
19. Driss A., Charrier L., Yan Y., Nduati V., Sitaraman S. and Merlin D. (2006) Dystroglycan receptor is involved in integrin activation in intestinal epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G1228-G1242. (Pubitemid 43788306)
20. Feltri M. L., Graus Porta D., Previtali S. C. et al. (2002) Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J. Cell Biol. 156, 199-209. (Pubitemid 34846947)
21. Ferletta M., Kikkawa Y., Yu H., Talts J. F., Durbeej M., Sonnenberg A., Timpl R., Campbell K. P., Ekblom P. and Genersch E. (2003) Opposing roles of integrin alpha6Abeta1 and dystroglycan in laminin-mediated extracellular signal-regulated kinase activation. Mol. Biol. Cell 14, 2088-2103. (Pubitemid 36583555)
22. Forrest A. D., Beggs H. E., Reichardt L. F., Dupree J. L., Colello R. J. and Fuss B. (2009) Focal adhesion kinase (FAK): a regulator of CNS myelination. J. Neurosci. Res. 87, 3456-3464.
23. Hoshina N., Tezuka T., Yokoyama K., Kozuka-Hata H., Oyama M. and Yamamoto T. (2007) Focal adhesion kinase regulates laminin-induced oligodendroglial process outgrowth. Genes Cells 12, 1245-1254. (Pubitemid 350042422)
24. Jang K. J., Kim M. S., Feltrin D., Jeon N. L., Suh K. Y. and Pertz O. (2010) Two distinct filopodia populations at the growth cone allow to sense nanotopographical extracellular matrix cues to guide neurite outgrowth. PLoS ONE 5, e15966.
25. Jones K. J., Morgan G., Johnston H., Tobias V., Ouvrier R. A., Wilkinson I. and North K. N. (2001) The expanding phenotype of laminin alpha2 chain (merosin) abnormalities: case series and review. J. Med. Genet. 38, 649-657. (Pubitemid 32946785)
26. 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. (Pubitemid 44315279)
27. Lafrenaye A. D. and Fuss B. (2010) Focal adhesion kinase can play unique and opposing roles in regulating the morphology of differentiating oligodendrocytes. J. Neurochem. 115, 269-282.
28. Lunn K. F., Baas P. W. and Duncan I. D. (1997) Microtubule organization and stability in the oligodendrocyte. J. Neurosci. 17, 4921-4932. (Pubitemid 27263806)
29. Matsumura K., Yamada H., Saito F., Sunada Y. and Shimizu T. (1997) Peripheral nerve involvement in merosin-deficient congenital muscular dystrophy and dy mouse. Neuromusc. Disord. 7, 7-12. (Pubitemid 27122405)
30. Mattila P. K. and Lappalainen P. (2008) Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-54. (Pubitemid 351733400)
31. McCarthy K. D. and de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902. (Pubitemid 10007455)
32. Milner R. and ffrench-Constant C. (1994) A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development 120, 3497-3506.
33. Mitra S. K., Hanson D. A. and Schlaepfer D. D. (2005) Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68. (Pubitemid 40064899)
34. Miyagoe-Suzuki Y., Nakagawa M. and Takeda S. (2000) Merosin and congenital muscular dystrophy. Microsc. Res. Tech. 48, 181-191. (Pubitemid 30086191)
35. Moore C. J. and Winder S. J. (2010) Dystroglycan versatility in cell adhesion: a tale of multiple motifs. Cell Commun. Signal. 8, 3.
36. Moore S. A., Saito F., Chen J. et al. (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418, 422-425. (Pubitemid 34826842)
37. Mostoslavsky G., Fabian A. J., Rooney S., Alt F. W. and Mulligan R. C. (2006) Complete correction of murine Artemis immunodeficiency by lentiviral vector-mediated gene transfer. Proc. Natl Acad. Sci. USA 103, 16406-16411. (Pubitemid 44715209)
38. Nodari A., Previtali S. C., Dati G. et al. (2008) Alpha6beta4 integrin and dystroglycan cooperate to stabilize the myelin sheath. J. Neurosci. 28, 6714-6719.
39. Occhi S., Zambroni D., Del Carro U. 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. (Pubitemid 41464755)
40. O'Meara R. W., Michalski J. P. and Kothary R. (2010) Integrin signaling in oligodendrocytes and its importance in CNS myelination. J. Signal Transduct. 2011, 354091.
41. Relucio J., Tzvetanova I. D., Ao W., Lindquist S. and Colognato H. (2009) Laminin alters fyn regulatory mechanisms and promotes oligodendrocyte development. J. Neurosci. 29, 11794-11806.
42. Richter-Landsberg C. (2008) The cytoskeleton in oligodendrocytes. Microtubule dynamics in health and disease. J. Mol. Neurosci. 35, 55-63.
43. Rumsby M., Afsari F., Stark M. and Hughson E. (2003) Microfilament and microtubule organization and dynamics in process extension by central glia-4 oligodendrocytes: evidence for a microtubule organizing center. Glia 42, 118-129. (Pubitemid 36565116)
44. Saito F., Moore S. A., Barresi R. et al. (2003) Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization. Neuron 38, 747-758. (Pubitemid 36694781)
45. Satz J. S., Barresi R., Durbeej M., Willer T., Turner A., Moore S. A. and Campbell K. P. (2008) Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J. Neurosci. 28, 10567-10575.
46. Satz J. S., Ostendorf A. P., Hou S. et al. (2010) Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J. Neurosci. 30, 14560-14572.
47. Song J., Goetz B. D., Baas P. W. and Duncan I. D. (2001) Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol. Cell. Neurosci. 17, 624-636. (Pubitemid 32430039)
48. Spence H. J., Chen Y. J., Batchelor C. L., Higginson J. R., Suila H., Carpen O. and Winder S. J. (2004) Ezrin-dependent regulation of the actin cytoskeleton by beta-dystroglycan. Hum. Mol. Genet. 13, 1657-1668. (Pubitemid 39136721)
49. Thompson O., Kleino I., Crimaldi L., Gimona M., Saksela K. and Winder S. J. (2008) Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS ONE 3, e3638.
50. Thompson O., Moore C. J., Hussain S. A., Kleino I., Peckham M., Hohenester E., Ayscough K. R., Saksela K. and Winder S. J. (2009) Modulation of cell spreading and cell-substrate adhesion dynamics by dystroglycan. J. Cell Sci. 123, 118-127.
51. Thompson O., Moore C.J., Hussain S.A., Kleino I., Peckham M., Hohenester E., Ayscough K.R., Saksela K. and Winder S.J. (2010) Modulation of cell spreading and cell-substrate adhesion dynamics by dystroglycan. J. Cell Sci. 123, 118-127.