Perlecan is recruited by dystroglycan to nodes of ranvier and binds the clustering molecule gliomedin

Journal of Cell Biology

Volumn 208, Issue 3, 2015, Pages 313-329

  Colombelli, Cristina ^a   Palmisano, Marilena ^a,b   Eshed Eisenbach, Yael ^c   Zambroni, Desirée ^a   Pavoni, Ernesto ^a   Ferri, Cinzia ^a   Saccucci, Stefania ^a   Nicole, Sophie ^d,e,f,g   Soininen, Raija ^h   McKee, Karen K ⁱ   Yurchenco, Peter D ⁱ   Peles, Elior ^c   Wrabetz, Lawrence ^a,b   Feltri, M L ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY AT BUFFALO   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^e INSERM   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g CNRS   (France)

^h UNIVERSITY OF OULU   (Finland)

ⁱ RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROGLYCAN; GLIOMEDIN; PERLECAN; PROTEIN DERIVATIVE; SODIUM CHANNEL; UNCLASSIFIED DRUG; GLIOMEDIN PROTEIN, MOUSE; NERVE CELL ADHESION MOLECULE; PROTEIN BINDING; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; MICROVILLUS; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RANVIER NODE; RAT; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; COCULTURE; DBA MOUSE; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; PROTEIN DEGRADATION; PROTEIN TRANSPORT; TRANSGENIC MOUSE;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DYSTROGLYCANS; EXTRACELLULAR MATRIX; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MICROVILLI; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOLYSIS; RANVIER'S NODES; SODIUM CHANNELS;

EID: 84961291957     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201403111     Document Type: Article

References (89)

1. Apostolski, S., S.A. Sadiq, A. Hays, M. Corbo, L. Suturkova-Milosevic, P. Chaliff, K. Stefansson, R.G. LeBaron, E. Ruoslahti, A.P. Hays, et al. 1994. Identification of Gal(β1-3)GalNAc bearing glycoproteins at the nodes of Ranvier in peripheral nerve. J. Neurosci. Res. 38:134-141. http://dx.doi.org/10.1002/jnr.490380203
2. Arikawa-Hirasawa, E., H. Watanabe, H. Takami, J.R. Hassell, and Y. Yamada. 1999. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23:354-358. http://dx.doi.org/10.1038/15537
3. Bangratz, M., N. Sarrazin, J. Devaux, D. Zambroni, A. Echaniz-Laguna, F. René, D. Boërio, C.S. Davoine, B. Fontaine, M.L. Feltri, et al. 2012. A mouse model of Schwartz-Jampel syndrome reveals myelinating Schwann cell dysfunction with persistent axonal depolarization in vitro and distal peripheral nerve hyperexcitability when perlecan is lacking. Am. J. Pathol. 180:2040-2055. http://dx.doi.org/10.1016/j.ajpath.2012.01.035
4. Bekku, Y., L. Vargová, Y. Goto, I. Vorísek, L. Dmytrenko, M. Narasaki, A. Ohtsuka, R. Fässler, Y. Ninomiya, E. Syková, and T. Oohashi. 2010. Bral1: its role in diffusion barrier formation and conduction velocity in the CNS. J. Neurosci. 30:3113-3123. http://dx.doi.org/10.1523/JNEUROSCI.5598-09.2010
5. Bhat, M.A., J.C. Rios, Y. Lu, G.P. Garcia-Fresco, W. Ching, M. St Martin, J. Li, S. Einheber, M. Chesler, J. Rosenbluth, et al. 2001. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron. 30:369-383. http://dx.doi.org/10.1016/S0896-6273(01)00294-X
6. Bishop, J.R., M. Schuksz, and J.D. Esko. 2007. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 446:1030-1037. http://dx.doi.org/10.1038/nature05817
7. Bix, G., and R.V. Iozzo. 2008. Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc. Res. Tech. 71:339-348. http://dx.doi.org/10.1002/jemt.20562
8. Boiko, T., M.N. Rasband, S.R. Levinson, J.H. Caldwell, G. Mandel, J.S. Trimmer, and G. Matthews. 2001. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron. 30:91-104. http://dx.doi.org/10.1016/S0896-6273(01)00265-3
9. Brakebusch, C., C.I. Seidenbecher, F. Asztely, U. Rauch, H. Matthies, H. Meyer, M. Krug, T.M. Böckers, X. Zhou, M.R. Kreutz, et al. 2002. Brevican-deficient mice display impaired hippocampal CA1 longterm potentiation but show no obvious deficits in learning and memory. Mol. Cell. Biol. 22:7417-7427. http://dx.doi.org/10.1128/MCB.22.21.7417-7427.2002
10. Bretscher, A., K. Edwards, and R.G. Fehon. 2002. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3:586-599. http://dx.doi.org/10.1038/nrm882
11. Cai, H., R.A. Erdman, L. Zweier, J. Chen, J.H. Shaw IV, K.A. Baylor, M.M. Stecker, D.J. Carey, and Y.M. Chan. 2007. The sarcoglycan complex in Schwann cells and its role in myelin stability. Exp. Neurol. 205:257-269. http://dx.doi.org/10.1016/j.expneurol.2007.02.015
12. Chen, Y., T. Maguire, and R.M. Marks. 1996. Demonstration of binding of dengue virus envelope protein to target cells. J. Virol. 70:8765-8772.
13. Court, F.A., D.L. Sherman, T. Pratt, E.M. Garry, R.R. Ribchester, D.F. Cottrell, S.M. Fleetwood-Walker, and P.J. Brophy. 2004. Restricted growth of Schwann cells lacking Cajal bands slows conduction in myelinated nerves. Nature. 431:191-195. http://dx.doi.org/10.1038/nature02841
14. Court, F.A., J.E. Hewitt, K. Davies, B.L. Patton, A. Uncini, L. Wrabetz, and M.L. Feltri. 2009. A laminin-2, dystroglycan, utrophin axis is required for compartmentalization and elongation of myelin segments. J. Neurosci. 29:3908-3919. http://dx.doi.org/10.1523/JNEUROSCI.5672-08.2009
15. Court, F.A., D. Zambroni, E. Pavoni, C. Colombelli, C. Baragli, G. Figlia, L. Sorokin, W. Ching, J.L. Salzer, L. Wrabetz, and M.L. Feltri. 2011. MMP2-9 cleavage of dystroglycan alters the size and molecular composition of Schwann cell domains. J. Neurosci. 31:12208-12217. http://dx.doi.org/10.1523/JNEUROSCI.0141-11.2011
16. Custer, A.W., K. Kazarinova-Noyes, T. Sakurai, X. Xu, W. Simon, M. Grumet, and P. Shrager. 2003. The role of the ankyrin-binding protein NrCAM in node of Ranvier formation. J. Neurosci. 23:10032-10039.
17. Dours-Zimmermann, M.T., K. Maurer, U. Rauch, W. Stoffel, R. Fässler, and D.R. Zimmermann. 2009. Versican V2 assembles the extracellular matrix surrounding the nodes of ranvier in the CNS. J. Neurosci. 29:7731-7742. http://dx.doi.org/10.1523/JNEUROSCI.4158-08.2009
18. Dzhashiashvili, Y., Y. Zhang, J. Galinska, I. Lam, M. Grumet, and J.L. Salzer. 2007. Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J. Cell Biol. 177:857-870. http://dx.doi.org/10.1083/jcb.200612012
19. Elfvin, L.G. 1961. The ultrastructure of the nodes of Ranvier in cat sympathetic nerve fibers. J. Ultrastruct. Res. 5:374-387. http://dx.doi.org/10.1016/S0022-5320(61)80014-2
20. Eshed, Y., K. Feinberg, S. Poliak, H. Sabanay, O. Sarig-Nadir, I. Spiegel, J.R. Bermingham Jr., and E. Peles. 2005. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron. 47:215-229. http://dx.doi.org/10.1016/j.neuron.2005.06.026
21. Eshed, Y., K. Feinberg, D.J. Carey, and E. Peles. 2007. Secreted gliomedin is a perinodal matrix component of peripheral nerves. J. Cell Biol. 177:551-562. http://dx.doi.org/10.1083/jcb.200612139
22. Eshed-Eisenbach, Y., and E. Peles. 2013. The making of a node: a co-production of neurons and glia. Curr. Opin. Neurobiol. 23:1049-1056. http://dx.doi.org/10.1016/j.conb.2013.06.003
23. Farach-Carson, M.C., C.R. Warren, D.A. Harrington, and D.D. Carson. 2014. Border patrol: Insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol. 34:64-79.
24. + channels during the formation of nodes of Ranvier. Neuron. 65:490-502. http://dx.doi.org/10.1016/j.neuron.2010.02.004
25. Feltri, M.L., S.S. Scherer, L. Wrabetz, J. Kamholz, and M.E. Shy. 1992. Mitogenexpanded Schwann cells retain the capacity to myelinate regenerating axons after transplantation into rat sciatic nerve. Proc. Natl. Acad. Sci. USA. 89:8827-8831. http://dx.doi.org/10.1073/pnas.89.18.8827
26. 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.
27. 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. NY Acad. Sci. 883:116-123. http://dx.doi.org/10.1111/j.1749-6632.1999.tb08574.x
28. Gesemann, M., A. Brancaccio, B. Schumacher, and M.A. Ruegg. 1998. Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J. Biol. Chem. 273:600-605. http://dx.doi.org/10.1074/jbc.273.1.600
29. Gollan, L., D. Salomon, J.L. Salzer, and E. Peles. 2003. Caspr regulates the processing of contactin and inhibits its binding to neurofascin. J. Cell Biol. 163:1213-1218. http://dx.doi.org/10.1083/jcb.200309147
30. Goutebroze, L., M. Carnaud, N. Denisenko, M.C. Boutterin, and J.A. Girault. 2003. Syndecan-3 and syndecan-4 are enriched in Schwann cell perinodal processes. BMC Neurosci. 4:29. http://dx.doi.org/10.1186/1471-2202-4-29
31. Handler, M., P.D. Yurchenco, and R.V. Iozzo. 1997. Developmental expression of perlecan during murine embryogenesis. Dev. Dyn. 210:130-145. http://dx.doi.org/10.1002/(SICI)1097-0177(199710)210:2<130::AID-AJA6>3.0.CO;2-H
32. Haspel, J., D.R. Friedlander, N. Ivgy-May, S. Chickramane, C. Roonprapunt, S. Chen, M. Schachner, and M. Grumet. 2000. Critical and optimal Ig domains for promotion of neurite outgrowth by L1/Ng-CAM. J. Neurobiol. 42:287-302. http://dx.doi.org/10.1002/(SICI)1097-4695(20000215)42:3<287::AID-NEU1>3.0.CO;2-X
33. Hedstrom, K.L., X. Xu, Y. Ogawa, R. Frischknecht, C.I. Seidenbecher, P. Shrager, and M.N. Rasband. 2007. Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J. Cell Biol. 178:875-886. http://dx.doi.org/10.1083/jcb.200705119
34. Hess, A., and J.Z. Young. 1952. The nodes of Ranvier. Proc. R. Soc. Lond. B Biol. Sci. 140:301-320. http://dx.doi.org/10.1098/rspb.1952.0063
35. Hildebrand, C. 1971. Ultrastructural and light-microscopic studies of the developing feline spinal cord white matter. I. The nodes of Ranvier. Acta Physiol. Scand. Suppl. 82:81-107. http://dx.doi.org/10.1111/j.1365-201X.1971.tb10979.x
36. Hildebrand, C., and S.G. Waxman. 1984. Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J. Comp. Neurol. 224:25-37. http://dx.doi.org/10.1002/cne.902240103
37. Hnia, K., G. Hugon, A. Masmoudi, J. Mercier, F. Rivier, and D. Mornet. Effect of β-dystroglycan processing on utrophin/Dp116 anchorage in normal and mdx mouse Schwann cell membrane. Neuroscience. 141:607-620. http://dx.doi.org/10.1016/j.neuroscience.2006.04.043
38. Hodgkin, A.L., and A.F. Huxley. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544. http://dx.doi.org/10.1113/jphysiol.1952.sp004764
39. Ichimura, T., and M.H. Ellisman. 1991. Three-dimensional fine structure of cytoskeletal-membrane interactions at nodes of Ranvier. J. Neurocytol. 20:667-681. http://dx.doi.org/10.1007/BF01187068
40. Kanagawa, M., F. Saito, S. Kunz, T. Yoshida-Moriguchi, R. Barresi, Y.M. Kobayashi, J. Muschler, J.P. Dumanski, D.E. Michele, M.B. Oldstone, and K.P. Campbell. 2004. Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell. 117:953-964. http://dx.doi.org/10.1016/j.cell.2004.06.003
41. Kaplan, M.R., A. Meyer-Franke, S. Lambert, V. Bennett, I.D. Duncan, S.R. Levinson, and B.A. Barres. 1997. Induction of sodium channel clustering by oligodendrocytes. Nature. 386:724-728. http://dx.doi.org/10.1038/386724a0
42. Kaplan, M.R., M.H. Cho, E.M. Ullian, L.L. Isom, S.R. Levinson, and B.A. Barres. 2001. Differential control of clustering of the sodium channels Nav1.2 and Nav1.6 at developing CNS nodes of Ranvier. Neuron. 30:105-119. http://dx.doi.org/10.1016/S0896-6273(01)00266-5
43. Komada, M., and P. Soriano. 2002. βIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J. Cell Biol. 156:337-348. http://dx.doi.org/10.1083/jcb.200110003
44. Koticha, D., J. Babiarz, N. Kane-Goldsmith, J. Jacob, K. Raju, and M. Grumet. Cell adhesion and neurite outgrowth are promoted by neurofascin NF155 and inhibited by NF186. Mol. Cell. Neurosci. 30:137-148. http://dx.doi.org/10.1016/j.mcn.2005.06.007
45. Koticha, D., P. Maurel, G. Zanazzi, N. Kane-Goldsmith, S. Basak, J. Babiarz, J. Salzer, and M. Grumet. 2006. Neurofascin interactions play a critical role in clustering sodium channels, ankyrinG and βIV spectrin at peripheral nodes of Ranvier. Dev. Biol. 293:1-12. http://dx.doi.org/10.1016/j.ydbio.2005.05.028
46. Kunz, S., N. Sevilla, D.B. McGavern, K.P. Campbell, and M.B. Oldstone. Molecular analysis of the interaction of LCMV with its cellular receptor α-dystroglycan. J. Cell Biol. 155:301-310. http://dx.doi.org/10.1083/jcb.200104103
47. Kwok, J.C., G. Dick, D. Wang, and J.W. Fawcett. 2011. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 71:1073-1089. http://dx.doi.org/10.1002/dneu.20974
48. Labasque, M., J.J. Devaux, C. Lévêque, and C. Faivre-Sarrailh. 2011. Fibronectin type III-like domains of neurofascin-186 protein mediate gliomedin binding and its clustering at the developing nodes of Ranvier. J. Biol. Chem. 286:42426-42434. http://dx.doi.org/10.1074/jbc.M111.266353
49. Lacas-Gervais, S., J. Guo, N. Strenzke, E. Scarfone, M. Kolpe, M. Jahkel, P. De Camilli, T. Moser, M.N. Rasband, and M. Solimena. 2004. βIV∑1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J. Cell Biol. 166:983-990. http://dx.doi.org/10.1083/jcb.200408007
50. Lambert, S., J.Q. Davis, and V. Bennett. 1997. Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J. Neurosci. 17:7025-7036.
51. Landon, D.N., and O.K. Langley. 1971. The local chemical environment of nodes of Ranvier: a study of cation binding. J. Anat. 108:419-432.
52. Lustig, M., L. Erskine, C.A. Mason, M. Grumet, and T. Sakurai. 2001. Nr-CAM expression in the developing mouse nervous system: ventral midline structures, specific fiber tracts, and neuropilar regions. J. Comp. Neurol. 434:13-28. http://dx.doi.org/10.1002/cne.1161
53. Maertens, B., D. Hopkins, C.W. Franzke, D.R. Keene, L. Bruckner-Tuderman, D.S. Greenspan, and M. Koch. 2007. Cleavage and oligomerization of gliomedin, a transmembrane collagen required for node of Ranvier formation. J. Biol. Chem. 282:10647-10659. http://dx.doi.org/10.1074/jbc.M611339200
54. Martin, P.T. 2003. Dystroglycan glycosylation and its role in matrix binding in skeletal muscle. Glycobiology. 13:55R-66R. http://dx.doi.org/10.1093/glycob/cwg076
55. Martin, S., A.K. Levine, Z.J. Chen, Y. Ughrin, and J.M. Levine. 2001. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J. Neurosci. 21:8119-8128.
56. Melendez-Vasquez, C., D.J. Carey, G. Zanazzi, O. Reizes, P. Maurel, and J.L. Salzer. 2005. Differential expression of proteoglycans at central and peripheral nodes of Ranvier. Glia. 52:301-308. http://dx.doi.org/10.1002/glia.20245
57. Moore, S.A., F. Saito, J. Chen, D.E. Michele, M.D. Henry, A. Messing, R.D. Cohn, S.E. Ross-Barta, S. Westra, R.A. Williamson, et al. 2002. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature. 418:422-425. http://dx.doi.org/10.1038/nature00838
58. Nico, B., R. Tamma, T. Annese, D. Mangieri, A. De Luca, P. Corsi, V. Benagiano, V. Longo, E. Crivellato, A. Salmaggi, and D. Ribatti. 2010. Glial dystrophin-associated proteins, laminin and agrin, are downregulated in the brain of mdx mouse. Lab. Invest. 90:1645-1660. http://dx.doi.org/10.1038/labinvest.2010.149
59. Occhi, S., D. Zambroni, U. Del Carro, S. Amadio, E.E. Sirkowski, S.S. Scherer, K.P. Campbell, S.A. Moore, Z.L. Chen, S. Strickland, 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. http://dx.doi.org/10.1523/JNEUROSCI.2068-05.2005
60. Pan, Z., T. Kao, Z. Horvath, J. Lemos, J.Y. Sul, S.D. Cranstoun, V. Bennett, S.S. Scherer, and E.C. Cooper. 2006. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26:2599-2613. http://dx.doi.org/10.1523/JNEUROSCI.4314-05.2006
61. Pedraza, L., J.K. Huang, and D.R. Colman. 2001. Organizing principles of the axoglial apparatus. Neuron. 30:335-344. http://dx.doi.org/10.1016/S0896-6273(01)00306-3
62. Peters, A. 1966. The node of Ranvier in the central nervous system. Q. J. Exp. Physiol. Cogn. Med. Sci. 51:229-236.
63. Raine, C.S. 1984. On the association between perinodal astrocytic processes and the node of Ranvier in the C.N.S. J. Neurocytol. 13:21-27. http://dx.doi.org/10.1007/BF01148316
64. Ranvier, L. 1871. Sur les éléments conjonctifs de la moelle épinière. Comptes Rendus de l'Académie des Sciences. 73:1168-1171.
65. Rieger, F., J.K. Daniloff, M. Pincon-Raymond, K.L. Crossin, M. Grumet, and G.M. Edelman. 1986. Neuronal cell adhesion molecules and cytotactin are colocalized at the node of Ranvier. J. Cell Biol. 103:379-391. http://dx.doi.org/10.1083/jcb.103.2.379
66. Rossi, M., H. Morita, R. Sormunen, S. Airenne, M. Kreivi, L. Wang, N. Fukai, B.R. Olsen, K. Tryggvason, and R. Soininen. 2003. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22:236-245. http://dx.doi.org/10.1093/emboj/cdg019
67. 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. http://dx.doi.org/10.1016/S0896-6273(03)00301-5
68. Saito, F., Y. Saito-Arai, A. Nakamura, T. Shimizu, and K. Matsumura. 2008. Processing and secretion of the N-terminal domain of α-dystroglycan in cell culture media. FEBS Lett. 582:439-444. http://dx.doi.org/10.1016/j.febslet.2008.01.006
69. Schafer, D.P., A.W. Custer, P. Shrager, and M.N. Rasband. 2006. Early events in node of Ranvier formation during myelination and remyelination in the PNS. Neuron Glia Biol. 2:69-79. http://dx.doi.org/10.1017/S1740925X06000093
70. Sherman, D.L., S. Tait, S. Melrose, R. Johnson, B. Zonta, F.A. Court, W.B. Macklin, S. Meek, A.J. Smith, D.F. Cottrell, and P.J. Brophy. 2005. Neurofascins are required to establish axonal domains for saltatory conduction. Neuron. 48:737-742. http://dx.doi.org/10.1016/j.neuron.2005.10.019
71. Singh, J., Y. Itahana, S. Knight-Krajewski, M. Kanagawa, K.P. Campbell, M.J. Bissell, and J. Muschler. 2004. Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 64:6152-6159. http://dx.doi.org/10.1158/0008-5472.CAN-04-1638
72. Skarnes, W.C., J.E. Moss, S.M. Hurtley, and R.S. Beddington. 1995. Capturing genes encoding membrane and secreted proteins important for mouse development. Proc. Natl. Acad. Sci. USA. 92:6592-6596. http://dx.doi.org/10.1073/pnas.92.14.6592
73. Spence, H.J., Y.J. Chen, C.L. Batchelor, J.R. Higginson, H. Suila, O. Carpen, and S.J. Winder. 2004. Ezrin-dependent regulation of the actin cytoskeleton by β-dystroglycan. Hum. Mol. Genet. 13:1657-1668. http://dx.doi.org/10.1093/hmg/ddh170
74. Stum, M., E. Girard, M. Bangratz, V. Bernard, M. Herbin, A. Vignaud, A. Ferry, C.S. Davoine, A. Echaniz-Laguna, F. René, et al. 2008. Evidence of a dosage effect and a physiological endplate acetylcholinesterase deficiency in the first mouse models mimicking Schwartz-Jampel syndrome neuromyotonia. Hum. Mol. Genet. 17:3166-3179. http://dx.doi.org/10.1093/hmg/ddn213
75. Susuki, K., K.J. Chang, D.R. Zollinger, Y. Liu, Y. Ogawa, Y. Eshed-Eisenbach, M.T. Dours-Zimmermann, J.A. Oses-Prieto, A.L. Burlingame, C.I. Seidenbecher, et al. 2013. Three mechanisms assemble central nervous system nodes of Ranvier. Neuron. 78:469-482. http://dx.doi.org/10.1016/j.neuron.2013.03.005
76. Talts, J.F., Z. Andac, W. Göhring, A. Brancaccio, and R. Timpl. 1999. Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J. 18:863-870. http://dx.doi.org/10.1093/emboj/18.4.863
77. Tao-Cheng, J.H., and J. Rosenbluth. 1983. Axolemmal differentiation in myelinated fibers of rat peripheral nerves. Brain Res. 9:251-263. http://dx.doi.org/10.1016/0165-3806(83)90023-8
78. Thaxton, C., A.M. Pillai, A.L. Pribisko, J.L. Dupree, and M.A. Bhat. 2011. Nodes of Ranvier act as barriers to restrict invasion of flanking paranodal domains in myelinated axons. Neuron. 69:244-257. http://dx.doi.org/10.1016/j.neuron.2010.12.016
79. Voas, M.G., D.A. Lyons, S.G. Naylor, N. Arana, M.N. Rasband, and W.S. Talbot. αII-spectrin is essential for assembly of the nodes of Ranvier in myelinated axons. Curr. Biol. 17:562-568. http://dx.doi.org/10.1016/j.cub.2007.01.071
80. Walko, G., K.L. Wögenstein, L. Winter, I. Fischer, M.L. Feltri, and G. Wiche. Stabilization of the dystroglycan complex in Cajal bands of myelinating Schwann cells through plectin-mediated anchorage to vimentin filaments. Glia. 61:1274-1287. http://dx.doi.org/10.1002/glia.22514
81. Waxman, S.G., and J.A. Black. 1984. Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res. 308:77-87. http://dx.doi.org/10.1016/0006-8993(84)90919-3
82. Weber, P., U. Bartsch, M.N. Rasband, R. Czaniera, Y. Lang, H. Bluethmann, R.U. Margolis, S.R. Levinson, P. Shrager, D. Montag, and M. Schachner. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19:4245-4262.
83. Whitelock, J.M., J. Melrose, and R.V. Iozzo. 2008. Diverse cell signaling events modulated by perlecan. Biochemistry. 47:11174-11183. http://dx.doi.org/10.1021/bi8013938
84. Winkler, S., R.C. Stahl, D.J. Carey, and R. Bansal. 2002. Syndecan-3 and perlecan are differentially expressed by progenitors and mature oligodendrocytes and accumulate in the extracellular matrix. J. Neurosci. Res. 69:477-487. http://dx.doi.org/10.1002/jnr.10311
85. Yamada, H., F. Saito, H. Fukuta-Ohi, D. Zhong, A. Hase, K. Arai, A. Okuyama, R. Maekawa, T. Shimizu, and K. Matsumura. 2001. Processing of β-dystroglycan by matrix metalloproteinase disrupts the link between the extracellular matrix and cell membrane via the dystroglycan complex. Hum. Mol. Genet. 10:1563-1569. http://dx.doi.org/10.1093/hmg/10.15.1563
86. Yang, Y., S. Lacas-Gervais, D.K. Morest, M. Solimena, and M.N. Rasband. βIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J. Neurosci. 24:7230-7240. http://dx.doi.org/10.1523/JNEUROSCI.2125-04.2004
87. Zhang, Y., Y. Bekku, Y. Dzhashiashvili, S. Armenti, X. Meng, Y. Sasaki, J. Milbrandt, and J.L. Salzer. 2012. Assembly and maintenance of nodes of Ranvier rely on distinct sources of proteins and targeting mechanisms. Neuron. 73:92-107. http://dx.doi.org/10.1016/j.neuron.2011.10.016
88. Zhong, D., F. Saito, Y. Saito, A. Nakamura, T. Shimizu, and K. Matsumura. Characterization of the protease activity that cleaves the extracellular domain of β-dystroglycan. Biochem. Biophys. Res. Commun. 345:867-871. http://dx.doi.org/10.1016/j.bbrc.2006.05.004
89. Zonta, B., S. Tait, S. Melrose, H. Anderson, S. Harroch, J. Higginson, D.L. Sherman, and P.J. Brophy. 2008. Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J. Cell Biol. 181:1169-1177. http://dx.doi.org/10.1083/jcb.200712154