Dystonin is an essential component of the Schwann cell cytoskeleton at the time of myelination

Development

Volumn 125, Issue 11, 1998, Pages 2135-2148

  Bernier, Gilbert ^a,e   De Repentigny, Yves ^a   Mathieu, Martine ^a   David, Samuel ^b   Kothary, Rashmi ^a,c,d  

^a Institut du Cancer de Montreal   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Cytoskeleton; Dystonia musculorum; Dystonin Bpag 1; Mouse; Myelination; Schwann cell

Indexed keywords

CYTOSKELETON PROTEIN; MUTANT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL CULTURE; CONTROLLED STUDY; CYTOSKELETON; HETEROZYGOTE; MOUSE; MYELINATION; NERVE GRAFT; NEWBORN; NONHUMAN; PERIPHERAL NERVE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SCHWANN CELL;

ANIMALS; ANIMALS, NEWBORN; CARRIER PROTEINS; CYTOSKELETAL PROTEINS; CYTOSKELETON; DEMYELINATING DISEASES; DYSTONIA; HETEROZYGOTE; HOMOZYGOTE; MICE; MICE, MUTANT STRAINS; MYELIN P0 PROTEIN; MYELIN SHEATH; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; PERIPHERAL NERVES; RNA, MESSENGER; SCHWANN CELLS; SPINAL NERVE ROOTS;

EID: 0031835293     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Adlkofer, K., Martini, R., Aguzzi, A., Zielasek, J., Toyka, K. V. and Suter, U. (1995). Hypermyelination and demyelinating peripheral neuropathy in Pmp22-deficient mice. Nature Genet. 11, 274-280.
2. Al-Ali, S. Y. and Al-Zuhar, A. G. H. (1989). Fine structural study of the spinal cord and spinal ganglia in mice afflicted with a hereditary sensory neuropathy, dystonia musculorum. J. Submicroscopic Cytol. Pathol. 21, 737- 748.
3. Andrä, K., Lassmann, H., Bittner, R., Shorny, S., Fässler, R., Propst, F. and Wiche, G. (1997). Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle and heart cytoarchitecture. Genes Dev. 11, 3143-3156.
4. Ausubel, F. M. (1994). Current Protocols in Molecular Biology. New York: Wiley.
5. Bedell, M. A., Largaespada, D. A., Jenkins, N. A. and Copeland, N. G. (1997). Mouse models of human disease. 2. Recent progress and future directions. Genes Dev. 11, 11-43.
6. Bernier, G., Brown, A., Dalpé, G., De Repentigny, Y., Mathieu, M. and Kothary, R. (1995a). Dystonin expression in the developing nervous system predominates in the neurons that degenerate in dystonia musculorum mutant mice. Molec. Cell. Neurosci. 6, 509-520.
7. 24J. Biochem. Cell Biol. 73, 605- 609.
8. Bernier, G., Mathieu, M., De Repentigny, Y., Vidal, S. M. and Kothary, R. (1996). Cloning and characterization of mouse Acf7. a novel member of the dystonin subfamily of actin binding proteins. Genomics 38, 19-29.
9. Bernier, G. and Kothary, R. (1998). Prenatal onset of axonopathy in dystonia musculorum mice. Dev. Genet, (in press).
10. Brown, A., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Rossant, J. and Kothary, R. (1994). The genomic structure of an insertional mutation in the dystonia musculorum locus. Genomics 20, 371-376.
11. Brown, A., Bernier, G., Mathieu, M., Rossant, J. and Kothary, R. (1995). The mouse dystonia musculorum gene is a neural isoform of bullous pemphigoid antigen 1. Nature Genet. 10, 301-306.
12. Bunge, M. B., Williams, A. K. and Wood, P. M. (1982). Neuron-Schwann cell interaction in basal lamina formation. Dev. Biol. 92, 449-460.
13. Bunge, R. P., Bunge, M. B. and 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.
14. Burridge, K., Nuckolls, G., Otey, C., Pavalko, F., Simon, K. and Turner, C. (1990). Actin-membrane interaction in focal adhesions. Cell Diff. Devel. 32, 337-342.
15. Campbell, R. M. and Peterson, A. C. (1992). An intrinsic neuronal defect operates in dystonia musculorum: a study of dt/dt<>+/+ chimeras. Neuron 9, 693-703.
16. Chavanas, S., Pulkkinen, L., Cache, Y., Smith, F. J. D., McLean, W. H. I., Uitto, J., Ortonne, J. P. and Meneguzzi, G. (1996). A homozygous nonsense mutation in the Plec1 gene in patients with epidermolysis bullosa simplex with muscular dystrophy. J. Clin. Invest. 98, 2196-2200.
17. Cheng, L. and Mudge, A. W. (1996). Cultured Schwann cells constitutively express the myelin protein P0. Neuron 16, 309-319.
18. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
19. Dalpé, G., Leclerc, N., Vallée, A., Messer, A., Mathieu, M., De Repentigny, Y. and Kothary, R. (1998). Dystonin is essential for maintaining neuronal cytoskeleton organization. Mol. Cell. Neurosci. 10, 243-257.
20. de Waegh, S. M., Lee, V. M. -Y. and Brady, S. T. (1992). Local modulation of neurofilament phosphorylation, axonal caliber and slow axonal transport by myelinating Schwann cells. Cell 68, 451-463.
21. Dowling, J., Yu, Q. C. and Fuchs, E. (1996). Beta-4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol. 134, 559-572.
22. Duchen, L. W. (1976). Dystonia musculorum - an inherited disease of the nervous system in the mouse. Adv. Neural. 14, 353-365.
23. Duchen, L. W., Falconer, D. S. and Strich, S. J. (1963). Dystonia Musculorum. A hereditary neuropathy of mice affecting mainly sensory pathways. J. Physiol. 165, 7-9.
24. Duchen, L. W. and Strich, S. J. (1964). Clinical and pathological studies of an hereditary neuropathy in mice. Brain 87, 367-378.
25. Einheber, S., Milner, T. A., Giancotti, F. and Salzer, J. L. (1993). Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J. Cell Biol. 123, 1223-1236.
26. Elliott, C. E., Becker, B., Oehler, S., Castanon, M. J., Hauptmann, R. and Wiche, G. (1997). Plectin transcript diversity: Identification and tissue distribution of variants with distinct first coding exons and rodless isoforms. Genomics 42, 115-125.
27. Fässler, R., Georges-Labouesse, E. and Hirsch, E. (1996). Genetic analyses of integrin function in mice. Curr. Opin. Cell Biol. 8, 641-646.
28. Feltri, M. L., Scherer, S. S., Nemni, R., Kamholz, J., Vogelbacker, H., Scott, M. O., Canal, N., Quaranta, V. and Wrabetz, L. (1994). Beta 4 integrin expression in myelinating Schwann cells is polarized, developmentally regulated and axonally dependent. Development 120, 1287-1301.
29. 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.
30. Giese, K. P., Martini, R., Lemke, G., Soriano, P. and Schachner, M. (1992). Mouse Po gene disruption leads to hypomyelination, abnormal expression of recognition molecules and degeneration of myelin and axons. Cell 71, 565-576.
31. Gillespie, C. S., Sherman, D. L., Blair, G. E. and Brophy, P. J. (1994). Periaxin, a novel protein of myelinating Schwann cells with a possible role in axonal ensheathment. Neuron 12, 497-508.
32. Green, K. J., Virata, M. L. A., Elgart, G. W., Stanley, J. R. and Parry, D. A. D. (1992a). Comparative structural analysis of desmoplakin, bullous pemphigoid antigen and plectin: members of a new gene family involved in organization of intermediate filaments. Int. J. Biol. Macromol. 14, 145-153.
33. Green, K. J., Stappenbeck, T. S., Parry, D. A. and Virata, M. L. (1992b). Structure of desmoplakin and its association with intermediate filaments. J. Dermatol 19, 765-769.
34. Green, K. J. and Jones, J. C. R. (1996). Desmosomes and hemidesmosomes - structure and function of molecular components. FASEB J. 10, 871-881.
35. Guo, L. F., Degenstein, L., Dowling, J., Yu, Q. C., Wollmann, R., Perman, B. and Fuchs, E. (1995). Gene targeting of bpag1 - abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell 81, 233-243.
36. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Press.
37. Hieda, Y., Nishizawa, Y., Uematsu, J. and Owaribe, K. (1992). Identification of a new hemidesmosomal protein, HD1: a major, high molecular mass component of isolated hemidesmosomes. J. Cell Biol. 116, 1497-1506.
38. Hogan, B., Costantini, F. and Lacy, E. (1986). Manipulating the Mouse Embryo, A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
39. Hynes, R. O. (1992). Integrins: Versatility, modulation and signaling in cell adhesion. Cell 69, 11-25.
40. Janota, I. (1972). Ultrastructural studies of an hereditary sensory neuropathy in mice (dystonia musculorum). Brain 95, 529-536.
41. Jones, J. C. R., Asmuth, J., Baker, S. E., Langhofer, M., Roth, S. I. and Hopkinson, S. B. (1994). Hemidesmosomes: extracellular matrix/intermediate filament connectors. Exp. Cell Res. 213, 1-11.
42. Kelly, B. M., Gillespie, C. S., Sherman, D. L. and Brophy, P. J. (1992). Schwann cells of the myelin-forming phenotype express neurofilament protein NF-M. J. Cell Biol. 118, 397-410.
43. Klatte, D. H., Kurpakus, M. A., Grelling, K. A. and Jones, J. C. R. (1989). Immunochemical characterization of three components of the hemidesmosome and their expression in cultured epithelial cells. J. Cell Biol. 109, 3377-3390.
44. Kothary, R., Clapoff, S., Brown, A., Campbell, R., Peterson, A. and Rossant, J. (1988). A transgene containing lacZ inserted into the dystonia locus is expressed in neural tube. Nature 335, 435-437.
45. Kothary, R., Clapoff, S., Darling, S., Perry, M. D., Moran, L. A. and Rossant, J. (1989). Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105, 707-714.
46. Laemmli, U. K. (1972). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
47. Madrid, R. E., Jaros, E. Cullen, M. J. and Bradley, W. G. (1975). Genetically determined defect of Schwann cell basement membrane in dystrophic mouse. Nature 257, 319-321.
48. Martini, R., Zielasek, J., Toyka, K. V., Giese, K. P. and Schachner, M. (1995). Protein zero (Po)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nature Genet. 11, 281-286.
49. McLean, W. H. I., Pulkkinen, L., Smith, F. J. D., Rugg, E. L., Lane, E. B., Bullrich, F., Burgeson, R. E., Amano, S., Hudson, D. L., Owaribe, K., McGrath, J. A., McMillan, J. R., Eady, R. A. J., Leigh, I. M., Christiano, A. M. and Ditto, J. (1996). Loss of plectin causes epidermolysis bullosa with muscular dystrophy - cDNA cloning and genomic organization. Genes Dev. 10, 1724-1735.
50. Moss, T. H. (1981a). Segmental demyelination in the peripheral nerves of mice affected by a hereditary neuropathy (dystonia musculorum). Acta Neuropathologica 53, 51-56.
51. Moss, T. H. (1981b). Schwann cell involvement in the neurological lesion of the dystonic mutant mouse. J. Neurol. Sci. 49, 207-222.
52. Mutasim, D. F., Takahashi, Y., Labib, R. S., Anhalt, G. J., Patel, H. P. and Diaz, L. A. (1985). A pool of bullous pemphigoid is intracellular and associated with the basal cell cytoskeleton-hemidesmosome complex. J. Invest. Dermatol. 84, 47-53.
53. Niessen, C. M., Hulsman, E. H. M., Rots, E. S., Sanchezaparicio, P. and Sonnenberg, A. (1997). Integrin alpha-6-beta-4 forms a complex with the cytoskeletal protein HD1 and induces its redistribution in transfected Cos-7 cells. Mol. Biol. Cell 8, 555-566.
54. Nikolic, B., Macnulty, E., Mir, B. and Wiche, G. (1996). Basic amino acid residue cluster within nuclear targeting sequence motif is essential for cytoplasmic plectin-vimentin network junctions. J. Cell Biol. 134. 1455- 1467 .
55. Obremski, V. J., Wood, P. M. and Bunge, M. B. (1993). Fibroblasts promote Schwann cell basal lamina deposition and elongation in the absence of neurons in culture. Dev. Biol. 160, 119-134.
56. Pulkkinen, L., Smith, F. J. D., Shimizu, H., Murata, S., Yaoita, H., Hachisuka, H., Nishikawa, T., McLean, W. H. I. and Uitto, J. (1996). Homozygous deletion mutations in the plectin gene (Plec1) in patients with epidermolysis bullosa simplex associated with late-onset muscular dystrophy. Hum. Mol. Genet. 5, 1539-1546.
57. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989), Molecular Cloning: A Laboratory Manual, second Edition. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
58. Sereda, M., Griffiths, I., Puhlhofer, A., Stewart, H., Rossner, M. J., Zimmerman, F., Magyar, J. P., Schneider, A., Hund, E., Meinck, H. M., Suter, U. and Nave, K. A. (1996). A transgenic rat model of Charcot-Marie- Tooth disease. Neuron 16, 1049-1060.
59. Smith, F. J. D., Eady, R. A. J., McMillan, J. R., Leigh, I. M., Geddes, J. F., Rugg, E. L., Kelsell, D. P., Bryant, S. P., Spurr, N. K., Kirtschig, G., Milana, G., de Bono, A. G., Owaribe, K., Wiche, G., Pulkkinen, L., Uitto, J., McLean, W. H. I. and Lane, E. B. (1996). Plectin deficiency: Hereditary basis for muscular dystrophy with epidermolysis bullosa. Nature Genet. 13, 450-457.
60. Sotelo, C. and Guenet, J. L. (1988). Pathologic changes in the CNS of dystonia musculorum mutant mouse: an animal model for human spinocerebellar ataxia. Neurosci. 27, 403-424.
61. Spector, D. L., Goldman, R. D. and Leinwand, L. A. (1998). Cells. A Laboratory Mannual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
62. Stappenbeck, T. S. and Green, K. J. (1992). The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells. J. Cell Biol. 116, 1197-1209.
63. Stappenbeck, T. S., Bornslaeger, E. A., Corcoran, C. M., Luu, H. H., Virata, M. L. and Green, K. J. (1993). Functional analysis of desmoplakin domains: specification of the interaction with keratin versus vimentin intermediate filament networks. J. Cell Biol. 123, 691-705.
64. Stepp, M. A., Spurr Michaud, S., Tisdale, A., Elwell, J. and Gipson, I. K. (1990). α6β4 integrin heterodimer is a component of hemidesmosomes. Proc. Nat. Acad. Sci. USA 87, 8970-8974.
65. Sunada, Y., Bernier, S. M., Kozak, C. A., Yamada, Y. and Campbell, K. P. (1994). Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. J. Biol. Chem. 269, 13729-13732.
66. Suter, U., Welcher, A. A., Ozcelik, T., Snipes, G. J., Kosaras, B., Francke, U., Billings-Gagliardi, S., Sidman, R. L. and Shooter, E. M. (1992a). Trembler mouse carries a point mutation in a myelin gene. Nature 356, 241- 244.
67. Suter, U., Moskow, J. J., Welcher, A. A., Snipes, G. J., Kosaras, B., Sidman, R. L., Buchberg, A. M. and Shooter, E. M. (1992b). A leucine-to-proline mutation in the putative first transmembrane domain of the 22-kDa peripheral myelin protein in the trembler-J mouse. Proc. Nat. Acad. Sci. USA 89, 4382-4386.
68. Trapp, B. D., Andrews, S. B., Wong, A., O'Connell, M. and Griffin, J. W. (1989). Co-localization of the myelin-associated glycoprotein and the microfilament components F-actin and spectrin in Schwann cells of myelinated fibers. J. Neurocytol. 18, 47-60.
69. Trapp, B. D., Kidd, G. J., Hauer, P., Mulrenin, E., Haney, C. A. and Andrews, S. B. (1995). Polarization of myelinating Schwann cell surface membranes: role of microtubules and the trans-Golgi network. J. Neurosci. 15, 1797-1807.
70. Tryggvason, K. (1993). The laminin family. Curr. Opin. Cell Biol. 5, 877-882.
71. van der Neut, R., Krimpenfort, P., Calafat, J., Niessen, C. M. and Sonnenberg, A. (1996). Epithelial detachment due to absence of hemidesmosomes in integrin beta 4 null mice. Nature Genet. 13, 366- 369.
72. Warner, L. E., Hilz, M. J., Appel, S. H., Killian, J. M., Kolodry, E. H., Karpati, G., Carpenter, S., Watters, G. V., Wheeler, C., Witt, D., Bodell, A., Nelis, E., Van Broeckhoven, C. and Lupski, J. R. (1996). Clinical phenotypes of different MPZ (P0) mutations may include Charcot-Marie- Tooth type IB. Dejerine-Sottas and congenital hypomyelination. Neuron 17, 451-460.
73. Wiche, G., Gromov, D., Donovan, A., Castanon, M. J. and Fuchs, E. (1993). Expression of plectin mutant cDNA in cultured cells indicates a role of COOH-terminal domain in intermediate filament association. J. Cell Biol. 121, 607-619.
74. Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225, 361-372.
75. Xu, H., Wu, X. R., Wewer, U. M. and Engvall, E. (1994). Murine muscular dystrophy caused by a mutation in the laminin alpha 2 (Lama2) gene. Nature Genet. 8, 297-302.
76. Yang, Y. M., Dowling, J., Yu, Q. C., Kouklis, P., Cleveland, D. W. and Fuchs, E. (1996). An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 86, 655-665.