Compensation for dystrophin-deficiency: ADAM12 overexpression in skeletal muscle results in increased α7 integrin, utrophin and associated glycoproteins

Human Molecular Genetics

Volumn 12, Issue 19, 2003, Pages 2467-2479

  Moghadaszadeh, Behzad ^a   Albrechtsen, Reidar ^a   Guo, Ling T ^b   Zaik, Michaela ^c   Kawaguchi, Nobuko ^a   Borup, Rehannah H ^d   Kronqvist, Pauliina ^a   Schröder, Henrik D ^e   Davies, Kay E ^f   Voit, Thomas ^c   Nielsen, Finn C ^d   Engvall, Eva ^b   Wewer, Ulla M ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d Rigshospitalet   (Denmark)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; CREATINE KINASE; DISINTEGRIN; DYSTROPHIN; GLYCOPROTEIN; INTEGRIN; METALLOPROTEINASE; PROTEIN ADAM12; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOUSE; MUSCLE INJURY; MUSCLE NECROSIS; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SKELETAL MUSCLE;

ADAM PROTEINS; ANIMALS; BIOLOGICAL MARKERS; CYTOSKELETAL PROTEINS; DYSTROPHIN; GENE EXPRESSION PROFILING; GLYCOPROTEINS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTEGRIN ALPHA CHAINS; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRECIPITIN TESTS; TISSUE DISTRIBUTION; TRANSGENES; UP-REGULATION; UTROPHIN;

ANIMALIA; MUS MUSCULUS;

EID: 10744227218     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg264     Document Type: Article

References (62)

1. O'Brien, K.F. and Kunkel, L.M. (2001) Dystrophin and muscular dystrophy: past, present, and future. Mol. Genet. Metab., 74, 75-88.
2. Blake, D.J., Weir, A., Newey, S.E. and Davies, K.E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev., 82, 291-329.
3. Tome, F.M., Evangelista, T., Leclerc, A., Sunada, Y., Manole, E., Estournet, B., Barois, A., Campbell, K.P. and Fardeau, M. (1994) Congenital muscular dystrophy with merosin deficiency. C. R. Acad. Sci. III, 317, 351-357.
4. 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. Nat. Genet., 8, 297-302.
5. Duggan, D.J. and Hoffman, E.P. (1996) Autosomal recessive muscular dystrophy and mutations of the sarcoglycan complex. Neuromusc. Disord., 6, 475-482.
6. Cohn, R.D. and Campbell, K.P. (2000) Molecular basis of muscular dystrophies. Muscle Nerve, 23, 1456-1471.
7. Engvall, E. and Wewer, U.M. (2003) The new frontier in muscular dystrophy: booster genes. FASEB J., in press.
8. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl Acad. Sci. USA, 90, 3710-3714.
9. Di Blasi, C., Morandi, L., Barresi, R., Blasevich, F., Cornelio, F. and Mora, M. (1996) Dystrophin-associated protein abnormalities in dystrophin-deficient muscle fibers from symptomatic and asymptomatic Duchenne/Becker muscular dystrophy carriers. Acta Neuropathol. (Berl.), 92, 369-377.
10. Cox, G.A., Cole, N.M., Matsumura, K., Phelps, S.F., Hauschka, S.D., Campbell, K.P., Faulkner, J.A. and Chamberlain, J.S. (1993) Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature, 364, 725-729.
11. Scott, J.M., Li, S., Harper, S.Q., Welikson, R., Bourque, D., DelloRusso, C., Hauschka, S.D. and Chamberlain, J.S. (2002) Viral vectors for gene transfer of micro-, mini-, or full-length dystrophin. Neuromusc. Disord., 12, S23-29.
12. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Trickett, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
13. Deconinck, N., Tinsley, J., De Backer, F., Fisher, R., Kahn, D., Phelps, S., Davies, K. and Gillis, J.M. (1997) Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat. Med., 3, 1216-1221.
14. Squire, S., Raymackers, J.M., Vandebrouck, C., Potter, A., Tinsley, J., Fisher, R., Gillis, J.M. and Davies, K.E. (2002) Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum. Mol. Genet., 11, 3333-3344.
15. Burkin, D.J., Wallace, G.Q., Nicol, K.J., Kaufman, D.J. and Kaufman, S.J. (2001) Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J. Cell Biol., 152, 1207-1218.
16. Nguyen, H.H., Jayasinha, V., Xia, B., Hoyte, K. and Martin, P.T. (2002) Overexpression of the cytotoxic T cell GalNAc transferase in skeletal muscle inhibits muscular dystrophy in mdx mice. Proc. Natl Acad. Sci. USA, 99, 5616-5621.
17. Kronqvist, P., Kawaguchi, N., Albrechtsen, R., Xu, X., Schroder, H.D., Moghadaszadeh, B., Nielsen, F.C., Frohlich, C., Engvall, E. and Wewer, U.M. (2002) ADAM12 alleviates the skeletal muscle pathology in mdx dystrophic mice. Am. J. Pathol., 161, 1535-1540.
18. White, J.M., Bigler, D., Chen, M. and Wolfsberg, T.G. (2001) Frontiers in molecular biology. In Beckerle, M. (ed.), Cell Adhesion. Oxford University Press, Oxford.
19. Blobel, C.P. (2002) Functional and biochemical characterization of ADAMs and their predicted role in protein ectodomain shedding. Inflamm. Res., 51, 83-84.
20. Seals, D.F. and Courtneidge, S.A. (2003) The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev., 17, 7-30.
21. Blobel, C.P. and White, J.M. (1992) Structure, function and evolutionary relationship of proteins containing a disintegrin domain. Curr. Opin. Cell Biol., 4, 760-765.
22. Wolfsberg, T.G. and White, J.M. (1996) ADAMs in fertilization and development. Dev. Biol., 180, 389-401.
23. Gould, R.J., Polokoff, M.A., Friedman, P.A., Huang, T.F., Holt, J.C., Cook, J.J. and Niewiarowski, S. (1990) Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proc. Soc. Exp. Biol. Med., 195, 168-171.
24. Iba, K., Albrechtsen, R., Gilpin, B.J., Loechel, F. and Wewer, U.M. (1999) Cysteine-rich domain of human ADAM 12 (meltrin alpha) supports tumor cell adhesion. Am. J. Pathol., 154, 1489-1501.
25. Eto, K., Puzon-McLaughlin, W., Sheppard, D., Sehara-Fujisawa, A., Zhang, X.P. and Takada, Y. (2000) RGD-independent binding of integrin alpha9beta1 to the ADAM-12 and -15 disintegrin domains mediates cell-cell interaction. J. Biol. Chem., 275, 34922-34930.
26. Iba, K., Albrechtsen, R., Gilpin, B., Frohlich, C., Loechel, F., Zolkiewska, A., Ishiguro, K., Kojima, T., Liu, W., Langford, J.K. et al. (2000) The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to beta1 integrin-dependent cell spreading. J. Cell Biol., 149, 1143-1156.
27. Thodeti, C.K., Albrechtsen, R., Grauslund, M., Asmar, M., Larsson, C., Takada, Y., Mercurio, A.M., Couchman, J.R. and Wewer, U.M. (2003) ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and RhoA. J. Biol. Chem., 278, 9576-9584.
28. Yagami-Hiromasa, T., Sato, T., Kurisaki, T., Kamijo, K., Nabeshima, Y. and Fujisawa-Sehara, A. (1995) A metalloprotease-disintegrin participating in myoblast fusion. Nature, 377, 652-656.
29. Galliano, M.F., Huet, C., Frygelius, J., Polgren, A., Wewer, U.M. and Engvall, E. (2000) Binding of ADAM12, a marker of skeletal muscle regeneration, to the muscle-specific actin-binding protein, alpha-actinin-2, is required for myoblast fusion. J. Biol. Chem., 275, 13933-13939.
30. Gilpin, B.J., Loechel, F., Mattei, M.G., Engvall, E., Albrechtsen, R. and Wewer, U.M. (1998) A novel, secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo. J. Biol. Chem., 273, 157-166.
31. Kawaguchi, N., Xu, X., Tajima, R., Kronqvist, P., Sundberg, C., Loechel, F., Albrechtsen, R. and Wewer, U.M. (2002) ADAM 12 protease induces adipogenesis in transgenic mice. Am. J. Pathol., 160, 1895-1903.
32. Thomas, M., Langley, B., Berry, C., Sharma, M., Kirk, S., Bass, J. and Kambadur, R. (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem., 275, 40235-40243.
33. Matsuda, R., Spector, D.H. and Strohman, R.C. (1983) Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin isoforms. Dev. Biol., 100, 478-488.
34. Chen, J., Kubalak, S.W., Minamisawa, S., Price, R.L., Becker, K.D., Hickey, R., Ross, J. Jr and Chien, K.R. (1998) Selective requirement of myosin light chain 2v in embryonic heart function. J. Biol. Chem., 273, 1252-1256.
35. Fidzianska, A. and Kaminska, A. (1995) Neural cell adhesion molecule (N-CAM) as a marker of muscle tissue alternations. Review of the literature and own observations. Folia Neuropathol., 33, 125-128.
36. Spencer, M.J. and Tidball, J.G. (2001) Do immune cells promote the pathology of dystrophin-deficient myopathies? Neuromusc. Disord., 11, 556-564.
37. Khurana, T.S. and Davies, K.E. (2003) Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug Discov., 2, 379-390.
38. Hodges, B.L., Hayashi, Y.K., Nonaka, I., Wang, W., Arahata, K. and Kaufman, S.J. (1997) Altered expression of the alpha7beta1 integrin in human and murine muscular dystrophies. J. Cell Sci., 110, 2873-2881.
39. Bao, Z.Z., Lakonishok, M., Kaufman, S. and Horwitz, A.F. (1993) Alpha 7 beta 1 integrin is a component of the myotendinous junction on skeletal muscle. J. Cell Sci., 106, 579-589.
40. Khurana, T.S., Watkins, S.C., Chafey, P., Chelly, J., Tome, F.M., Fardeau, M., Kaplan, J.C. and Kunkel, L.M. (1991) Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromusc. Disord., 1, 185-194.
41. De la Porte, S., Morin, S. and Koenig, J. (1999) Characteristics of skeletal muscle in mdx mutant mice. Int. Rev. Cytol., 191, 99-148.
42. Weir, A.P., Burton, E.A., Harrod, G. and Davies, K.E. (2002) A- and B-utrophin have different expression patterns and are differentially up-regulated in mdx muscle. J. Biol. Chem., 277, 45285-45290.
43. Courdier-Fruh, I., Barman, L., Briguet, A. and Meier, T. (2002) Glucocorticoid-mediated regulation of utrophin levels in human muscle fibers. Neuromusc. Disord., 12, S95-104.
44. Jasmin, B.J., Angus, L.M., Belanger, G., Chakkalakal, J.V., Gramolini, A.O., Lunde, J.A., Stocksley, M.A. and Thompson, J. (2002) Multiple regulatory events controlling the expression and localization of utrophin in skeletal muscle fibers: insights into a therapeutic strategy. for Duchenne muscular dystrophy. J. Physiol. Paris, 96, 31-42.
45. Ervasti, J.M. and Campbell, K.P. (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol., 122, 809-823.
46. Ervasti, J.M. and Campbell, K.P. (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell, 66, 1121-1131.
47. Mayer, U. (2003) Integrins, redundant or important players in skeletal muscle? J. Biol. Chem., 278, 14587-14590.
48. Watchko, J.F., O'Day, T.L. and Hoffman, E.P. (2002) Functional characteristics of dystrophic skeletal muscle: insights from animal models. J. Appl. Physiol., 93, 407-417.
49. Hayashi, Y.K., Chou, F.L., Engvall, E., Ogawa, M., Matsuda, C., Hirabayashi, S., Yokochi, K., Ziober, B.L., Kramer, R.H., Kaufman, S.J. et al. (1998) Mutations in the integrin alpha7 gene cause congenital myopathy. Nat. Genet., 19, 94-97.
50. Pegoraro, E., Cepollaro, F., Prandini, P., Marin, A., Fanin, M., Trevisan, C.P., El-Messlemani, A.H., Tarone, G., Engvall, E., Hoffman, E.P. et al. (2002) Integrin alpha 7 beta 1 in muscular dystrophy/myopathy of unknown etiology. Am. J. Pathol., 160, 2135-2143.
51. Blake, D.J., Tinsley, J.M. and Davies, K.E. (1996) Utrophin: a structural and functional comparison to dystrophin. Brain Pathol., 6, 37-47.
52. Donalies, M., Cramer, M., Ringwald, M. and Starzinski-Powitz, A. (1991) Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells. Proc. Natl Acad. Sci. USA, 88, 8024-8028.
53. Clerk, A., Morris, G.E., Dubowitz, V., Davies, K.E. and Sewry, C.A. (1993) Dystrophin-related protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem. J., 25, 554-561.
54. Gramolini, A.O., Wu, J. and Jasmin, B.J. (2000) Regulation and functional significance of utrophin expression at the mammalian neuromuscular synapse. Microsci. Res. Tech., 49, 90-100.
55. Helliwell, T.R., Man, N.T., Morris, G.E. and Davies, K.E. (1992) The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromusc. Disord., 2, 177-184.
56. Karpati, G., Carpenter, S., Morris, G.E., Davies, K.E., Guerin, C. and Holland, P. (1993) Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J. Neuropathol. Exp. Neurol., 52, 119-128.
57. Zhu, X., Hadhazy, M., Groh, M.E., Wheeler, M.T., Wollmann, R. and McNally, E.M. (2001) Overexpression of gamma-sarcoglycan induces severe muscular dystrophy. Implications for the regulation of sarcoglycan assembly. J. Biol. Chem., 276, 21785-21790.
58. Wewer, U.M., Iba, K., Durkin, M.E., Nielsen, F.C., Loechel, F., Gilpin, B.J., Kuang, W., Engvall, E. and Albrechtsen, R. (1998) Tetranectin is a novel marker for myogenesis during embryonic development, muscle regeneration, and muscle cell differentiation in vitro. Dev. Biol., 200, 247-259.
59. Floss, T., Arnold, H.H. and Braun, T. (1997) A role for FGF-6 in skeletal muscle regeneration. Genes. Dev., 11, 2040-2051.
60. Vachon, P.H., Xu, H., Liu, L., Loechel, F., Hayashi, Y., Arahata, K., Reed, J.C., Wewer, U.M. and Engvall, E. (1997) Integrins (alpha7beta1) in muscle function and survival. Disrupted expression in merosin-deficient congenital muscular dystrophy. J. Clin. Invest., 100, 1870-1881.
61. Statistical Algorithms Reference Guide (Affymetrix Technical Note), (2001) Part no. 701110.
62. Chen, Y.W., Zhao, P., Borup, R. and Hoffman, E.P. (2000) Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J. Cell Biol., 151, 1321-1336.