β1D chain increases α7β1 integrin and laminin and protects against sarcolemmal damage in mdx mice

Human Molecular Genetics

Volumn 21, Issue 7, 2012, Pages 1592-1603

  Liu, Jianming ^a,d   Milner, Derek J ^a   Boppart, Marni D ^a,b   Ross, Robert S ^c   Kaufman, Stephen J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA7 INTEGRIN; ALPHA7BETA1 INTEGRIN; BETA1 INTEGRIN; HETERODIMER; INTEGRIN; LAMININ; LAMININ ALPHA2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA CHAIN; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; IN VITRO STUDY; MEDIATOR; MOUSE; MUSCLE CELL; MUSCLE INJURY; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SARCOLEMMA; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD29; CELL LINE; ENDOPLASMIC RETICULUM; INTEGRIN ALPHA CHAINS; INTEGRINS; LAMININ; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; MUSCULAR DYSTROPHIES; SARCOLEMMA;

MUS;

EID: 84863257178     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr596     Document Type: Article

References (73)

1. Davies, K.E. and Nowak, K.J. (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat. Rev. Mol. Cell Biol., 7, 762-773.
2. Matsumura, K., Ohlendieck, K., Ionasescu, V.V., Tome, F.M., Nonaka, I., Burghes, A.H., Mora, M., Kaplan, J.C., Fardeau, M. and Campbell, K.P. (1993) The role of the dystrophin-glycoprotein complex in the molecular pathogenesis of muscular dystrophies. Neuromuscul. Disord., 3, 533-535.
3. Campbell, K.P. and Kahl, S.D. (1989) Association of dystrophin and an integral membrane glycoprotein. Nature, 338, 259-262.
4. 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.
5. von der Mark, H., Durr, J., Sonnenberg, A., von der Mark, K., Deutzmann, R. and Goodman, S.L. (1991) Skeletal myoblasts utilize a novel beta 1-series integrin and not alpha 6 beta 1 for binding to the E8 and T8 fragments of laminin. J. Biol. Chem., 266, 23593-23601.
6. Song, W.K., Wang, W., Foster, R.F., Bielser, D.A. and Kaufman, S.J. (1992) H36-alpha 7 is a novel integrin alpha chain that is developmentally regulated during skeletal myogenesis. J. Cell Biol., 117, 643-657.
7. Burkin, D.J. and Kaufman, S.J. (1999) The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res., 296, 183-190.
8. Song, W.K., Wang, W., Sato, H., Bielser, D.A. and Kaufman, S.J. (1993) Expression of alpha 7 integrin cytoplasmic domains during skeletal muscle development: alternate forms, conformational change, and homologies with serine/threonine kinases and tyrosine phosphatases. J. Cell Sci., 106 (Pt 4), 1139-1152.
9. Crawley, S., Farrell, E.M., Wang, W., Gu, M., Huang, H.Y., Huynh, V., Hodges, B.L., Cooper, D.N. and Kaufman, S.J. (1997) The alpha7beta1 integrin mediates adhesion and migration of skeletal myoblasts on laminin. Exp. Cell Res., 235, 274-286.
10. 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 (Pt 2), 579-589.
11. Boppart, M.D., Burkin, D.J. and Kaufman, S.J. (2006) Alpha7beta1-integrin regulates mechanotransduction and prevents skeletal muscle injury. Am. J. Physiol. Cell Physiol., 290, C1660-C1665.
12. Martin, P.T., Kaufman, S.J., Kramer, R.H. and Sanes, J.R. (1996) Synaptic integrins in developing, adult, and mutant muscle: selective association of alpha1, alpha7A, and alpha7B integrins with the neuromuscular junction. Dev. Biol., 174, 125-139.
13. Boppart, M.D., Volker, S.E., Alexander, N., Burkin, D.J. and Kaufman, S.J. (2008) Exercise promotes alpha7 integrin gene transcription and protection of skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R1623-R1630.
14. 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.
15. Mayer, U., Saher, G., Fassler, R., Bornemann, A., Echtermeyer, F., von der Mark, H., Miosge, N., Poschl, E. and von der Mark, K. (1997) Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat. Genet., 17, 318-323.
16. Flintoff-Dye, N.L., Welser, J., Rooney, J., Scowen, P., Tamowski, S., Hatton, W. and Burkin, D.J. (2005) Role for the alpha7beta1 integrin in vascular development and integrity. Dev. Dyn., 234, 11-21.
17. 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.
18. Peat, R.A., Smith, J.M., Compton, A.G., Baker, N.L., Pace, R.A., Burkin, D.J., Kaufman, S.J., Lamande, S.R. and North, K.N. (2008) Diagnosis and etiology of congenital muscular dystrophy. Neurology, 71, 312-321.
19. 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.
20. 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 (Pt 22), 2873-2881.
21. 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.
22. Burkin, D.J., Wallace, G.Q., Milner, D.J., Chaney, E.J., Mulligan, J.A. and Kaufman, S.J. (2005) Transgenic expression of {alpha}7{beta}1 integrin maintains muscle integrity, increases regenerative capacity, promotes hypertrophy, and reduces cardiomyopathy in dystrophic mice. Am. J. Pathol., 166, 253-263.
23. Grady, R.M., Teng, H., Nichol, M.C., Cunningham, J.C., Wilkinson, R.S. and Sanes, J.R. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell, 90, 729-738.
24. Deconinck, A.E., Rafael, J.A., Skinner, J.A., Brown, S.C., Potter, A.C., Metzinger, L., Watt, D.J., Dickson, J.G., Tinsley, J.M. and Davies, K.E. (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell, 90, 717-727.
25. Rooney, J.E., Welser, J.V., Dechert, M.A., Flintoff-Dye, N.L., Kaufman, S.J. and Burkin, D.J. (2006) Severe muscular dystrophy in mice that lack dystrophin and alpha7 integrin. J. Cell Sci., 119, 2185-2195.
26. Guo, C., Willem, M., Werner, A., Raivich, G., Emerson, M., Neyses, L. and Mayer, U. (2006) Absence of alpha 7 integrin in dystrophin-deficient mice causes a myopathy similar to Duchenne muscular dystrophy. Hum. Mol. Genet., 15, 989-998.
27. Allikian, M.J., Hack, A.A., Mewborn, S., Mayer, U. and McNally, E.M. (2004) Genetic compensation for sarcoglycan loss by integrin alpha7beta1 in muscle. J. Cell Sci., 117, 3821-3830.
28. Ziober, B.L., Vu, M.P., Waleh, N., Crawford, J., Lin, C.S. and Kramer, R.H. (1993) Alternative extracellular and cytoplasmic domains of the integrin alpha 7 subunit are differentially expressed during development. J. Biol. Chem., 268, 26773-26783.
29. Vignier, N., Moghadaszadeh, B., Gary, F., Beckmann, J., Mayer, U. and Guicheney, P. (1999) Structure, genetic localization, and identification of the cardiac and skeletal muscle transcripts of the human integrin alpha7 gene (ITGA7). Biochem. Biophys. Res. Commun., 260, 357-364.
30. Collo, G., Starr, L. and Quaranta, V. (1993) A new isoform of the laminin receptor integrin alpha 7 beta 1 is developmentally regulated in skeletal muscle. J. Biol. Chem., 268, 19019-19024.
31. Chernousov, M.A., Kaufman, S.J., Stahl, R.C., Rothblum, K. and Carey, D.J. (2007) Alpha7beta1 integrin is a receptor for laminin-2 on Schwann cells. Glia, 55, 1134-1144.
32. Armulik, A. (2002) Splice variants of human beta 1 integrins: origin, biosynthesis and functions. Front. Biosci., 7, d219-d227.
33. de Melker, A.A. and Sonnenberg, A. (1999) Integrins: alternative splicing as a mechanism to regulate ligand binding and integrin signaling events. Bioessays, 21, 499-509.
34. Brakebusch, C., Hirsch, E., Potocnik, A. and Fassler, R. (1997) Genetic analysis of beta1 integrin function: confirmed, new and revised roles for a crucial family of cell adhesion molecules. J. Cell Sci., 110 (Pt 23), 2895-2904.
35. Belkin, A.M., Retta, S.F., Pletjushkina, O.Y., Balzac, F., Silengo, L., Fassler, R., Koteliansky, V.E., Burridge, K. and Tarone, G. (1997) Muscle beta1D integrin reinforces the cytoskeleton-matrix link: modulation of integrin adhesive function by alternative splicing. J. Cell Biol., 139, 1583-1595.
36. Belkin, A.M., Zhidkova, N.I., Balzac, F., Altruda, F., Tomatis, D., Maier, A., Tarone, G., Koteliansky, V.E. and Burridge, K. (1996) Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells. J. Cell Biol., 132, 211-226.
37. Baudoin, C., Goumans, M.J., Mummery, C. and Sonnenberg, A. (1998) Knockout and knockin of the beta1 exon D define distinct roles for integrin splice variants in heart function and embryonic development. Genes Dev., 12, 1202-1216.
38. Stephens, L.E., Sutherland, A.E., Klimanskaya, I.V., Andrieux, A., Meneses, J., Pedersen, R.A. and Damsky, C.H. (1995) Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev., 9, 1883-1895.
39. Hynes, R.O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell, 69, 11-25.
40. Heino, J., Ignotz, R.A., Hemler, M.E., Crouse, C. and Massague, J. (1989) Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit. J. Biol. Chem., 264, 380-388.
41. Ignotz, R.A., Heino, J. and Massague, J. (1989) Regulation of cell adhesion receptors by transforming growth factor-beta. Regulation of vitronectin receptor and LFA-1. J. Biol. Chem., 264, 389-392.
42. Lenter, M. and Vestweber, D. (1994) The integrin chains beta 1 and alpha 6 associate with the chaperone calnexin prior to integrin assembly. J. Biol. Chem., 269, 12263-12268.
43. Salicioni, A.M., Gaultier, A., Brownlee, C., Cheezum, M.K. and Gonias, S.L. (2004) Low density lipoprotein receptor-related protein-1 promotes beta1 integrin maturation and transport to the cell surface. J. Biol. Chem., 279, 10005-10012.
44. Milner, D.J. and Kaufman, S.J. (2007) a7b1 integrin does not alleviate disease in a mouse model of limb girdle muscular dystrophy type 2F. Am. J. Pathol., 170, 609-619.
45. Liu, J., Burkin, D.J. and Kaufman, S.J. (2008) Increasing a7b1-integrin promotes muscle cell proliferation, adhesion, and resistance to apoptosis without changing gene expression. Am. J. Physiol. Cell Physiol., 294, C627-C640.
46. Bulfield, G., Siller, W.G., Wight, P.A. and Moore, K.J. (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl Acad. Sci. USA, 81, 1189-1192.
47. Bellet, M., Whalen, J.J., Bodin, F., Serrurier, D., Tanner, K. and Menard, J. (1990) Use of crossover trials to obtain antihypertensive dose-response curves and to study combination therapy during the development of benazepril. J. Hypertens. Suppl., 8, S43-S48.
48. Carlson, B.M. and Faulkner, J.A. (1983) The regeneration of skeletal muscle fibers following injury: a review. Med. Sci. Sports Exerc., 15, 187-198.
49. DiMario, J.X., Uzman, A. and Strohman, R.C. (1991) Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev. Biol., 148, 314-321.
50. Karpati, G., Carpenter, S. and Prescott, S. (1988) Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve, 11, 795-803.
51. Webster, C., Silberstein, L., Hays, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
52. Whalen, R.G., Harris, J.B., Butler-Browne, G.S. and Sesodia, S. (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev. Biol., 141, 24-40.
53. Rajagopalan, S., Xu, Y. and Brenner, M.B. (1994) Retention of unassembled components of integral membrane proteins by calnexin. Science, 263, 387-390.
54. 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.
55. Bakay, M., Zhao, P., Chen, J. and Hoffman, E.P. (2002) A web-accessible complete transcriptome of normal human and DMD muscle. Neuromuscul. Disord., 12 (Suppl. 1), S125-S141.
56. Cachaco, A.S., Chuva de Sousa Lopes, S.M., Kuikman, I., Bajanca, F., Abe, K., Baudoin, C., Sonnenberg, A., Mummery, C.L. and Thorsteinsdottir, S. (2003) Knock-in of integrin beta 1D affects primary but not secondary myogenesis in mice. Development, 130, 1659-1671.
57. Burkin, D.J., Gu, M., Hodges, B.L., Campanelli, J.T. and Kaufman, S.J. (1998) A functional role for specific spliced variants of the alpha7beta1 integrin in acetylcholine receptor clustering. J. Cell Biol., 143, 1067-1075.
58. Burkin, D.J., Kim, J.E., Gu, M. and Kaufman, S.J. (2000) Laminin and alpha7beta1 integrin regulate agrin-induced clustering of acetylcholine receptors. J. Cell Sci., 113 (Pt 16), 2877-2886.
59. Pham, C.G., Harpf, A.E., Keller, R.S., Vu, H.T., Shai, S.Y., Loftus, J.C. and Ross, R.S. (2000) Striated muscle-specific beta(1D)-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am. J. Physiol. Heart Circ. Physiol., 279, H2916-H2926.
60. Odom, G.L., Gregorevic, P. and Chamberlain, J.S. (2007) Viral-mediated gene therapy for the muscular dystrophies: successes, limitations and recent advances. Biochim. Biophys. Acta, 1772, 243-262.
61. Judge, L.M. and Chamberlain, J.S. (2005) Gene therapy for Duchenne muscular dystrophy: AAV leads the way. Acta Myol., 24, 184-193.
62. Duan, D. (2006) Challenges and opportunities in dystrophin-deficient cardiomyopathy gene therapy. Hum. Mol. Genet., 15 (Suppl. 2), R253-R261.
63. Matsuda, R., Nishikawa, A. and Tanaka, H. (1995) Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem., 118, 959-964.
64. Hoffman, E.P., Brown, R.H. Jr and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
65. Koenig, M., Hoffman, E.P., Bertelson, C.J., Monaco, A.P., Feener, C. and Kunkel, L.M. (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell, 50, 509-517.
66. Allamand, V. and Campbell, K.P. (2000) Animal models for muscular dystrophy: valuable tools for the development of therapies. Hum. Mol. Genet., 9, 2459-2467.
67. Boland, B.J., Silbert, P.L., Groover, R.V., Wollan, P.C. and Silverstein, M.D. (1996) Skeletal, cardiac, and smooth muscle failure in Duchenne muscular dystrophy. Pediatr. Neurol., 14, 7-12.
68. Lefaucheur, J.P., Pastoret, C. and Sebille, A. (1995) Phenotype of dystrophinopathy in old mdx mice. Anat. Rec., 242, 70-76.
69. Pastoret, C. and Sebille, A. (1993) Further aspects of muscular dystrophy in mdx mice. Neuromuscul. Disord., 3, 471-475.
70. Torres, L.F. and Duchen, L.W. (1987) The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain, 110 (Pt 2), 269-299.
71. Rooney, J.E., Gurpur, P.B. and Burkin, D.J. (2009) Laminin-111 protein therapy prevents muscle disease in the mdx mouse model for Duchenne muscular dystrophy. Proc. Natl Acad. Sci. USA, 106, 7991-7996.
72. -/- mouse model for Duchenne muscular dystrophy. Regen. Med., 2, 275-288.
73. Liu, J., Gurpur, P.B. and Kaufman, S.J. (2008) Genetically determined proteolytic cleavage modulates alpha7beta1 integrin function. J. Biol. Chem., 283, 35668-35678.