Myotendinous junction defects and reduced force transmission in mice that lack α7 integrin and utrophin

American Journal of Pathology

Volumn 175, Issue 4, 2009, Pages 1545-1554

  Welser, Jennifer V ^a   Rooney, Jachinta E ^a   Cohen, Nicolette C ^a   Gurpur, Praveen B ^a   Singer, Cherie A ^a   Evans, Rebecca A ^a   Haines, Bryan A ^a   Burkin, Dean J ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA7 INTEGRIN; BETA1 INTEGRIN; DYSTROPHIN; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; LETHALITY; MALE; MOUSE; MUSCLE DISEASE; MUSCLE FORCE; MUSCLE FUNCTION; MUSCLE STRENGTH; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

EID: 73549105246     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.090052     Document Type: Article

References (46)

1. Emery AEH: Duchenne muscular dystrophy-Meryon's disease. Neuromuscular Disorders 1993, 3:263-266
2. Moser H: Duchenne muscular dystrophy - pathogenetic aspects and genetic prevention. Human Genetics 1984, 66:17-40
3. Campbell KP: Three muscular dystrophies: loss of cytoskeletonextracellular matrix linkage. Cell 1995, 80:675-679
4. Bulfield G, Siller WG, Wight PA, Moore KJ: X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984, 81:1189-1192
5. Hoffman EP, Brown RH, Kunkel LM: Dystrophin - the protein product of the Duchenne Muscular Dystrophy locus. Cell 1987, 51:919-928
6. Matsumura K, Tome FMS, Collin H, Leturcq F, Jeanpierre M, Kaplan JC, Fardeau M, Campbell KP: Expression of dystrophin-associated proteins in dystrophin-positive muscle-fibers (revertants) in Duchenne muscular dystrophy. Neuromusc Dis 1994, 4:115-120
7. Monaco AP, Neve RL, Collettifeener C, Bertelson CJ, Kurnit DM, Kunkel LM: Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 1986, 323:646-650
8. Senter L, Luise M, Presotto C, Betto R, Teresi A, Ceoldo S, Salviati G: Interaction of dystrophin with cytoskeletal proteins - binding to talin and actin. Biochem Biophys Res Comm 1993, 192:899-904
9. Cohn RD, Campbell KP: Molecular basis of muscular dystrophies. Muscle Nerve 2000, 23:1456-1471
10. Burkin DJ, Wallace GQ, Nicol KJ, Kaufman DJ, Kaufman SJ: Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J Cell Biol 2001, 152:1207-1218
11. Burkin DJ, Wallace GQ, Milner DJ, Chaney EJ, Mulligan JA, Kaufman SJ: Transgenic expression of alpha7beta1 integrin maintains muscle integrity, increases regenerative capacity, promotes hypertrophy, and reduces cardiomyopathy in dystrophic mice. Am J Pathol 2005, 166:253-263
12. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, Young C, Metzinger L, Vincent A, Slater CR, Davies KE: Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 1997, 136:883-894
13. Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L, Watt DJ, Dickson JG, Tinsley JM, Davies KE: Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 1997, 90:717-727
14. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR: Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 1997, 90:729-738
15. Grady RM, Merlie JP, Sanes JR: Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 1997, 136:871-882
16. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE: Skeletal muscle-specific expression of a utrophin transgene rescues utrophindystrophin deficient mice. Nat Genet 1998, 19:79-82
17. Rafael JA, Townsend ER, Squire SE, Potter AC, Chamberlain JS, Davies KE: Dystrophin and utrophin influence fiber type composition and post-synaptic membrane structure. Hum Mol Genet 2000, 9:1357-1367
18. Heydemann A, McNally EM: Regenerating more than muscle in muscular dystrophy. Circulation 2004, 110:3290-3292
19. Hodges BL, Hayashi YK, Nonaka I, Wang W, Arahata K, Kaufman SJ: Altered expression of the alpha7beta1 integrin in human and murine muscular dystrophies. J Cell Sci 1997, 110 (Pt 22):2873-2881
20. Weir AP, Burton EA, Harrod G, Davies KE: A- and B-utrophin have different expression patterns and are differentially up-regulated in mdx muscle. J Biol Chem 2002, 277:45285-45290
21. Karpati G, Carpenter S, Morris GE, Davies KE, Guerin C, Holland P: Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J Neuropathol Exp Neurol 1993, 52:119-128
22. Martin PT, Kaufman SJ, Kramer RH, Sanes JR: Synaptic integrins in developing, adult, and mutant muscle: selective association of alpha1, alpha7A, and alpha7B integrins with the neuromuscular junction. Dev Biol 1996, 174:125-139
23. Burkin DJ, Kaufman SJ: The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res 1999, 296:183-190
24. Song WK, Wang W, Sato H, Bielser DA, Kaufman SJ: 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 1993, 106 (Pt 4):1139-1152
25. Hayashi YK, Chou FL, Engvall E, Ogawa M, Matsuda C, Hirabayashi S, Yokochi K, Ziober BL, Kramer RH, Kaufman SJ, Ozawa E, Goto Y, Nonaka I, Tsukahara T, Wang JZ, Hoffman EP, Arahata K: Mutations in the integrin alpha7 gene cause congenital myopathy. Nat Genet 1998, 19:94-97
26. Flintoff-Dye NL, Welser J, Rooney J, Scowen P, Tamowski S, Hatton W, Burkin DJ: Role for the alpha7beta1 integrin in vascular development and integrity. Dev Dyn 2005, 234:11-21
27. Welser JV, Lange ND, Flintoff-Dye N, Burkin HR, Burkin DJ: Placental defects in alpha7 integrin null mice. Placenta 2007, 28:1219-1228
28. Rooney JE, Welser JV, Dechert MA, Flintoff-Dye NL, Kaufman SJ, Burkin DJ: Severe muscular dystrophy in mice that lack dystrophin and alpha7 integrin. J Cell Sci 2006, 119:2185-2195
29. Mayer U, Saher G, Fassler R, Bornemann A, Echtermeyer F, von der MH, Miosge N, Poschl E, von der MK: Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat Genet 1997, 17:318-323
30. Nawrotzki R, Willem M, Miosge N, Brinkmeier H, Mayer U: Defective integrin switch and matrix composition at alpha 7-deficient myotendinous junctions precede the onset of muscular dystrophy in mice. Hum Mol Genet 2003, 12:483-495
31. Guo C, Willem M, Werner A, Raivich G, Emerson M, Neyses L, Mayer U: Absence of alpha 7 integrin in dystrophin-deficient mice causes a myopathy similar to Duchenne muscular dystrophy. Hum Mol Genet 2006, 15:989-998
32. Pearce M, Blake DJ, Tinsley JM, Byth BC, Campbell L, Monaco AP, Davies KE: The utrophin and dystrophin genes share similarities in genomic structure. Hum Mol Genet 1993, 2:1765-1772
33. Tinsley JM, Blake DJ, Roche A, Fairbrother U, Riss J, Byth BC, Knight AE, Kendrick-Jones J, Suthers GK, Love DR: Primary structure of dystrophin-related protein. Nature 1992, 360: 591-593
34. Ohlendieck K, Ervasti JM, Matsumura K, Kahl SD, Leveille CJ, Campbell KP: Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 1991, 7:499-508
35. Khurana TS, Watkins SC, Chafey P, Chelly J, Tome FM, Fardeau M, Kaplan JC, Kunkel LM: Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul Disord 1991, 1:185-194
36. Pons F, Nicholson LV, Robert A, Voit T, Leger JJ: Dystrophin, and dystrophin-related protein (utrophin) distribution in normal and dystrophin-deficient skeletal muscles. Neuromuscul Disord 1993, 3:507-514
37. Ervasti JM: Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim Biophys Acta (BBA) - Mol Basis Dis 2007, 1772:108-117
38. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K: Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 1998, 4:1441-1444
39. Belkin AM, Zhidkova NI, Balzac F, Altruda F, Tomatis D, Maier A, Tarone G, Koteliansky VE, Burridge K: Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells. J Cell Biol 1996, 132:211-226
40. Pons F, Robert A, Fabbrizio E, Hugon G, Califano JC, Fehrentz JA, Martinez J, Mornet D: Utrophin localization in normal and dystrophin-deficient heart. Circulation 1994, 90:369-374
41. Welser JV, Lange N, Singer CA, Elorza M, Scowen P, Keef KD, Gerthoffer WT, Burkin DJ: Loss of the alpha7 integrin promotes extracellular signal-regulated kinase activation and altered vascular remodeling. Circ Res 2007, 101:672-681
42. Law DJ, Tidball JG: Dystrophin deficiency is associated with myotendinous junction defects in prenecrotic and fully regenerated skeletal muscle. Am J Pathol 1993, 142:1513-1523
43. Ridge JC, Tidball JG, Ahl K, Law DJ, Rickoll WL: Modifications in myotendinous junction surface morphology in dystrophin-deficient mouse muscle. Exp Mol Pathol 1994, 61:58-68
44. Grady RM, Akaaboune M, Cohen AL, Maimone MM, Lichtman JW, Sanes JR: Tyrosine-phosphorylated and nonphosphorylated isoforms of alpha-dystrobrevin: roles in skeletal muscle and its neuromuscular and myotendinous junctions. J Cell Biol 2003, 160:741-752
45. Miner JH, Go G, Cunningham J, Patton BL, Jarad G: Transgenic isolation of skeletal muscle and kidney defects in laminin beta 2 mutant mice: implications for Pierson syndrome. Development 2006, 133:967-975
46. Banks GB, Combs AC, Chamberlain JR, Chamberlain JS: Molecular and cellular adaptations to chronic myotendinous strain injury in mdx mice expressing a truncated dystrophin. Hum Mol Genet 2008, 17:3975-3986