Combined deficiency of dystrophin and β1 integrin in the cardiac myocyte causes myocardial dysfunction, fibrosis and calcification

Circulation Research

Volumn 102, Issue 9, 2008, Pages 1109-1117

  Elsherif, Laila ^a,b   Huang, Michael S ^a,b,e   Shai, Shaw Yung ^c   Yang, Yuan ^b   Li, Rita Y ^a,b   Chun, June ^a,b   Mekany, Majid A ^a   Chu, Andrew L ^a   Kaufman, Stephen J ^d   Ross, Robert S ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Calcification; Dystrophin; Heart failure; Integrin; Muscular dystrophy

Indexed keywords

4 CARBOXYGLUTAMIC ACID; BETA1 INTEGRIN; DECORIN; DYSTROPHIN; ISOPRENALINE; TRANSCRIPTION FACTOR RUNX2;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEATH; DISEASE PREDISPOSITION; DISEASE SEVERITY; DUCHENNE MUSCULAR DYSTROPHY; EXPERIMENTAL ANIMAL; FEMALE; GENETIC TRANSCRIPTION; HEART FAILURE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE FUNCTION; MALE; MORTALITY; MOUSE; MYOCARDIAL DISEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PUERPERIUM; SKELETAL MUSCLE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ADRENERGIC BETA-AGONISTS; ANIMALS; ANTIGENS, CD29; CALCINOSIS; CALCIUM-BINDING PROTEINS; CARDIOMYOPATHIES; CELL ADHESION MOLECULES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DISEASE MODELS, ANIMAL; DOBUTAMINE; DYSTROPHIN; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FIBROSIS; HEART FAILURE; ISOPROTERENOL; MALE; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MYOCYTES, CARDIAC; NECROSIS; PHENOTYPE; PREGNANCY; PROTEOGLYCANS; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; TIME FACTORS; UP-REGULATION; VENTRICULAR FUNCTION;

EID: 43449121854     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.173153     Document Type: Article

References (45)

1. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC. Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol. 2002;18:637-706.
2. Ervasti JM. Costameres: the Achilles' heel of Herculean muscle. J Biol Chem. 2003;278:13591-13594.
3. Stevenson S, Rothery S, Cullen MJ, Severs NJ. Dystrophin is not a specific component of the cardiac costamere. Circ Res. 1997;80:269-280.
4. Lapidos KA, Kakkar R, McNally EM. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res. 2004;94:1023-1031.
5. Quinlan JG, Hahn HS, Wong BL, Lorenz JN, Wenisch AS, Levin LS. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord. 2004;14:491-496.
6. Kamogawa Y, Biro S, Maeda M, Setoguchi M, Hirakawa T, Yoshida H, Tei C. Dystrophin-deficient myocardium is vulnerable to pressure overload in vivo. Cardiovasc Res. 2001;50:509-515.
7. Janssen PM, Hiranandani N, Mays TA, Rafael-Fortney JA. Utrophin deficiency worsens cardiac contractile dysfunction present in dystrophin-deficient mdx mice. Am J Physiol Heart Circ Physiol. 2005;289:H2373-H2378.
8. Hainsey TA, Senapati S, Kuhn DE, Rafael JA. Cardiomyopathic features associated with muscular dystrophy are independent of dystrophin absence in cardiovasculature. Neuromuscul Disord. 2003;13:294-302.
9. Ross RS, Borg TK. Integrins and the myocardium. Circ Res. 2001;88:1112-1119.
10. Ingber D. Integrins as mechanochemical transducers. Curr Opin Cell Biol. 1991;3:841-848.
11. Rooney JE, Welser JV, Dechert MA, Flintoff-Dye NL, Kaufman SJ, Burkin DJ. Severe muscular dystrophy in mice that lack dystrophin and {alpha}7 integrin. J Cell Sci. 2006;119(pt 11):2185-2195.
12. 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.
13. Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, Omura M, Leil TA, Becker KD, Jiang M, Smith DJ, Cherry SR, Loftus JC, Ross RS. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res. 2002;90:458-464.
14. 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;106:1139-1152.
15. Valencik ML, McDonald JA. Cardiac expression of a gain-of-function alpha(5)-integrin results in perinatal lethality. Am J Physiol Heart Circ Physiol. 2001;280:H361-H367.
16. Grove BK, Kurer V, Lehner C, Doetschman TC, Perriard JC, Eppenberger HM. A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol. 1984;98:518-524.
17. Abbas AE, Lester SJ, Connolly H. Pregnancy and the cardiovascular system. Int J Cardiol. 2005;98:179-189.
18. Geissinger HD, Rao PV, Donald-Taylor CK. "mdx" mouse myopathy: histopathological, morphometric and histochemical observations on young mice. J Comp Pathol. 1990;102:249-263.
19. Abedin M, Tintut Y, Demer LL. Vascular calcification: mechanisms and clinical ramifications. Arterioscler Thromb Vasc Biol. 2004;24:1161-1170.
20. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechano-transduction. Am J Physiol Heart Circ Physiol. 2005;289:H2291-H2301.
21. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature. 1992;360:588-591.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, Davies KE. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature. 1996;384:349-353.
28. Bristow MR, Ginsburg R, Minobe W, Cubicciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DC, Stinson EB. Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med. 1982;307:205-211.
29. Lohse MJ, Engelhardt S, Eschenhagen T. What is the role of beta-adrenergic signaling in heart failure? Circ Res. 2003;93:896-906.
30. Cheng Q, Ross RS, Walsh KB. Overexpression of the integrin beta(1A) subunit and the beta(1A) cytoplasmic domain modifies the beta-adrenergic regulation of the cardiac L-type Ca(2+)current. J Mol Cell Cardiol. 2004;36:809-819.
31. Brunnert SR. Morphologic response of myocardium to freeze-thaw injury in mouse strains with dystrophic cardiac calcification. Lab Anim Sci. 1997;47:11-18.
32. Gang DL, Barrett LV, Wilson EJ, Rubin RH, Medearis DN. Myopericarditis and enhanced dystrophic cardiac calcification in murine cytomegalovirus infection. Am J Pathol. 1986;124:207-215.
33. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, Jaleel N, Chua BH, Hewett TE, Robbins J, Houser SR, Molkentin JD. Ca2+-and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J Clin Invest. 2007;117:2431-2444.
34. McConnell BK, Jones KA, Fatkin D, Arroyo LH, Lee RT, Aristizabal O, Turnbull DH, Georgakopoulos D, Kass D, Bond M, Niimura H, Schoen FJ, Conner D, Fischman DA, Seidman CE, Seidman JG. Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest. 1999;104:1235-1244.
35. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol. 1996;134:1255-1270.
36. Ikeda Y, Martone M, Gu Y, Hoshijima M, Thor A, Oh SS, Peterson KL, Ross J Jr. Altered membrane proteins and permeability correlate with cardiac dysfunction in cardiomyopathic hamsters. Am J Physiol Heart Circ Physiol. 2000;278:H1362-H1370.
37. Weisleder N, Soumaka E, Abbasi S, Taegtmeyer H, Capetanaki Y. Cardiomyocyte-specific desmin rescue of desmin null cardiomyopathy excludes vascular involvement. J Mol Cell Cardiol. 2004;36:121-128.
38. Petrof BJ. Molecular pathophysiology of myofiber injury in deficiencies of the dystrophin-glycoprotein complex. Am J Phys Med Rehabil. 2002;81:S162-S174.
39. Alloatti G, Gallo MP, Penna C, Levi RC. Properties of cardiac cells from dystrophic mouse. J Mol Cell Cardiol. 1995;27:1775-1779.
40. Alderton JM, Steinhardt RA. Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem. 2000;275:9452-9460.
41. Shanahan CM, Cary NR, Metcalfe JC, Weissberg PL. High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest. 1994;93:2393-2402.
42. Norris RA, Kern CB, Wessels A, Moralez EI, Markwald RR, Mjaatvedt CH. Identification and detection of the periostin gene in cardiac development. Anat Rec A Discov Mol Cell Evol Biol. 2004;281:1227-1233.
43. Katsuragi N, Morishita R, Nakamura N, Ochiai T, Taniyama Y, Hasegawa Y, Kawashima K, Kaneda Y, Ogihara T, Sugimura K. Periostin as a novel factor responsible for ventricular dilation. Circulation. 2004;110:1806-1813.
44. Stanton LW, Garrard LJ, Damm D, Garrick BL, Lam A, Kapoun AM, Zheng Q, Protter AA, Schreiner GF, White RT. Altered patterns of gene expression in response to myocardial infarction. Circ Res. 2000;86:939-945.
45. Ducy P. Cbfa1: a molecular switch in osteoblast biology. Dev Dyn. 2000;219:461-471.