Delta-Sarcoglycan gene therapy halts progression of cardiac dysfunction, improves respiratory failure, and prolongs life in myopathic hamsters

Circulation: Heart Failure

Volumn 4, Issue 1, 2011, Pages 89-97

  Hoshijima, Masahiko ^a,b,c,d   Hayashi, Takeharu ^a,c   Jeon, Young E ^a,b,c   Fu, Zhenxing ^b   Gu, Yusu ^a   Dalton, Nancy D ^b   Ellisman, Mark H ^a   Xiao, Xiao ^d   Powell, Frank L ^b   Ross, John ^b  

^a Research in Biological Systems   (United States)

^b Department of Medicine ^*  (United States)

^c National Center for Microscopy and Imaging Research   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cardiomyopathy; Gene therapy; Heart failure; Muscles; Respiration

Indexed keywords

ADENOVIRUS VECTOR; CAVEOLIN 3; DELTA SARCOGLYCAN; DYSTROPHIN; PLACEBO; CARDIOVASCULAR AGENT; SARCOGLYCAN;

AGE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ECHOCARDIOGRAPHY; ELECTRON TOMOGRAPHY; GENE THERAPY; HAMSTER; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CELL; LIFESPAN; MALE; MORTALITY; MUSCLE ATROPHY; MYOPATHY; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY FAILURE; RESPIRATORY FUNCTION; TRANSVERSE TUBULAR SYSTEM; TREATMENT OUTCOME; ADENOVIRUS; ANIMAL; BREATHING MUSCLE; DISEASE MODEL; GENETICS; HEART FAILURE; HEART MUSCLE; LONGEVITY; MUSCLE DISEASE; PATHOLOGY; SYRIAN HAMSTER;

ADENOVIRIDAE; ANIMALS; CARDIOVASCULAR AGENTS; CRICETINAE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE THERAPY; HEART FAILURE; LONGEVITY; MALE; MESOCRICETUS; MUSCULAR DISEASES; MYOCARDIUM; RESPIRATORY INSUFFICIENCY; RESPIRATORY MUSCLES; SARCOGLYCANS;

EID: 79952266296     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.110.957258     Document Type: Article

References (43)

1. McNally EM, Pytel P. Muscle diseases: the muscular dystrophies. Annu Rev Pathol. 2007;2:87-109. (Pubitemid 46448061)
2. Finsterer J. Cardiopulmonary support in Duchenne muscular dystrophy. Lung. 2006;184:205-215. (Pubitemid 44477406)
3. Wagner KR, Lechtzin N, Judge DP. Current treatment of adult Duchenne muscular dystrophy. Biochim Biophys Acta. 2007;1772:229-237. (Pubitemid 46123913)
4. Nigro V, Okazaki Y, Belsito A, Piluso G, Matsuda Y, Politano L, Nigro G, Ventura C, Abbondanza C, Molinari AM, Acampora D, Nishimura M, Hayashizaki Y, Puca GA. Identification of the Syrian hamster cardiomyopathy gene. Hum Mol Genet. 1997;6:601-607. (Pubitemid 27142112)
5. Sakamoto A, Ono K, Abe M, Jasmin G, Eki T, Murakami Y, Masaki T, Toyo-Oka T, Hanaoka F. Both hypertrophic and dilated cardiomyopathies are caused by mutation of the same gene, delta-sarcoglycan, in hamster: an animal model of disrupted dystrophin-associated glycoprotein complex. Proc Natl Acad Sci U S A. 1997;94:13873-13878. (Pubitemid 28009677)
6. Homburger F. Myopathy of hamster dystrophy: history and morphologic aspects. Ann N Y Acad Sci. 1979;317:1-17.
7. Holt KH, Lim LE, Straub V, Venzke DP, Duclos F, Anderson RD, Davidson BL, Campbell KP. Functional rescue of the sarcoglycan complex in the BIO 14.6 hamster using delta-sarcoglycan gene transfer. Mol Cell. 1998;1:841-848. (Pubitemid 128379068)
8. Ikeda Y, Gu Y, Iwanaga Y, Hoshijima M, Oh SS, Giordano FJ, Chen J, Nigro V, Peterson KL, Chien KR, Ross J Jr. Restoration of deficient membrane proteins in the cardiomyopathic hamster by in vivo cardiac gene transfer. Circulation. 2002;105:502-508. (Pubitemid 34141709)
9. Kawada T, Nakazawa M, Nakauchi S, Yamazaki K, Shimamoto R, Urabe M, Nakata J, Hemmi C, Masui F, Nakajima T, Suzuki J, Monahan J, Sato H, Masaki T, Ozawa K, Toyo-Oka T. Rescue of hereditary form of dilated cardiomyopathy by rAAV-mediated somatic gene therapy: amelioration of morphological findings, sarcolemmal permeability, cardiac performances, and the prognosis of TO-2 hamsters. Proc Natl Acad Sci U S A. 2002;99:901-906. (Pubitemid 34106608)
10. Li J, Wang D, Qian S, Chen Z, Zhu T, Xiao X. Efficient and long-term intracardiac gene transfer in delta-sarcoglycan-deficiency hamster by adeno-associated virus-2 vectors. Gene Ther. 2003;10:1807-1813. (Pubitemid 37185138)
11. Zhu T, Zhou L, Mori S, Wang Z, McTiernan CF, Qiao C, Chen C, Wang DW, Li J, Xiao X. Sustained whole-body functional rescue in congestive heart failure and muscular dystrophy hamsters by systemic gene transfer. Circulation. 2005;112:2650-2659. (Pubitemid 41532602)
12. Vitiello C, Faraso S, Sorrentino NC, Di Salvo G, Nusco E, Nigro G, Cutillo L, Calabro R, Auricchio A, Nigro V. Disease rescue and increased lifespan in a model of cardiomyopathy and muscular dystrophy by combined AAV treatments. PLoS One. 2009;4:e5051.
13. Goehringer C, Rutschow D, Bauer R, Schinkel S, Weichenhan D, Bekeredjian R, Straub V, Kleinschmidt JA, Katus HA, Muller OJ. Prevention of cardiomyopathy in delta-sarcoglycan knockout mice after systemic transfer of targeted adeno-associated viral vectors. Cardiovasc Res. 2009; 82:404-410.
14. Strobeck JE, Factor SM, Bhan A, Sole M, Liew CC, Fein F, Sonnenblick EH. Hereditary and acquired cardiomyopathies in experimental animals: mechanical, biochemical, and structural features. Ann N Y Acad Sci. 1979;317:59-88.
15. Jasmin G, Proschek L. Hereditary polymyopathy and cardiomyopathy in the Syrian hamster, I: progression of heart and skeletal muscle lesions in the UM-X7.1 line. Muscle Nerve. 1982;5:20-25. (Pubitemid 12164821)
16. Hoshijima M, Ikeda Y, Iwanaga Y, Minamisawa S, Date MO, Gu Y, Iwatate M, Li M, Wang L, Wilson JM, Wang Y, Ross J Jr, Chien KR. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat Med. 2002;8:864-871.
17. Iwanaga Y, Hoshijima M, Gu Y, Iwatate M, Dieterle T, Ikeda Y, Date MO, Chrast J, Matsuzaki M, Peterson KL, Chien KR, Ross J Jr. Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J Clin Invest. 2004;113: 727-736. (Pubitemid 38544166)
18. 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.
19. Aaron EA, Powell FL. Effect of chronic hypoxia on hypoxic ventilatory response in awake rats. J Appl Physiol. 1993;74:1635-1640. (Pubitemid 23133452)
20. Hayashi T, Martone ME, Yu Z, Thor A, Doi M, Holst MJ, Bajaj CL, Ellisman MH, Hoshijima M. Three-dimensional electron microscopy reveals new details of membrane systems for calcium signaling in the heart. J Cell Sci. 2009;122:1005-1013.
21. Inagaki K, Fuess S, Storm TA, Gibson GA, McTiernan CF, Kay MA, Nakai H. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther. 2006;14:45-53. (Pubitemid 43899488)
22. Pacak CA, Mah CS, Thattaliyath BD, Conlon TJ, Lewis MA, Cloutier DE, Zolotukhin I, Tarantal AF, Byrne BJ. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res. 2006;99:e3-e9. (Pubitemid 44255502)
23. Bostick B, Ghosh A, Yue Y, Long C, Duan D. Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Ther. 2007;14:1605-1609. (Pubitemid 350056232)
24. Yang L, Jiang J, Drouin LM, Agbandje-McKenna M, Chen C, Qiao C, Pu D, Hu X, Wang DZ, Li J, Xiao X. A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection. Proc Natl Acad Sci U S A. 2009;106:3946-3951.
25. Heydemann A, McNally EM. Consequences of disrupting the dystrophin-sarcoglycan complex in cardiac and skeletal myopathy. Trends Cardiovasc Med. 2007;17:55-59. (Pubitemid 46205328)
26. Brette F, Orchard C. Resurgence of cardiac t-tubule research. Physiology (Bethesda). 2007;22:167-173.
27. Sen LY, O'Neill M, Marsh JD, Smith TW. Myocyte structure, function, and calcium kinetics in the cardiomyopathic hamster heart. Am J Physiol. 1990;259:H1533-H1543. (Pubitemid 20385756)
28. Williams TM, Lisanti MP. The Caveolin genes: from cell biology to medicine. Ann Med. 2004;36:584-595. (Pubitemid 40051435)
29. Tanaka A, Hisanaga A, Ishinishi N. The frequency of spontaneouslyoccurring neoplasms in the male Syrian golden hamster. Vet Hum Toxicol. 1991;33:318-321.
30. Kamino K, Tillmann T, Boschmann E, Mohr U. Age-related incidence of spontaneous non-neoplastic lesions in a colony of Han:AURA hamsters. Exp Toxicol Pathol. 2001;53:157-164. (Pubitemid 32625758)
31. Coral-Vazquez R, Cohn RD, Moore SA, Hill JA, Weiss RM, Davisson RL, Straub V, Barresi R, Bansal D, Hrstka RF, Williamson R, Campbell KP. Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: a novel mechanism for cardiomyopathy and muscular dystrophy. Cell. 1999;98:465-474. (Pubitemid 29402484)
32. Belenkie I, Smith ER, Tyberg JV. Ventricular interaction: from bench to bedside. Ann Med. 2001;33:236-241. (Pubitemid 32500405)
33. Agostoni P, Cattadori G, Bussotti M, Apostolo A. Cardiopulmonary interaction in heart failure. Pulm Pharmacol Ther. 2007;20:130-134. (Pubitemid 44780154)
34. Yu Z, Holst MJ, Hayashi T, Bajaj CL, Ellisman MH, McCammon JA, Hoshijima M. Three-dimensional geometric modeling of membrane-bound organelles in ventricular myocytes: bridging the gap between microscopic imaging and mathematical simulation. J Struct Biol. 2008;164:304-313.
35. Page E, Iida H, Doyle DD. Cell physiology and cell biology of myocardial cell caveolae. In: Page E, Fozzard HA, Solaro RJ, eds. Section 2, The Cardiovascular System: Volume I, The Heart. Bethesda, Md: American Physiological Society; 2002:145-168.
36. Stan RV. Structure of caveolae. Biochim Biophys Acta. 2005;1746: 334-348. (Pubitemid 41815027)
37. Forbes MS, Sperelakis N. The presence of transverse and axial tubules in the ventricular myocardium of embryonic and neonatal guinea pigs. Cell Tissue Res. 1976;166:83-90.
38. Forbes MS, Sperelakis N. Ultrastructure of mammalian cardiac muscle. In: Sperelakis N, ed. Physiology and Pathophysiology of the Heart. Dordrecht, The Netherlands: Kluwer Academic Publishers;1984:3-42.
39. Crosbie RH, Yamada H, Venzke DP, Lisanti MP, Campbell KP. Caveolin-3 is not an integral component of the dystrophin glycoprotein complex. FEBS Lett. 1998;427:279-282. (Pubitemid 28225074)
40. Minetti C, Bado M, Broda P, Sotgia F, Bruno C, Galbiati F, Volonte D, Lucania G, Pavan A, Bonilla E, Lisanti MP, Cordone G. Impairment of caveolae formation and T-system disorganization in human muscular dystrophy with caveolin-3 deficiency. Am J Pathol. 2002;160:265-270. (Pubitemid 34052287)
41. Kemper AR, Wake MA. Duchenne muscular dystrophy: issues in expanding newborn screening. Curr Opin Pediatr. 2007;19:700-704. (Pubitemid 350145241)
42. Townsend D, Yasuda S, Li S, Chamberlain JS, Metzger JM. Emergent dilated cardiomyopathy caused by targeted repair of dystrophic skeletal muscle. Mol Ther. 2008;16:832-835. (Pubitemid 351587091)
43. McMinn TR Jr, Ross J Jr. Hereditary dilated cardiomyopathy. Clin Cardiol. 1995;18:7-15.