Nerve growth factor gene therapy using adeno-associated viral vectors prevents cardiomyopathy in type 1 diabetic mice

Diabetes

Volumn 61, Issue 1, 2012, Pages 229-240

  Meloni, Marco ^a   Descamps, Betty ^a   Caporali, Andrea ^a   Zentilin, Lorena ^b   Floris, Ilaria ^a   Giacca, Mauro ^b   Emanueli, Costanza ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF TRIESTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; MESSENGER RNA; NERVE GROWTH FACTOR; PARVOVIRUS VECTOR; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE TRANSFER; HEART DILATATION; HEART FUNCTION; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART MUSCLE PERFUSION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MICROVASCULARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; STREPTOZOCIN DIABETES; SURVIVAL; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; DEPENDOVIRUS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC CARDIOMYOPATHIES; GENE EXPRESSION REGULATION; GENE THERAPY; GENETIC VECTORS; HEK293 CELLS; HUMANS; MALE; MICE; MYOCARDIUM; NERVE GROWTH FACTOR; STREPTOZOCIN;

EID: 84555186722     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0763     Document Type: Article

References (48)

1. Litwin SE, Raya TE, Anderson PG, Daugherty S, Goldman S. Abnormal cardiac function in the streptozotocin-diabetic rat. Changes in active and passive properties of the left ventricle. J Clin Invest 1990;86:481-488 (Pubitemid 20271880)
2. Moir S, Hanekom L, Fang ZY, et al. Relationship between myocardial perfusion and dysfunction in diabetic cardiomyopathy: a study of quantitative contrast echocardiography and strain rate imaging. Heart 2006;92: 1414-1419 (Pubitemid 44578830)
3. Sabbah HN, Sharov VG, Lesch M, Goldstein S. Progression of heart failure: a role for interstitial fibrosis. Mol Cell Biochem 1995;147:29-34
4. Caporali A, Sala-Newby GB, Meloni M, et al. Identification of the prosurvival activity of nerve growth factor on cardiac myocytes. Cell Death Differ 2008;15:299-311
5. Meloni M, Caporali A, Graiani G, et al. Nerve growth factor promotes cardiac repair following myocardial infarction. Circ Res 2010;106:1275-1284
6. Cantarella G, Lempereur L, Presta M, et al. Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 2002;16: 1307-1309
7. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P. Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 2002;106:2257-2262 (Pubitemid 35222222)
8. Hellweg R, Hartung HD. Endogenous levels of nerve growth factor (NGF) are altered in experimental diabetes mellitus: a possible role for NGF in the pathogenesis of diabetic neuropathy. J Neurosci Res 1990;26:258-267 (Pubitemid 20197832)
9. Ieda M, Kanazawa H, Ieda Y, et al. Nerve growth factor is critical for cardiac sensory innervation and rescues neuropathy in diabetic hearts. Circulation 2006;114:2351-2363 (Pubitemid 44847452)
10. Schmid H, Forman LA, Cao X, Sherman PS, Stevens MJ. Heterogeneous cardiac sympathetic denervation and decreased myocardial nerve growth factor in streptozotocin-induced diabetic rats: implications for cardiac sympathetic dysinnervation complicating diabetes. Diabetes 1999;48:603-608 (Pubitemid 29106876)
11. Kaye DM, Vaddadi G, Gruskin SL, Du XJ, Esler MD. Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ Res 2000;86:E80-E84
12. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008;16:1073-1080 (Pubitemid 351737072)
13. Gao G, Vandenberghe LH, Wilson JM. New recombinant serotypes of AAV vectors. Curr Gene Ther 2005;5:285-297 (Pubitemid 40895013)
14. Nathwani AC, Davidoff A, Hanawa H, Zhou JF, Vanin EF, Nienhuis AW. Factors influencing in vivo transduction by recombinant adeno-associated viral vectors expressing the human factor IX cDNA. Blood 2001;97:1258-1265 (Pubitemid 32183747)
15. Pacak CA, Mah CS, Thattaliyath BD, et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 2006;99:e3-e9 (Pubitemid 44255502)
16. Ferrarini M, Arsic N, Recchia FA, et al. Adeno-associated virus-mediated transduction of VEGF165 improves cardiac tissue viability and functional recovery after permanent coronary occlusion in conscious dogs. Circ Res 2006;98:954-961
17. Arsic N, Zacchigna S, Zentilin L, et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther 2004;10:844-854 (Pubitemid 39419911)
18. Grimm D, Kern A, Rittner K, Kleinschmidt JA. Novel tools for production and purification of recombinant adenoassociated virus vectors. Hum Gene Ther 1998;9:2745-2760 (Pubitemid 29027018)
19. Inagaki K, Fuess S, Storm TA, et al. 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)
20. Rabinowitz JE, Rolling F, Li C, et al. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 2002;76:791-801 (Pubitemid 34033377)
21. Emanueli C, Salis MB, Pinna A, et al. Prevention of diabetes-induced microangiopathy by human tissue kallikrein gene transfer. Circulation 2002; 106:993-999 (Pubitemid 34925336)
22. Katare R, Caporali A, Zentilin L, et al. Intravenous gene therapy with PIM-1 via a cardiotropic viral vector halts the progression of diabetic cardiomyopathy through promotion of prosurvival signaling. Circ Res 2011;108:1238-1251
23. Yoon YS, Uchida S, Masuo O, et al. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation 2005;111:2073-2085 (Pubitemid 40577902)
24. Chowdhry MF, Vohra HA, Galinanes M. Diabetes increases apoptosis and necrosis in both ischemic and nonischemic human myocardium: role of caspases and poly-adenosine diphosphate-ribose polymerase. J Thorac Cardiovasc Surg 2007;134:124-131
25. Potente M, Urbich C, Sasaki K, et al. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 2005;115:2382-2392 (Pubitemid 41266200)
26. Skurk C, Izumiya Y, Maatz H, et al. The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling. J Biol Chem 2005;280:20814-20823 (Pubitemid 40776786)
27. Lekli I, Mukherjee S, Ray D, et al. Functional recovery of diabetic mouse hearts by glutaredoxin-1 gene therapy: role of Akt-FoxO-signaling network. Gene Ther 2010;17:478-485
28. Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 1993;16:434-444 (Pubitemid 23046633)
29. Van Linthout S, Spillmann F, Riad A, et al. Human apolipoprotein A-I gene transfer reduces the development of experimental diabetic cardiomyopathy. Circulation 2008;117:1563-1573 (Pubitemid 351444665)
30. Katare RG, Caporali A, Oikawa A, Meloni M, Emanueli C, Madeddu P. Vitamin B1 analog benfotiamine prevents diabetes-induced diastolic dysfunction and heart failure through Akt/Pim-1-mediated survival pathway. Circ Heart Fail 2010;3:294-305
31. Bugger H, Abel ED. Rodent models of diabetic cardiomyopathy. Dis Model Mech 2009;2:454-466
32. Levi-Montalcini R. The nerve growth factor. Ann N Y Acad Sci 1964;118: 149-170
33. Hiltunen JO, Laurikainen A, Väkevä A, Meri S, Saarma M. Nerve growth factor and brain-derived neurotrophic factor mRNAs are regulated in distinct cell populations of rat heart after ischaemia and reperfusion. J Pathol 2001;194:247-253
34. Bartlett RJ, McCue JM. Adeno-associated virus based gene therapy in skeletal muscle. Methods Mol Biol 2000;133:127-156
35. Johnson JS, Samulski RJ. Enhancement of adeno-associated virus infection by mobilizing capsids into and out of the nucleolus. J Virol 2009;83: 2632-2644
36. Schannwell CM, Schneppenheim M, Perings S, Plehn G, Strauer BE. Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology 2002;98:33-39 (Pubitemid 35375651)
37. Palmieri V, Capaldo B, Russo C, et al. Uncomplicated type 1 diabetes and preclinical left ventricular myocardial dysfunction: insights from echocardiography and exercise cardiac performance evaluation. Diabetes Res Clin Pract 2008;79:262-268
38. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 2004;25:543-567 (Pubitemid 39096070)
39. Fischer VW, Barner HB, Larose LS. Pathomorphologic aspects of muscular tissue in diabetes mellitus. Hum Pathol 1984;15:1127-1136 (Pubitemid 15128118)
40. Cameron DP, Amherdt M, Leuenberger P, Orci L, Stauffacher W. Microvascular alterations in chronically streptozotocin-diabetic rats. Adv Metab Disord 1973;2(Suppl 2): 257-269
41. Frustaci A, Kajstura J, Chimenti C, et al. Myocardial cell death in human diabetes. Circ Res 2000;87:1123-1132
42. Cai L, Li W, Wang G, Guo L, Jiang Y, Kang YJ. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002;51:1938-1948 (Pubitemid 34564309)
43. Salis MB, Graiani G, Desortes E, Caldwell RB, Madeddu P, Emanueli C. Nerve growth factor supplementation reverses the impairment, induced by type 1 diabetes, of hindlimb post-ischaemic recovery in mice. Diabetologia 2004;47:1055-1063 (Pubitemid 38918165)
44. Graiani G, Emanueli C, Desortes E, et al. Nerve growth factor promotes reparative angiogenesis and inhibits endothelial apoptosis in cutaneous wounds of Type 1 diabetic mice. Diabetologia 2004;47:1047-1054 (Pubitemid 38918164)
45. Holgado-Madruga M, Moscatello DK, Emlet DR, Dieterich R, Wong AJ. Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc Natl Acad Sci USA 1997;94:12419-12424 (Pubitemid 27492543)
46. Park MJ, Kwak HJ, Lee HC, et al. Nerve growth factor induces endothelial cell invasion and cord formation by promoting matrix metalloproteinase- 2 expression through the phosphatidylinositol 3-kinase/Akt signaling pathway and AP-2 transcription factor. J Biol Chem 2007;282: 30485-30496
47. Shimizu M, Umeda K, Sugihara N, et al. Collagen remodelling in myocardia of patients with diabetes. J Clin Pathol 1993;46:32-36 (Pubitemid 23039583)
48. Devereux RB, Roman MJ, Paranicas M, et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 2000;101:2271-2276 (Pubitemid 30317129)