Heart angiotensin II-induced cardiomyocyte hypertrophy suppresses coronary angiogenesis and progresses diabetic cardiomyopathy

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 9, 2012, Pages

  Masuda, Takahiro ^a   Muto, Shigeaki ^a   Fujisawa, Genro ^b   Iwazu, Yoshitaka ^a   Kimura, Mariko ^c   Kobayashi, Takahisa ^a   Nonaka Sarukawa, Mutsuko ^c   Sasaki, Nobuhiro ^a   Watanabe, Yuko ^a   Shinohara, Masami ^d   Murakami, Takashi ^e   Shimada, Kazuyuki ^c   Kobayashi, Eiji ^e   Kusano, Eiji ^a  

^a Divisions of Nephrology   (Japan)

^b Fujisawa Medical Clinic   (Japan)

^c Department of Internal Medicine   (Japan)

^d CLEA Japan Inc   (Japan)

^e JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Angiogenic factor; Antiangiogenic factor; Thrombospondin 1; Vascular endothelial growth factor; Vascular endothelial growth factor receptor 2

Indexed keywords

ANGIOTENSIN II; CE 2; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INSULIN; MYOSIN; OLMESARTAN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAPILLARY PROLIFERATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; GLUCOSE BLOOD LEVEL; HEART HYPERTROPHY; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HYPOXIA; INSULIN RELEASE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; UPREGULATION;

ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANIMALS; APOPTOSIS; DIABETES MELLITUS, TYPE 2; DIABETIC CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; HYPERTROPHY; HYPERTROPHY, LEFT VENTRICULAR; IMIDAZOLES; MALE; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, MUTANT STRAINS; RATS, SPRAGUE-DAWLEY; TETRAZOLES; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84860511322     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00663.2011     Document Type: Article

References (56)

1. Aneja A, Tang WH, Bansilal S, Garcia MJ, Farkouh ME. Diabetic cardiomyopathy: insights into pathogenesis, diagnostic challenges, and therapeutic options. Am J Med 121: 748-757, 2008.
2. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 115: 3213-3223, 2007.
3. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345: 861-869, 2001.
4. + exchanger and cardiac hypertrophy. Circ Res 83: 870-873, 1998.
5. Fiordaliso F, Li B, Latini R, Sonnenblick EH, Anversa P, Leri A, Kajstura J. Myocyte death in streptozotocin-induced diabetes in rats in angiotensin II-dependent. Lab Invest 80: 513-527, 2000.
6. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, Nadal-Ginard B, Anversa P. Myocardial cell death in human diabetes. Circ Res 87: 1123-1132, 2000.
7. Fujii H, Hamada Y, Fukagawa M. Bone formation in spontaneously diabetic Torii-newly established model of non-obese type 2 diabetes rats. Bone 42: 372-379, 2008.
8. Fujisawa G, Okada K, Muto S, Fujita N, Itabashi N, Kusano E, Ishibashi S. Na/H exchange isoform 1 is involved in mineralocorticoid/ salt-induced cardiac injury. Hypertension 41: 493-498, 2003.
9. Fujisawa G, Okada K, Muto S, Fujita N, Itabashi N, Kusano E, Ishibashi S. Spironolactone prevents early renal injury in streptozotocininduced diabetic rats. Kidney Int 66: 1493-1502, 2004.
10. Guo N, Krutzsch HC, Inman JK, Roberts DD. Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res 57: 1735-1742, 1997.
11. Han B, Baliga R, Huang H, Giannone PJ, Bauer JA. Decreased cardiac expression of vascular endothelial growth factor and redox imbalance in murine diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 297: H829-H835, 2009.
12. Heart Outcomes Prevention Evaluation (HOPE) Study Investigators. Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICROHOPE substudy. Lancet 355: 253-259, 2000.
13. Howlett SE. Age-associated changes in excitation-contraction coupling are more prominent in ventricular myocytes from male rats than in myocytes from female rats. Am J Physiol Heart Circ Physiol 298: H659-H670, 2010.
14. Iruela-Arispe ML, Bornstein P, Sage H. Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cells in vitro. Proc Natl Acad Sci USA 88: 5026-5030, 1991.
15. Iwazu Y, Muto S, Fujisawa G, Nakazawa E, Okada K, Ishibashi S, Kusano E. Spironolactone suppresses peritubular capillary loss and prevents deoxycorticosterone acetate/salt-induced tubulointerstitial fibrosis. Hypertension 51: 749-754, 2008.
16. Izumiya Y, Kim S, Izumi Y, Yoshida K, Yoshiyama M, Matsuzawa A, Ichijo H, Iwao H. Apoptosis signal-regulating kinase 1 plays a pivotal role in angiotensin II-induced cardiac hypertrophy and remodeling. Circ Res 93: 874-883, 2003.
17. Irigoyen M, Anso E, Salvo E, de las Herreritas J, Martinez-Irujo JJ, Rouzaunt A. TGF-induced protein mediates lymphatic endothelial cell adhesion to the extracellular matrix under low oxygen conditions. Cell Mol Lif Sci 65: 2244-2255, 2008.
18. Jalil JE, Doering CW, Janicki JS, Pick R, Shroff SG, Weber KT. Fibrillar collagen and myocardial stiffness in the intact hypertrophied rat left ventricle. Circ Res 64: 1041-1050, 1989.
19. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6: 41-48, 2000.
20. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, Roberts DD. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J Biol Chem 285: 38923-38932, 2010.
21. Knollmann BC, Blatt SA, Horton K, de Freitas F, Miller T, Bell M, Housmans PR, Weissman NJ, Morad M, Potter JD. Inotropic stimulation induces cardiac dysfunction in transgenic mice expressing a troponin T (I79N) mutation linked to familial hypertrophic cardiomyopathy. J Biol Chem 276: 10039-10048, 2001.
22. Masuyama T, Komeda K, Hara A, Noda M, Shinohara M, Oikawa T, Kanazawa Y, Taniguchi K. Chronological characterization of diabetes development in male spontaneously diabetic Torii rats. Biochem Biophys Res Commun 314: 870-877, 2004.
23. Mazzolai L, Pedrazzini T, Nicoud F, Gabbiani G, Brunner HR, Nussberger J. Increased cardiac angiotensin II levels induce right and left ventricular hypertrophy in normotensive mice. Hypertension 35: 985-991, 2000.
24. Mbanya JC, Thomas TH, Taylor R, Alberti KG, Wilkinson R. Increased proximal tubular sodium reabsorption in hypertensive patients with type 2 diabetes. Diabet Med 6: 614-620, 1989.
25. Miao G, Ito T, Uchikoshi F, Kamei M, Akamaru Y, Kiyomoto T, Komoda H, Nozawa M, Matsuda H. Stage-dependent effect of pancreatic transplantation on diabetic ocular complications in the spontaneously diabetic Torii rat. Transplantation 77: 658-663, 2004.
26. Miele C, Rochford JJ, Filippa N, Giorgetti-Peraldi S, Van Obberghen E. Insulin and insulin-like growth factor-I induce vascular endothelial growth factor mRNA expression via different signaling pathways. J Biol Chem 275: 21695-21702, 2000.
27. Mizuno M, Sada T, Kato M, Koike H. Renoprotective effects of blockade of angiotensin II AT1 receptors in an animal model of type 2 diabetes. Hypertens Res 25: 271-278, 2002.
28. Morgan-Rowe L, Nikitorowicz J, Shiwen X, Leask A, Tsui J, Abraham D, Stratton R. Thrombospondin 1 in hypoxia-conditioned media blocks the growth of human microvascular endothelial cells and is increased in systemic sclerosis tissues. Firogenesis Tissue Repair 4: 13, 2011.
29. Nakagawa T, Li JH, Garcia G, Mu W, Pie KE, Bottinger EP, Chen Y, Zhu HJ, Kang DH, Schreiner GF, Lan HY, Johnson RJ. TGF- induced proangiogenic and antiangiogenic factors via parallel but distinct Smad pathways. Kidney Int 66: 605-613, 2004.
30. Negoescu A, Lafeuillade B, Pellerin S, Chambaz EM, Feige JJ. Transforming growth factors stimulate both thrombospondin-1 and CISP/ thrombospondin-2 synthesis by bovine adrenocortical cells. Exp Cell Res 217: 404-409, 1995.
31. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13: 9-22, 1999.
32. Okamoto M, Ono M, Uchiumi T, Ueno H, Kohno K, Sugimachi K, Kuwano M. Up-regulation of thrombospondin-1 gene by epidermal growth factor and transforming growth factor in human cancer cells- transcriptional activation and messenger RNA stabilization. Biochim Biophys Acta 1574: 24-34, 2002.
33. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling-in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371, 2006.
34. Osada-Oka M, Ikeda T, Akiba S, Sato T. Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1α-dependent expression of thrombospondin-1. J Cell Biochem 104: 1918-1926, 2008.
35. Price DA, Porter LE, Gordon M, Fisher ND, De'Oliveira JM, Laffel LM, Passan DR, Williams GH, Hollenberg NK. The paradox of the low-renin state in diabetic nephropathy. J Am Soc Nephrol 10: 2382-2391, 1999.
36. Sabri A, Samuel JL, Marotte F, Poitevin P, Rappaport L, Levy BI. Microvasculature in angiotensin II-dependent cardiac hypertrophy in the rat. Hypertension 32: 371-375, 1998.
37. Sano M, Minamino T, Toko H, Miyauchi H, Orimo M, Qin Y, Akazawa H, Tateno K, Kayama Y, Harada M, Shimizu I, Asahara T, Hamada H, Tomita S, Molkentin JD, Zou Y, Komuro I. p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload. Nature 446: 444-448, 2007.
38. Sasso FC, Carbonara O, Persico E, D'Ambrosio R, Coppola L, Nasti R, Campana B, Moschella S, Torella R, Cozzolino D. Increased vascular endothelial growth factor mRNA expression in the heart of streptozotocin- induced diabetic rats. Metabolism 52: 675-678, 2003.
39. Sasso FC, Torella D, Carbonara O, Ellison GM, Torella M, Scardone M, Marra C, Nasti R, Marfella R, Cozzolino D, Indolfi C, Cotrufo M, Torella R, Salvatore T. Increased vascular endothelial growth factor expression but impaired vascular endothelial growth factor receptor signaling in the myocardium of type 2 diabetic patients with chronic coronary heart disease. J Am Coll Cardiol 46: 827-834, 2005.
40. Schunkert H, Dzau VJ, Tang SS, Hirsch AT, Apstein CS, Lorell BH. Increased rat cardiac angiotensin converting enzyme activity and mRNA expression in pressure overload left ventricular hypertrophy. Effects on coronary resistance, contractility, and relaxation. J Clin Invest 86: 1913-1920, 1990.
41. Schunkert H, Sadoshima J, Cornelius T, Kagaya Y, Weinberg EO, Izumo S, Riegger G, Lorell BH. Angiotensin II-induced growth responses in isolated adult rat hearts. Evidence for load-independent induction of cardiac protein synthesis by angiotensin II. Circ Res 76: 489-497, 1995.
42. Schwocho LR, Masonson HN. Pharmacokinetics of CS-866, a new angiotensin II receptor blocker, in healthy subjects. J Clin Pharmacol 41: 515-527, 2001.
43. Shimoni Y, Hunt D, Chen K, Emmett T, Kargacin G. Differential autocrine modulation of atrial and ventricular potassium currents and of oxidative stress in diabetic rats. Am J Physiol Heart Circ Physiol 290: H1879-H1888, 2006.
44. Shinohara M, Masuyama T, Shoda T, Takahashi T, Katsuda Y, Komeda K, Kuroki M, Kakehashi A, Kanazawa Y. A new spontaneously diabetic non-obese Torii rat strain with severe ocular complications. Int J Exp Diabetes Res 1: 89-100, 2000.
45. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest 115: 2108-2118, 2005.
46. Singh VP, Le B, Khode R, Baker KM, Kumar R. Intracellular angiotensin II production in diabetic rats is correlated with cardiomyocyte apoptosis, oxidative stress, and cardiac fibrosis. Diabetes 57: 3297-3306, 2008.
47. Stenina OI, Krukovets I, Wang K, Zhou Z, Forudi F, Penn MS, Topol EJ, Plow EF. Increased expression of thrombospondin-1 in vessel wall of diabetic Zucker rat. Circulation 107: 3209-3215, 2003.
48. Tanaka H, Nagasawa I, Matsui I, Hamano T, Iwatani H, Kawada N, Horio M, Ito T, Isaka Y, Imai E. Pharmacokinetics of olmesartan medoxomil in hemodialysis patients: little effect of dialysis upon its pharmacokinetics. Clin Exp Nephrol 13: 61-65, 2009.
49. Thomas WG, Brandenburger Y, Autelitano DJ, Pham T, Qian H, Hannan RD. Adenoviral-directed expression of the type 1A angiotensin receptor promotes cardiomyocyte hypertrophy via transactivation of the epidermal growth factor receptor. Circ Res 90: 135-142, 2002.
50. Tojo A, Onozato ML, Kobayashi N, Goto A, Matsuoka H, Fujita T. Angiotensin II and oxidative stress in Dahl Salt-sensitive rat with heart failure. Hypertension 40: 834-839, 2002.
51. Walker EM, Nillas MS, Mangiarua EI, Cansino S, Morrison RG, Perdue RR, Triest WE, Wright GL, Studeny M, Wehner P, Rice KM, Blough ER. Age-associated changes in hearts of male Fisher 344/Brown Norway F1 rats. Ann Clin Lab Sci 36: 427-437, 2006.
52. Yagi S, Aihara K, Ikeda Y, Sumitomo Y, Yoshida S, Ise T, Iwase T, Ishikawa K, Azuma H, Akaike M, Matsumoto T. Pitavastatin, an HMG-CoA reductase inhibitor, exerts eNOS-independent protective actions against angiotensin II induced cardiovascular remodeling and renal insufficiency. Circ Res 102: 68-76, 2008.
53. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am J Physiol Heart Circ Physiol 277: H1967-H1974, 1999.
54. Yoon YS, Uchida S, Masuo O, Cejna M, Park JS, Gwon HC, Kirchmair R, Bahlman F, Walter D, Curry C, Hanley A, Isner JM, Losordo DW. 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 111: 2073-2085, 2005.
55. Zhou Y, Poczatek MH, Berecek KH, Murphy-Ullrich JE. Thrombospondin 1 mediates angiotensin II induction of TGF- activation by cardiac and renal cells under both high and low glucose conditions. Biochem Biophys Res Commun 339: 633-641, 2006.
56. Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12: 452-458, 2006.