Renin inhibition attenuates insulin resistance, oxidative stress, and pancreatic remodeling in the transgenic Ren2 rat

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5643-5653

  Habibi, Javad ^a   Whaley Connell, Adam ^a,c   Hayden, Melvin R ^a   DeMarco, Vincent G ^a   Schneider, Rebecca ^a   Sowers, Susan D ^a   Karuparthi, Poorna ^a   Ferrario, Carlos M ^b   Sowers, James R ^a,c  

^a University of Missouri   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ALISKIREN; ANGIOTENSIN II; INSULIN RECEPTOR SUBSTRATE 2; PROTEIN KINASE B; PROTEIN SUBUNIT; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART INJURY; INSULIN RESISTANCE; KIDNEY INJURY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PANCREAS FUNCTION; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; TRANSGENIC RAT;

AMIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; FUMARATES; GLUCOSE TOLERANCE TEST; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; OXIDATIVE STRESS; PANCREAS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; REGENERATION; RENIN;

EID: 54349098473     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0070     Document Type: Article

References (41)

1. Cooper, SA, Whaley-Connell A, Habibi, J, Wei Y, Lastra G, Manrique C, Stas S, Sowers JR 2007 Renin-angiotensin-aldosterone system and oxidative stress in cardiovascular insulin resistance. Am J Physiol Heart Circ Physiol 293:H2009-H2023
2. Lau T, Carlsson PO, Leung PS 2004 Evidence for a local angiotensin system and dose-dependent inhibition of glucose-stimulated insulin release by angiotensin II in isolated pancreatic islets. Diabetologia 47:240-248
3. Tahmasebi M, Puddefoot JR, Inwang ER, Vinson GP 1999 The tissue renin-angiotensin system in human pancreas. J Endocrinol 161:317-322
4. Leung PS, Carlsson PO 2001 Tissue renin-angiotensin system: its expression, localization, regulation and potential role in the pancreas. J Mol Endocrinol 26:155-164
5. Leung PS, Chappell MC 2003 A local pancreatic renin-angiotensin system: endocrine and exocrine roles. Int J Biochem Cell Biol 35:838-846
6. Tikellis C, Wookey PJ, Candido R, Andrikopoulos S, Thomas MC, Cooper ME 2004 Improved islet morphology after blockade of the renin-angiotensin system in the ZDF rat. Diabetes 53:989-997
7. Nakayama M, Inoguchi T, Sonta T, Maeda Y, Sasaki S, Sawada F, Tsubouchi H, Sonoda N, Kobayashi K, Sumimoto H, Nawata H 2005 Increased expression of NAD(P)H oxidase in islets of animal models of type 2 diabetes and its improvement by AT1 receptor antagonist. Biochem Biophys Res Commun 332:4:927-933
8. Oliveira HR, Verlengia R, Carvalho CR, Britto LR, Curi R, Carpinelli AR 2003 Pancreatic β-cells express phagocyte-like NAD(P)H oxidase. Diabetes 52:1457-1463
9. Blendea MC, Jacobs D, Stump CS, McFarlane SI, Ogrin C, Bahtyiar G, Stas S, Kumar P, Sha Q, Ferrario CM, Sowers JR 2005 Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am J Physiol Endocrinol Metab 288:E353-E359
10. Whaley-Connell AT, Chowdhury NA, Hayden MR, Stump CS, Habibi J, Wiedmeyer CE, Ferrario CM, Sowers JR 2006 Oxidative stress and glomerular filtration barrier injury: role of the renin-angiotensin system in the Ren2 transgenic rat. Am J Physiol Renal Physiol 291:F1308-F1314
11. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, Morris EM, Szary N, Manrique C, Stump CS 2006 Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 281:35137-35146
12. Whaley-Connell A, Govindarajan G, Habibi J, Hayden MR, Cooper SA, Wei Y, Ma L, Qazi M, Link D, Karuparthi PR, Stump C, Ferrario C, Sowers JR 2007 Angiotensin-II mediated oxidative stress promotes myocardial tissue remodeling in the transgenic TG (mRen2) 27 Ren2 Rat. Am J Physiol Endocrinol Metab 293:E355-E363
13. Habibi J, Whaley-Connell A, Qazi MA, Hayden MR, Cooper SA, Tramontano A, Thyfault J, Stump C, Ferrario C, Muniyappa R, Sowers JR 2007 Rosuvastatin, a HMG-CoA reductase inhibitor, decreases cardiac oxidative stress and remodeling in Ren2 transgenic rats. Endocrinology 148:2181-2188
14. Stas S, Whaley-Connell A, Habibi J, Appesh L, Hayden MR, Karuparthi PR, Qazi M, Morris EM, Cooper SA, Link CD, Stump C, Hay M, Ferrario C, Sowers JR 2007 Mineralocorticoid receptor blockade attenuates chronic angiotensin-II overexpression stimulation of NADPH oxidase and cardiac remodeling. Endocrinology 148:3773-3780
15. Hayden MR, Chowdhury NA, Cooper SA, Whaley-Connell A, Habibi J, Witte L, Wiedmeyer C, Manrique CM, Lastra G, Ferrario C, Stump C, Sowers JR 2007 Proximal tubule microvilli remodeling and albuminuria in the Ren2 transgenic rat. Am J Physiol Renal Physiol 292:F861-F867
16. Hayden MR, Stump C, Sowers JR 2006 Organ involvement in cardiometabolic syndrome. J Cardiometab Syndr 1:16-24
17. Hayden MR, Sowers JR 2007 Isletopathy in type 2 diabetes: implications of islet RAS, islet fibrosis, islet amyloid, remodeling, and oxidative stress. Antiox Redox Signal 9:891-910
18. Hayden MR, Karuparthi PR, Habibi J, Wasekar C, Lastra G, Manrique C, Stas S, Sowers JR 2007 Ultrastructural islet study of early fibrosis in the Ren 2 rat model of hypertension. Emerging role of the islet pancreatic pericyte-stellate cell. J Pancreas 8:725-738
19. Robertson RP, Harmon J, Tran PO, Tanaka Y, Takahashi H 2003 Glucose toxicity in β-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 52:581-587
20. Sakurai K, Katoh M, Someno K, Fujimoto Y 2001 Apoptosis and mitochondrial damage in INS-1 cells treated with alloxan. Biol Pharm Bull 24:876-882
21. Turk J, Corbett JA, Ramanadham S, Bohrer A, McDaniel ML 1993 Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islet. Biochem Biophys Res Commun 197:1458-1464
22. Kampf C, Lau T, Olsson R, Leung PS, Carlsson PO 2005 Angiotensin II type 1 receptor inhibition markedly improves the blood perfusion, oxygen tension and first phase of glucose-stimulated insulin secretion in revascularised syngeneic mouse islet grafts. Diabetologia 48:1159-1167
23. Chu KY, Lau T, Carlsson PO, Leung PS 2006 Angiotensin II type 1 receptor blockade improves β-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 55:367-374
24. Rahuel J, Rasetti V, Maibaum J, Rueger H, Goschke R, Cohen NC, Stutz S, Cumin F, Fuhrer W, Wood JM, Grutter MG 2000 Structure-based drug design: the discovery of novel nonpeptide orally active inhibitors of human renin. Chem Biol 7:493-504
25. Wood JM, Schnell CR, Cumin F, Menard J, Webb RL 2005 Aliskiren, a novel, orally effective renin inhibitor, lowers blood pressure in marmosets and spontaneously hypertensive rats. J Hypertens 23:417-426
26. Lee MA, Bohm M, Kim S, Bachmann S, Bachmann J, Bader M, Ganten D 1995 Differential gene expression of renin and angiotensinogen in the TGR(mREN-2)27 transgenic rat. Hypertension 25(4 Pt 1):570-580
27. Rector RS, Thyfault JP, Morris RT, Laye MJ, Borengasser SJ, Booth FW, Ibdah JA 2008 Daily exercise increases hepatic fatty acid oxidation and prevents steatosis in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Am J Physiol Gastrointest Liver Physiol 294:G619-G626
28. Nguyen G, Delarue F, Burcklé C, Bouzhir L, Giller T, Sraer JD 2002 Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109:1417-1427
29. Danser AH 2006 Prorenin: back into the arena. Hypertension 47:824-826
30. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Görgün C, Glimcher LH, Hotamisligil GS 2005 Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461
31. Laight DW, Desai KM, Gopaul NK, Anggård EE, Carrier MJ 1999 Pro-oxidant challenge in vivo provokes the onset of NIDDM in the insulin resistant Zucker rat. Br Journal Pharmacol 128:269-271
32. Tanaka Y, Gleason CE, Tran PO, Harmon JS, Robertson RP 1999 Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci USA 96:10857-10862
33. Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, Hiai H, Seino Y, Yamada Y 1999 Hyperglycemia causes oxidative stress in pancreatic β-cells of GK rats, a model of type 2 diabetes. Diabetes 48:927-932
34. Tsubouchi H, Inoguchi T, Inuo M, Kakimoto M, Sonta T, Sonoda N, Sasaki S, Kobayashi K, Sumimoto H, Nawata H 2005 Sulfonylurea as well as elevated glucose levels stimulate reactive oxygen species production in the pancreatic β cell line, MIN6-a role in NADPH oxidase in β cells. Biochem Biophys Res Commun 7:60-65
35. Chappell MC, Diz DL, Gallager PE 2001 The renin-angiotensin system and the exocrine pancreas. J Pancreas 2:33-39
36. Tsang SW, Cheng CH, Leung PS 2004 The role of pancreatic renin-angiotensin system in acinar digestive enzyme secretion and acute pancreatitis. Regul Pept 119:213-219
37. Tzang SW, Ip SP, Wong TP, Che CT, Leung PS 2003 Differential effects of saralasin and ramaprilat, the inhibitors of renin-angiotensin system, on cerulean-induced acute pancreatitis. Regul Pept 111:47-53
38. Kuno A, Yamada T, Masuda K, Ogawa K, Sogawa M, Nakamura S, Nakazawa T, Ohara H, Nomura T, Joh T, Shirai T, Itoh M 2003 Angiotensin-converting enzyme inhibitor attenuates pancreatic inflammation and fibrosis in male Wistar Bonn/Kobori rats. Gastroenterology 124:1010-1019
39. Krauss S, Zhang CY, Scorrano L, Dalgaard LT, St. Pierre J, Grey ST, Lowell BB 2003 Superoxide-mediated activation of uncoupling protein 2 causes pancreatic β cell dysfunction. J Clin Invest 112:1831-1842
40. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD 2002 Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99
41. Kaneto H, Nakatani Y, Kawamori D, Miyatsuka T, Matsuoka TA, Matsuhisa M, Yamasaki Y 2005 Role of oxidative stress, endoplasmic reticulum stress, and c-Jun-terminal kinase in pancreatic β-cell dysfunction and insulin resistance. Int J Biochem Cell Biol 37:1595-1608