The renin angiotensin system, oxidative stress and mitochondrial function in obesity and insulin resistance

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1863, Issue 5, 2017, Pages 1106-1114

  Ramalingam, Latha ^a   Menikdiwela, Kalhara ^a   LeMieux, Monique ^b   Dufour, Jannette M ^a,c   Kaur, Gurvinder ^a,c   Kalupahana, Nishan ^a,d   Moustaid Moussa, Naima ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b TEXAS WOMAN'S UNIVERSITY   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PERADENIYA   (Sri Lanka)

Author keywords

NADPH oxidases; Obesity and insulin resistance; Oxidative stress; Renin angiotensin System

Indexed keywords

ANGIOTENSIN RECEPTOR; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SIRTUIN;

ADIPOSE TISSUE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GLUCOSE HOMEOSTASIS; HEART; HUMAN; INFLAMMATION; INSULIN RESISTANCE; LIVER; METABOLIC DISORDER; MITOCHONDRION; NONHUMAN; OBESITY; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SKELETAL MUSCLE; TARGET TISSUE; ANIMAL; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; MITOCHONDRIA; OBESITY; OXIDATIVE STRESS; RENIN-ANGIOTENSIN SYSTEM;

EID: 84992702465     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2016.07.019     Document Type: Review

References (99)

1. [1] O'Neill, S., O'Driscoll, L., Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes. Rev. 16:1 (2015), 1–12.
2. [2] Kalupahana, N.S., Moustaid-Moussa, N., Claycombe, K.J., Immunity as a link between obesity and insulin resistance. Mol. Asp. Med. 33:1 (2012), 26–34.
3. [3] Chawla, A., Nguyen, K.D., Goh, Y.P., Macrophage-mediated inflammation in metabolic disease. Nat. Rev. Immunol. 11:11 (2011), 738–749.
4. [4] Ouchi, N., Parker, J.L., Lugus, J.J., Walsh, K., Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11:2 (2011), 85–97.
5. [5] Kalupahana, N.S., Moustaid-Moussa, N., The renin-angiotensin system: a link between obesity, inflammation and insulin resistance. Obes. Rev. 13:2 (2012), 136–149.
6. [6] Banday, A.A., Lokhandwala, M.F., Oxidative stress causes renal angiotensin II type 1 receptor upregulation, Na +/H + exchanger 3 overstimulation, and hypertension. Hypertension 57:3 (2011), 452–459.
7. [7] Cichoz-Lach, H., Michalak, A., Oxidative stress as a crucial factor in liver diseases. World J. Gastroenterol. 20:25 (2014), 8082–8091.
8. [8] Luo, H., Wang, X., Chen, C., Wang, J., Zou, X., Li, C., et al. Oxidative stress causes imbalance of renal renin angiotensin system (RAS) components and hypertension in obese Zucker rats. J. Am. Heart Assoc., 4(2), 2015.
9. [9] Sukhanov, S., Semprun-Prieto, L., Yoshida, T., Michael Tabony, A., Higashi, Y., Galvez, S., et al. Angiotensin II, oxidative stress and skeletal muscle wasting. Am. J. Med. Sci. 342:2 (2011), 143–147.
10. [10] Cassis, L.A., Police, S.B., Yiannikouris, F., Thatcher, S.E., Local adipose tissue renin-angiotensin system. Curr. Hypertens. Rep. 10:2 (2008), 93–98.
11. [11] Leung, P.S., The physiology of a local renin-angiotensin system in the pancreas. J. Physiol. 580:Pt 1 (2007), 31–37.
12. [12] Hsieh, T.J., Zhang, S.L., Filep, J.G., Tang, S.S., Ingelfinger, J.R., Chan, J.S., High glucose stimulates angiotensinogen gene expression via reactive oxygen species generation in rat kidney proximal tubular cells. Endocrinology 143:8 (2002), 2975–2985.
13. [13] Esser, N., Legrand-Poels, S., Piette, J., Scheen, A.J., Paquot, N., Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract. 105:2 (2014), 141–150.
14. [14] Youn, J.Y., Siu, K.L., Lob, H.E., Itani, H., Harrison, D.G., Cai, H., Role of vascular oxidative stress in obesity and metabolic syndrome. Diabetes 63:7 (2014), 2344–2355.
15. [15] Kelly, A.S., Ryder, J.R., Marlatt, K.L., Rudser, K.D., Jenkins, T., Inge, T.H., Changes in inflammation, oxidative stress and adipokines following bariatric surgery among adolescents with severe obesity. Int. J. Obes. 40:2 (2016), 275–280.
16. [16] Keaney, J.F. Jr., Larson, M.G., Vasan, R.S., Wilson, P.W., Lipinska, I., Corey, D., et al. Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham study. Arterioscler. Thromb. Vasc. Biol. 23:3 (2003), 434–439.
17. [17] Sowers, J.R., Hypertension, angiotensin II, and oxidative stress. N. Engl. J. Med. 346:25 (2002), 1999–2001.
18. [18] Kalupahana, N.S., Moustaid-Moussa, N., The adipose tissue renin-angiotensin system and metabolic disorders: a review of molecular mechanisms. Crit. Rev. Biochem. Mol. Biol. 47:4 (2012), 379–390.
19. [19] Yvan-Charvet, L., Quignard-Boulangé, A., Role of adipose tissue renin-angiotensin system in metabolic and inflammatory diseases associated with obesity. Kidney Int. 79:2 (2011), 162–168.
20. [20] Higuchi, S., Ohtsu, H., Suzuki, H., Shirai, H., Frank, G.D., Eguchi, S., Angiotensin II signal transduction through the AT1 receptor: novel insights into mechanisms and pathophysiology. Clin. Sci. 112:7–8 (2007), 417–428.
21. [21] Lemarié, C.A., Schiffrin, E.L., The angiotensin II type 2 receptor in cardiovascular disease. J. Renin Angiotensin Aldosterone Syst. 11:1 (2010), 19–31.
22. [22] Frigolet, M.E., Torres, N., Tovar, A.R., The renin-angiotensin system in adipose tissue and its metabolic consequences during obesity. J. Nutr. Biochem. 24:12 (2013), 2003–2015.
23. [23] Schling, P., Mallow, H., Trindl, A., Loffler, G., Evidence for a local renin angiotensin system in primary cultured human preadipocytes. Int. J. Obes. Relat. Metab. Disord. 23:4 (1999), 336–341.
24. [24] Leung, P.S., de Gasparo, M., Involvement of the pancreatic renin-angiotensin system in insulin resistance and the metabolic syndrome. J. Cardiometab. Syndr. 1:3 (2006), 197–203.
25. [25] Jones, B.H., Standridge, M.K., Taylor, J.W., Moustaid, N., Angiotensinogen gene expression in adipose tissue: analysis of obese models and hormonal and nutritional control. Am. J. Phys. 273:1 Pt 2 (1997), R236–R242.
26. [26] Jones, B.H., Standridge, M.K., Moustaid, N., Angiotensin II increases lipogenesis in 3 T3-L1 and human adipose cells. Endocrinology 138:4 (1997), 1512–1519.
27. [27] Kalupahana, N.S., Massiera, F., Quignard-Boulange, A., Ailhaud, G., Voy, B.H., Wasserman, D.H., et al. Overproduction of angiotensinogen from adipose tissue induces adipose inflammation, glucose intolerance, and insulin resistance. Obesity 20:1 (2012), 48–56.
28. [28] Feraco, A., Armani, A., Mammi, C., Fabbri, A., Rosano, G.M.C., Caprio, M., Role of mineralocorticoid receptor and renin–angiotensin–aldosterone system in adipocyte dysfunction and obesity. J. Steroid Biochem. Mol. Biol. 137:0 (2013), 99–106.
29. [29] Kim, S., Soltani-Bejnood, M., Quignard-Boulange, A., Massiera, F., Teboul, M., Ailhaud, G., et al. The adipose renin-angiotensin system modulates systemic markers of insulin sensitivity and activates the Intrarenal renin-angiotensin system. J. Biomed. Biotechnol., 2006, 2006.
30. [30] Ailhaud, G., Fukamizu, A., Massiera, F., Negrel, R., Saint-Marc, P., Teboul, M., Angiotensinogen, angiotensin II and adipose tissue development. Int. J. Obes. Relat. Metab. Disord. 24:Suppl. 4 (2000), S33–S35.
31. [31] Maeda, A., Tamura, K., Wakui, H., Ohsawa, M., Azushima, K., Uneda, K., et al. Effects of the angiotensin receptor blocker olmesartan on adipocyte hypertrophy and function in mice with metabolic disorders. BioMed Res. Int., 2014, 2014, 10.
32. [32] Goossens, G.H., Moors, C.C.M., van der Zijl, N.J., Venteclef, N., Alili, R., Jocken, J.W.E., et al. Valsartan improves adipose tissue function in humans with impaired glucose metabolism: a randomized placebo-controlled double-blind trial. PLoS One, 7(6), 2012, e39930.
33. [33] Çelebi Bitkin, E., Boyraz, M., Taşkın, N., Akçay, A., Ulucan, K., Akyol, M.B., et al. Effects of ACE inhibitors on insulin resistance and lipid profile in children with metabolic syndrome. J. Clin. Res. Pediatr. Endocrinol. 5:3 (2013), 164–169.
34. [34] Yang, Y., Wei, R.-b., Wang, Z.-c., Wang, N., Gao, Y.-w., Li, M.-x., et al. A meta-analysis of the effects of angiotensin converting enzyme inhibitors and angiotensin II receptor blockers on insulin sensitivity in hypertensive patients without diabetes. Diabetes Res. Clin. Pract. 107:3 (2015), 415–423.
35. [35] Rahmouni, K., Mark, A.L., Haynes, W.G., Sigmund, C.D., Adipose depot-specific modulation of angiotensinogen gene expression in diet-induced obesity. Am. J. Physiol. Endocrinol. Metab. 286:6 (2004), E891–E895.
36. [36] LeMieux, M.J., Ramalingam, L., Mynatt, R.L., Kalupahana, N.S., Kim, J.H., Moustaid-Moussa, N., Inactivation of adipose angiotensinogen reduces adipose tissue macrophages and increases metabolic activity. Obesity 24:2 (2016), 359–367.
37. [37] Carroll, W.X., Kalupahana, N.S., Booker, S.L., Siriwardhana, N., Lemieux, M., Saxton, A.M., et al. Angiotensinogen gene silencing reduces markers of lipid accumulation and inflammation in cultured adipocytes. Front. Endocrinol. 4 (2013), 1–12.
38. [38] Fletcher, S.J., Kalupahana, N.S., Soltani-Bejnood, M., Kim, J.H., Saxton, A.M., Wasserman, D.H., et al. Transgenic mice overexpressing renin exhibit glucose intolerance and diet-genotype interactions. Front. Endocrinol., 3, 2012, 166.
39. [39] Manucha, W., Ritchie, B., Ferder, L., Hypertension and insulin resistance: implications of mitochondrial dysfunction. Curr. Hypertens. Rep. 17:1 (2014), 1–7.
40. [40] Ray, P.D., Huang, B.W., Tsuji, Y., Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24:5 (2012), 981–990.
41. [41] Zablocki, D., Sadoshima, J., Angiotensin II and oxidative stress in the failing heart. Antioxid. Redox Signal. 19:10 (2013), 1095–1109.
42. [42] Doughan, A.K., Harrison, D.G., Dikalov, S.I., Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 102:4 (2008), 488–496.
43. [43] Wei, Y., Sowers, J., Nistala, R., Gong, H., Uptergrove, G., Clark, S., et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J. Biol. Chem. 281 (2006), 35137–35146.
44. [44] Rincón, J., Correia, D., Arcaya, J.L., Finol, E., Fernández, A., Pérez, M., et al. Role of angiotensin II type 1 receptor on renal NAD(P)H oxidase, oxidative stress and inflammation in nitric oxide inhibition induced-hypertension. Life Sci. 124:0 (2015), 81–90.
45. [45] Abadir, P.M., Foster, D.B., Crow, M., Cooke, C.A., Rucker, J.J., Jain, A., et al. Identification and characterization of a functional mitochondrial angiotensin system. Proc. Natl. Acad. Sci. U. S. A. 108:36 (2011), 14849–14854.
46. [46] de Cavanagh, E.M., Ferder, M., Inserra, F., Ferder, L., Angiotensin II, Mitochondria, Cytoskeletal, and Extracellular Matrix Connections: An Integrating Viewpoint. 2009, H550–H558.
47. [47] de Cavanagh, E.M.V., Inserra, F., Ferder, M., Ferder, L., From mitochondria to disease: role of the renin-angiotensin system. Am. J. Nephrol. 27:6 (2007), 545–553.
48. [48] Ricci, C., Pastukh, V., Schaffer, S.W., Involvement of the mitochondrial permeability transition pore in angiotensin II-mediated apoptosis. Exp. Clin. Cardiol. 10:3 (2005), 160–164.
49. [49] Dikalov, S.I., Nazarewicz, R.R., Angiotensin II-induced production of mitochondrial reactive oxygen species: potential mechanisms and relevance for cardiovascular disease. Antioxid. Redox Signal. 19:10 (2013), 1085–1094.
50. [50] Zhang, G.X., Lu, X.M., Kimura, S., Nishiyama, A., Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation. Cardiovasc. Res. 76:2 (2007), 204–212.
51. [51] Griendling, K.K., Sorescu, D., Ushio-Fukai, M., NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86:5 (2000), 494–501.
52. [52] Touyz, R.M., Chen, X., Tabet, F., Yao, G., He, G., Quinn, M.T., et al. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ. Res. 90:11 (2002), 1205–1213.
53. [53] Hingtgen, S.D., Tian, X., Yang, J., Dunlay, S.M., Peek, A.S., Wu, Y., et al. Nox2-containing NADPH oxidase and Akt activation play a key role in angiotensin II-induced cardiomyocyte hypertrophy. Physiol. Genomics 26:3 (2006), 180–191.
54. [54] Valente, A.J., Yoshida, T., Murthy, S.N., Sakamuri, S.S., Katsuyama, M., Clark, R.A., et al. Angiotensin II enhances AT1-Nox1 binding and stimulates arterial smooth muscle cell migration and proliferation through AT1, Nox1, and interleukin-18. Am. J. Physiol. Heart Circ. Physiol. 303:3 (2012), H282–H296.
55. [55] Seshiah, P.N., Weber, D.S., Rocic, P., Valppu, L., Taniyama, Y., Griendling, K.K., Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ. Res. 91:5 (2002), 406–413.
56. [56] Lavoie, J.L., Sigmund, C.D., Minireview: overview of the renin-angiotensin system–an endocrine and paracrine system. Endocrinology 144:6 (2003), 2179–2183.
57. [57] Dikalov, S.I., Nazarewicz, R.R., Bikineyeva, A., Hilenski, L., Lassegue, B., Griendling, K.K., et al. Nox2-induced production of mitochondrial superoxide in angiotensin II-mediated endothelial oxidative stress and hypertension. Antioxid. Redox Signal. 20:2 (2014), 281–294.
58. [58] Inagami, T., Mitochondrial angiotensin receptors and aging. Circ. Res. 109:12 (2011), 1323–1324.
59. [59] Hernandez, J.S., Barreto-Torres, G., Kuznetsov, A.V., Khuchua, Z., Javadov, S., Crosstalk between AMPK activation and angiotensin II-induced hypertrophy in cardiomyocytes: the role of mitochondria. J. Cell. Mol. Med. 18:4 (2014), 709–720.
60. [60] Khaper, N., Singal, P.K., Modulation of oxidative stress by a selective inhibition of angiotensin II type 1 receptors in MI rats. J. Am. Coll. Cardiol. 37:5 (2001), 1461–1466.
61. [61] Kurokawa, H., Sugiyama, S., Nozaki, T., Sugamura, K., Toyama, K., Matsubara, J., et al. Telmisartan enhances mitochondrial activity and alters cellular functions in human coronary artery endothelial cells via AMP-activated protein kinase pathway. Atherosclerosis 239:2 (2015), 375–385.
62. [62] Vazquez-Medina, J.P., Popovich, I., Thorwald, M.A., Viscarra, J.A., Rodriguez, R., Sonanez-Organis, J.G., et al. Angiotensin receptor-mediated oxidative stress is associated with impaired cardiac redox signaling and mitochondrial function in insulin-resistant rats. Am. J. Physiol. Heart Circ. Physiol. 305:4 (2013), H599–H607.
63. [63] Guarente, L., Sirtuins as potential targets for metabolic syndrome. Nature 444:7121 (2006), 868–874.
64. [64] Lijnen, P.J., van Pelt, J.F., Fagard, R.H., Downregulation of manganese superoxide dismutase by angiotensin II in cardiac fibroblasts of rats: association with oxidative stress in myocardium. Am. J. Hypertens. 23:10 (2010), 1128–1135.
65. [65] Theres, H., Wagner, K.D., Schulz, S., Strube, S., Leiterer, K.P., Romberg, D., et al. Oxygen radical system in chronic infarcted rat heart: the effect of combined beta blockade and ACE inhibition. J. Cardiovasc. Pharmacol. 35:5 (2000), 708–715.
66. [66] Murtaza, I., Wang, H.X., Feng, X., Alenina, N., Bader, M., Prabhakar, B.S., et al. Down-regulation of catalase and oxidative modification of protein kinase CK2 lead to the failure of apoptosis repressor with caspase recruitment domain to inhibit cardiomyocyte hypertrophy. J. Biol. Chem. 283:10 (2008), 5996–6004.
67. [67] Lijnen, P.J., Piccart, Y., Coenen, T., Prihadi, J.S., Angiotensin II-induced mitochondrial reactive oxygen species and peroxiredoxin-3 expression in cardiac fibroblasts. J. Hypertens. 30:10 (2012), 1986–1991.
68. [68] Landmesser, U., Spiekermann, S., Preuss, C., Sorrentino, S., Fischer, D., Manes, C., et al. Angiotensin II induces endothelial xanthine oxidase activation: role for endothelial dysfunction in patients with coronary disease. Arterioscler. Thromb. Vasc. Biol. 27:4 (2007), 943–948.
69. [69] Zhao, H., Qi, G., Han, Y., Shen, X., Yao, F., Xuan, C., et al. 20-hydroxyeicosatetraenoic acid is a key mediator of angiotensin II-induced apoptosis in cardiac Myocytes. J. Cardiovasc. Pharmacol. 66:1 (2015), 86–95.
70. [70] Luther, J.M., Brown, N.J., The renin-angiotensin-aldosterone system and glucose homeostasis. Trends Pharmacol. Sci. 32:12 (2011), 734–739.
71. [71] Chhabra, K.H., Xia, H., Pedersen, K.B., Speth, R.C., Lazartigues, E., Pancreatic angiotensin-converting enzyme 2 improves glycemia in angiotensin II-infused mice. Am. J. Physiol. Endocrinol. Metab. 304:8 (2013), E874–E884.
72. [72] Saitoh, Y., Hongwei, W., Ueno, H., Mizuta, M., Nakazato, M., Candesartan attenuates fatty acid-induced oxidative stress and NAD(P)H oxidase activity in pancreatic beta-cells. Diabetes Res. Clin. Pract. 90:1 (2010), 54–59.
73. [73] van der Zijl, N.J., Moors, C.C., Goossens, G.H., Hermans, M.M., Blaak, E.E., Diamant, M., Valsartan improves {beta}-cell function and insulin sensitivity in subjects with impaired glucose metabolism: a randomized controlled trial. Diabetes Care 34:4 (2011), 845–851.
74. [74] Shigihara, N., Uchida, T., Yorifuji, T., Toyofuku, Y., Tamaki, M., Fujitani, Y., et al. Olmesartan and telmisartan comparably preserve pancreatic beta-cell mass with reduction of oxidative stress in db/db mice. Diabetol. Int. 5:1 (2014), 62–68.
75. [75] Chu, K.Y., Leung, P.S., Angiotensin II type 1 receptor antagonism mediates uncoupling protein 2-driven oxidative stress and ameliorates pancreatic islet beta-cell function in young type 2 diabetic mice. Antioxid. Redox Signal. 9:7 (2007), 869–878.
76. [76] He, J., Yang, Z., Yang, H., Wang, L., Wu, H., Fan, Y., et al. Regulation of insulin sensitivity, insulin production, and pancreatic β cell survival by angiotensin-(1-7) in a rat model of streptozotocin-induced diabetes mellitus. Peptides 64:0 (2015), 49–54.
77. [77] Shao, C., Yu, L., Gao, L., Activation of angiotensin type 2 receptors partially ameliorates streptozotocin-induced diabetes in male rats by islet protection. Endocrinology 155:3 (2014), 793–804.
78. [78] Okada, S., Kozuka, C., Masuzaki, H., Yasue, S., Ishii-Yonemoto, T., Tanaka, T., et al. Adipose tissue-specific dysregulation of angiotensinogen by oxidative stress in obesity. Metab. Clin. Exp. 59:9 (2010), 1241–1251.
79. [79] Yanagitani, Y., Rakugi, H., Okamura, A., Moriguchi, K., Takiuchi, S., Ohishi, M., et al. Angiotensin II type 1 receptor-mediated peroxide production in human macrophages. Hypertension 33:1 Pt 2 (1999), 335–339.
80. [80] Kurata, A., Nishizawa, H., Kihara, S., Maeda, N., Sonoda, M., Okada, T., et al. Blockade of angiotensin II type-1 receptor reduces oxidative stress in adipose tissue and ameliorates adipocytokine dysregulation. Kidney Int. 70:10 (2006), 1717–1724.
81. [81] Hirata, A., Maeda, N., Hiuge, A., Hibuse, T., Fujita, K., Okada, T., et al. Blockade of mineralocorticoid receptor reverses adipocyte dysfunction and insulin resistance in obese mice. Cardiovasc. Res. 84:1 (2009), 164–172.
82. [82] Wada, T., Ohshima, S., Fujisawa, E., Koya, D., Tsuneki, H., Sasaoka, T., Aldosterone inhibits insulin-induced glucose uptake by degradation of insulin receptor substrate (IRS) 1 and IRS2 via a reactive oxygen species-mediated pathway in 3 T3-L1 adipocytes. Endocrinology 150:4 (2009), 1662–1669.
83. [83] Inoue, N., Kinugawa, S., Suga, T., Yokota, T., Hirabayashi, K., Kuroda, S., et al. Angiotensin II-induced reduction in exercise capacity is associated with increased oxidative stress in skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 302:5 (2012), H1202–H1210.
84. [84] Lastra, G., Whaley-Connell, A., Manrique, C., Habibi, J., Gutweiler, A.A., Appesh, L., et al. Low-dose spironolactone reduces reactive oxygen species generation and improves insulin-stimulated glucose transport in skeletal muscle in the TG(mRen2)27 rat. Am. J. Physiol. Endocrinol. Metab. 295:1 (2008), E110–E116.
85. [85] Lastra, G., Habibi, J., Whaley-Connell, A.T., Manrique, C., Hayden, M.R., Rehmer, J., et al. Direct renin inhibition improves systemic insulin resistance and skeletal muscle glucose transport in a transgenic rodent model of tissue renin overexpression. Endocrinology 150:6 (2009), 2561–2568.
86. [86] Marchionne, E.M., Diamond-Stanic, M.K., Prasonnarong, M., Henriksen, E.J., Chronic renin inhibition with aliskiren improves glucose tolerance, insulin sensitivity, and skeletal muscle glucose transport activity in obese Zucker rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302:1 (2012), R137–R142.
87. [87] Macconi, D., Perico, L., Longaretti, L., Morigi, M., Cassis, P., Buelli, S., et al. Sirtuin3 dysfunction is the key determinant of skeletal muscle insulin resistance by angiotensin II. PLoS One, 10(5), 2015, e0127172.
88. [88] Kadoguchi, T., Kinugawa, S., Takada, S., Fukushima, A., Furihata, T., Homma, T., et al. Angiotensin II can directly induce mitochondrial dysfunction, decrease oxidative fibre number and induce atrophy in mouse hindlimb skeletal muscle. Exp. Physiol. 100:3 (2015), 312–322.
89. [89] Takada, S., Kinugawa, S., Hirabayashi, K., Suga, T., Yokota, T., Takahashi, M., et al. Angiotensin II Receptor Blocker Improves the Lowered Exercise Capacity and Impaired Mitochondrial Function of the Skeletal Muscle in Type 2 Diabetic Mice. 2013, 844–857.
90. [90] Morel, Y., Gadient, A., Keller, U., Vadas, L., Golay, A., Insulin sensitivity in obese hypertensive dyslipidemic patients treated with enalapril or atenolol. J. Cardiovasc. Pharmacol. 26:2 (1995), 306–311.
91. [91] Fujii, H., Kawada, N., Inflammation and fibrogenesis in steatohepatitis. J. Gastroenterol. 47:3 (2012), 215–225.
92. [92] Wei, Y., Clark, S.E., Morris, E.M., Thyfault, J.P., Uptergrove, G.M., Whaley-Connell, A.T., et al. Angiotensin II-induced non-alcoholic fatty liver disease is mediated by oxidative stress in transgenic TG(mRen2)27(Ren2) rats. J. Hepatol. 49:3 (2008), 417–428.
93. [93] Wei, Y., Clark, S.E., Thyfault, J.P., Uptergrove, G.M., Li, W., Whaley-Connell, A.T., et al. Oxidative stress-mediated mitochondrial dysfunction contributes to angiotensin II-induced nonalcoholic fatty liver disease in transgenic Ren2 rats. Am. J. Pathol. 174:4 (2009), 1329–1337.
94. [94] Qiang, G., Zhang, L., Yang, X., Xuan, Q., Shi, L., Zhang, H., et al. Effect of valsartan on the pathological progression of hepatic fibrosis in rats with type 2 diabetes. Eur. J. Pharmacol. 685:1–3 (2012), 156–164.
95. [95] Moreira de Macedo, S., Guimaraes, T.A., Feltenberger, J.D., Sousa Santos, S.H., The role of renin-angiotensin system modulation on treatment and prevention of liver diseases. Peptides 62 (2014), 189–196.
96. [96] Reza, H.M., Tabassum, N., Sagor, M.A., Chowdhury, M.R., Rahman, M., Jain, P., et al. Angiotensin-converting enzyme inhibitor prevents oxidative stress, inflammation, and fibrosis in carbon tetrachloride-treated rat liver. Toxicol. Mech. Methods 26:1 (2016), 46–53.
97. [97] Sugimoto, K., Qi, N.R., Kazdova, L., Pravenec, M., Ogihara, T., Kurtz, T.W., Telmisartan but not valsartan increases caloric expenditure and protects against weight gain and hepatic steatosis. Hypertension 47:5 (2006), 1003–1009.
98. [98] Kishina, M., Koda, M., Kato, J., Tokunaga, S., Matono, T., Sugihara, T., et al. Therapeutic effects of the direct renin inhibitor, aliskiren, on non-alcoholic steatohepatitis in fatty liver Shionogi ob/ob male mice. Hepatol. Res. 44:8 (2014), 888–896.
99. [99] Colmenero, J., Bataller, R., Sancho-Bru, P., Dominguez, M., Moreno, M., Forns, X., et al. Effects of losartan on hepatic expression of nonphagocytic NADPH oxidase and fibrogenic genes in patients with chronic hepatitis C. Am. J. Physiol. Gastrointest. Liver Physiol. 297:4 (2009), G726–G734.