The role of the renin-angiotensin system in the development of insulin resistance in skeletal muscle

Molecular and Cellular Endocrinology

Volumn 378, Issue 1-2, 2013, Pages 15-22

  Henriksen, Erik J ^a   Prasannarong, Mujalin ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b Mahidol University   (Thailand)

Author keywords

Angiotensin II; Angiotensin (1 7); Glucose transport; Insulin signaling; Oxidative stress

Indexed keywords

ALISKIREN; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONIST; ANGIOTENSIN[1-7]; ANGIOTENSINOGEN; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN; RENIN INHIBITOR; TEMPOL;

DRUG EFFICACY; DRUG TARGETING; ENDOTHELIAL DYSFUNCTION; GLUCOSE TRANSPORT; HUMAN; HYPERTENSION; INSULIN RESISTANCE; INSULIN SENSITIVITY; METABOLIC REGULATION; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANGIOTENSIN II; ANGIOTENSIN-(1-7); GLUCOSE TRANSPORT; INSULIN SIGNALING; OXIDATIVE STRESS;

ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; DIABETES MELLITUS, TYPE 2; GLUCOSE; HUMANS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MUSCLE, SKELETAL; PEPTIDYL-DIPEPTIDASE A; RECEPTOR, ANGIOTENSIN, TYPE 1; RENIN-ANGIOTENSIN SYSTEM;

EID: 84884530768     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.04.011     Document Type: Review

References (103)

1. Aguirre V., Uchida T., Yenush L., Davis R.J., White M.F. The c-Jun NH2-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser307. J. Biol. Chem. 2000, 275:9047-9054.
2. 307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 2002, 277:1531-1537.
3. Anai M., Funaki M., Ogihara T., Terasaki J., Inukai K., Katagiri H., Fukushima Y., Yazaki Y., Kikuchi M., Oka Y., Asano T. Altered expression levels and impaired steps in pathways to phosphatidylinositol-3-kinase activation via insulin receptor substrates 1 and 2 in Zucker fatty rats. Diabetes 1998, 47:13-23.
4. Archuleta T.L., Lemieux A.M., Saengsirisuwan V., Teachey M.K., Lindborg K.A., Kim J.S., Henriksen E.J. Oxidant stress-induced loss of IRS-1 and IRS-2 proteins in rat skeletal muscle: role of p38 MAPK. Free Radic. Biol. Med. 2009, 47:1486-1493.
5. Baron A.D., Brechtel G., Wallace P., Edelman S.V. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am. J. Physiol. Endocrinol. Metab. 1988, 255:E769-E774.
6. Bindom S.M., Hans C.P., Xia H., Boulares A.H., Lazartigues E. Angiotensin I-converting enzyme type 2 (ACE2) gene therapy improves glycemic control in diabetic mice. Diabetes 2010, 59:2540-2548.
7. Blendea M.C., Jacobs D., Stump C.S., McFarlane S.I., Ogrin C., Bahtyiar G., Stas S., Kumar P., Sha Q., Ferrario C.M., et al. Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am. J. Physiol. Endocrinol. Metab. 2005, 288:E353-E359.
8. 632 in the induction of insulin resistance by oxidative stress. Diabetologia 2006, 49:2463-2473.
9. Bosch J., Yusuf S., Gerstein H.C., Pogue J., Sheridan P., Dagenais G., Diaz R., Avezum A., Lanas F., Probstfield J., et al. Effect of ramipril on the incidence of diabetes. N. Engl. J. Med. 2006, 355(2006):1551-1562.
10. Campbell D.J., Rong P., Kladis A., Rees B., Skinner S.L. Angiotensin and bradykinin peptides in the TGR(mREN2)27 rat. Hypertension 1995, 25:1014-1020.
11. Cartee G.D., Wojtaszewski J.F. Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl. Physiol. Nutr. Metabol. 2007, 32:557-566.
12. Cat A.N., Touyz R.M. A new look at the renin-angiotensin system-focusing on the vascular system. Peptides 2011, 32:2141-2150.
13. CDC, Centers for Disease Control and Prevention National, Diabetes Fact Sheet 2011: Available from: <> 2011 (accessed: 15.03.11). http://www.cdc.gov/diabetes/pubs/pdf/ndfs_2011.pdf.
14. Crettaz M., Prentki M., Zaninetti D., Jeanrenaud B. Insulin resistance in soleus muscle from obese Zucker rats: involvement of several defective sites. Biochem. J. 1980, 186:525-534.
15. Dal Ponte D.B., Fogt D.L., Jacob S., Henriksen E.J. Interactions of captopril and verapamil on glucose transport in insulin-resistant rat skeletal muscle. Metabolism 1998, 47:982-987.
16. DeFronzo R.A., Ferrannini E., Hendler R., Felig P., Wahren J. Regulation of splanchnic and peripheral glucose uptake by insulin and hyperglycemia in man. Diabetes 1983, 32:32-45.
17. DeFronzo R.A., Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 1991, 14:173-194.
18. Diamond-Stanic M.K., Henriksen E.J. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch. Physiol. Biochem. 2010, 116:88-95.
19. Diamond-Stanic M.K., Marchionne E.M., Teachey M.K., Durazo D.E., Kim J.S., Henriksen E.J. Critical role of transient p38 MAPK activation in skeletal muscle insulin resistance caused by low-level in vitro oxidant stress. Biochem. Biophys. Res. Commun. 2011, 405:439-444.
20. Dietze G.J., Henriksen E.J. Angiotensin I-converting enzyme in skeletal muscle: sentinel of blood pressure control and glucose homeostasis. J. Renin Angiotensin Aldosterone Syst. 2008, 9:75-88.
21. Donoghue M., Hsieh F., Baronas E., Godbout K., Gosselin M., Stagliano N., Donovan M., Woolf B., Robison K., Jeyaseelan R., Breitbart R.E., Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ. Res. 2000, 87:e1-e9.
22. Dokken B.B., Saengsirisuwan V., Kim J.S., Teachey M.K., Henriksen E.J. Oxidative stress-induced insulin resistance in rat skeletal muscle: role of glycogen synthase kinase-3. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E615-E621.
23. Dzau V.J., Bernstein K., Celermajer D., Cohen J., Dahlof B., Deanfield J., et al. The relevance of tissue angiotensin-converting enzyme: manifestations in mechanistic and endpoint data. Am. J. Cardiol. 2001, 88:1L-20L.
24. Erdös E. Angiotensin I converting enzyme. Circ. Res. 1975, 36:247-255.
25. Etgen G.J., Wilson C.M., Jensen J., Cushman S.W., Ivy J.L. Glucose transport and cell surface GLUT-4 protein in skeletal muscle of the obese Zucker rat. Am. J. Physiol. Endocrinol. Metab. 1996, 271:E294-E301.
26. Ferreira A.J., Santos R.A.S., Bradford C.N., Mecca A.P., Sumners C., Katovich M.J., Raizada M.K. Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases. Hypertension 2010, 55:207-213.
27. Folli F., Kahn C.R., Hansen H., Bouchie J.L., Feener E.P. Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J. Clin. Invest. 1997, 100:2158-2169.
28. Gao J., Ren J., Gulve E.A., Holloszy J.O. Additive effect of contractions and insulin on GLUT-4 translocation into the sarcolemma. J. Appl. Physiol. 1994, 77:1587-1601.
29. Giani J.F., Mayer M.A., Muñoz M.C., Silberman E.A., Höcht C., Taira C.A., Gironacci M.M., Turyn D., Dominici F.P. Chronic infusion of angiotensin-(1-7) improves insulin resistance and hypertension induced by a high-fructose diet in rats. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E262-E271.
30. Gress T.W., Nieto F.J., Shahar E., Wofford M.R., Brancati F.L. Hypertension and antihypertensive therapy as risk factors for type 2 diabetes mellitus. Atherosclerosis Risk in Communities Study. N. Engl. J. Med. 2000, 342:905-912.
31. Guma A., Zierath J.R., Wallberg-Henriksson H., Klip A. Insulin induces translocation of GLUT-4 glucose transporters in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 1995, 268:E613-E622.
32. Habibi J., Whaley-Connell A., Hayden M.R., DeMarco V.G., Schneider R., Sowers S.D., Karuparthi P., Ferrario C.M., Sowers J.R. Renin inhibition attenuates insulin resistance, oxidative stress, and pancreatic remodeling in the transgenic Ren2 rat. Endocrinology 2008, 149:5643-5653.
33. Hansson L., Lindholm L.H., Niskanen L., Lanke J., Hedner T., Niklason A., Luomanmaki K., Dahlof B., de Faire U., Morlin C., Karlberg B.E., Wester P.O., Bjorck J.E. Effect of angiotensin-converting-enzyme inhibition compared with conventional therapy on cardiovascular morbidity and mortality in hypertension: the Captopril Prevention Project (CAPPP) randomised trial. Lancet 1999, 353:611-616.
34. Hayden M.R., Stump C.S., Sowers J.R. Introduction: organ involvement in the cardiometabolic syndrome. J. Cardiometab. Syndr. 2006, 1:16-24.
35. Henriksen E.J., Jacob S. Effects of captopril on glucose transport activity in skeletal muscle of obese Zucker rats. Metabolism 1995, 44:267-272.
36. Henriksen E.J., Jacob S., Fogt D.L., Dietze G.J. Effect of chronic bradykinin administration on insulin action in an animal model of insulin resistance. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 1998, 275:R40-R45.
37. Henriksen E.J., Jacob S., Kinnick T.R., Youngblood E.B., Schmit M.B., Dietze G.J. ACE inhibition and glucose transport in insulin-resistant muscle: roles of bradykinin and nitric oxide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1999, 277:R332-R336.
38. Henriksen E.J., Jacob S., Kinnick T.R., Teachey M.K., Krekler M. Selective angiotensin II receptor receptor antagonism reduces insulin resistance in obese Zucker rats. Hypertension 2001, 38:884-890.
39. Henriksen E.J. Invited review: effects of acute exercise and exercise training on insulin resistance. J. Appl. Physiol. 2002, 93:788-796.
40. Henriksen E.J., Jacob S. Angiotensin converting enzyme inhibitors and modulation of insulin resistance. Diab. Obes. Metab. 2003, 5:214-222.
41. Henriksen E.J. Improvement of insulin sensitivity by antagonism of the renin-angiotensin system. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R974-R980.
42. Henriksen E.J., Teachey M.K. Short-term in vitro inhibition of glycogen synthase kinase-3 potentiates insulin signaling in skeletal muscle of Zucker Diabetic Fatty rats. Metabolism 2007, 56:931-938.
43. Henriksen E.J. Dysregulation of glycogen synthase kinase-3 and the etiology of insulin resistance and type 2 diabetes. Curr. Diab. Rev. 2010, 6:285-293.
44. Henriksen E.J., Diamond-Stanic M.K., Marchionne E.M. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic. Biol. Med. 2011, 51:993-999.
45. Higashiura K., Ura N., Miyazaki Y., Shimamoto K. Effect of an angiotensin II receptor antagonist, candesartan, on insulin resistance and pressor mechanisms in essential hypertension. J. Human Hypertens. 1999, 13(Suppl. 1):S71-S74.
46. Holness M.J., Sugden M.C. The impact of genetic hypertension on insulin secretion and glucoregulatory control in vivo: studies with the TGR(mRen2)27 transgenic rat. J. Hypertension. 1998, 16:369-376.
47. Ikenoue T., Inoki K., Yang Q., Zhou X., Guan K.L. Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signaling. EMBO J. 2008, 27:1919-1931.
48. Jamerson K.A., Nesbitt S.D., Amerena J.V., Grant E., Julius S. Angiotensin mediates forearm glucose uptake by hemodynamic rather than direct effects. Hypertension 1996, 27:854-858.
49. Jones A., Woods D.R. Skeletal muscle RAS and exercise performance. Int. J. Biochem. Cell Biol. 2003, 35:855-866.
50. King P.A., Horton E.D., Hirshman M.F., Horton E.S. Insulin resistance in obese Zucker rat (fa/fa) is associated with a failure of glucose transporter translocation. J. Clin. Invest. 1992, 90:1568-1575.
51. Kinnick T.R., Youngblood E.B., O'Keefe M.P., Saengsirisuwan V., Teachey M.K., Henriksen E.J. Modulation of insulin resistance and hypertension by voluntary exercise training in the TG(mREN2)27 rat. J. Appl. Physiol. 2002, 93:805-813.
52. Kjeldsen S.E., Dahlof B., Devereux R.B., Julius S., Aurup P., Edelman J., Beevers G., de Faire U., Fyhrquist F., Ibsen H., et al. Effects of losartan on cardiovascular morbidity and mortality in patients with isolated systolic hypertension and left ventricular hypertrophy: a Losartan Intervention for Endpoint Reduction (LIFE) substudy. JAMA 2002, 288:1491-1498.
53. Kleiman E., Carter G., Ghansah T., Patel N.A., Cooper D.R. Developmentally spliced PKCbetaII provides a possible link between mTORC2 and Akt kinase to regulate 3T3-L1 adipocyte insulin-stimulated glucose transport. Biochem. Biophys. Res. Commun. 2009, 388:554-559.
54. Langheinrich M., Lee M.A., Bohm M., Pinto Y.M., Ganten D., Paul M. The hypertensive Ren-2 transgenic rat TGR(mREN2)27 in hypertension research: characteristics and functional aspects. Am. J. Hypertens. 1996, 9:506-512.
55. Lastra G., Habibi J., Whaley-Connell A.T., Manrique C., Hayden M.R., Rehmer J., Patel K., Ferrario C., Sowers J.R. Direct renin inhibition improves systemic insulin resistance and skeletal muscle glucose transport in a transgenic rodent model of tissue renin overexpression. Endocrinology 2009, 150:2561-2568.
56. Lee M.A., Bohm M., Kim S., Bachmann S., Bachmann J., Bader M., Ganten D. Differential gene expression of rennin and angiotensinogen in the TGR(mREN2)27 transgenic rat. Hypertension 1995, 25:570-580.
57. Lee M.A., Bohm M., Paul M., Bader M., Ganten U., Ganten D. Physiological characterization of the hypertensive transgenic rat TGR(mREN2)27. Am. J. Physiol. Endocrinol. Metab. 1996, 270:E919-E929.
58. Lemieux A.M., Diehl C.J., Sloniger J.A., Henriksen E.J. Voluntary exercise training enhances glucose transport but not insulin signaling capacity in muscle of hypertensive TG(mREN2)27 rats. J. Appl. Physiol. 2005, 99:357-362.
59. Lender D., Arauz-Pacheco C., Breen L., Mora-Mora P., Ramirez L.C., Raskin P. A double blind comparison of the effects of amlopidine and enalapril on insulin sensitivity in hypertensive patients. Am. J. Hypertens. 1999, 12:298-303.
60. Lund S., Holman G.D., Schmitz O., Pedersen O. Glut 4 content in the plasma membrane of rat skeletal muscle: comparative studies of the subcellular fractionation method and the exofacial photolabelling technique using ATB-BMPA. FEBS Lett. 1993, 330:312-318.
61. Marchionne E.M., Diamond-Stanic M.K., Prasannarong M., Henriksen E.J. Chronic renin inhibition using aliskiren improves glucose tolerance, insulin sensitivity, and skeletal muscle glucose transport activity in obese Zucker rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302:R137-R142.
62. Mathe D. Dyslipidemia and diabetes: animal models. Diab. Metabol. 1995, 21:106-111.
63. Metzger R., Bader M., Ludwig T., Berberich C., Bunnemann B., Ganten D. Expression of the mouse and rat mas proto-oncogene in the brain and peripheral tissues. FEBS Lett. 1995, 357:27-32.
64. 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. 1995, 26:306-311.
65. Mullins J.J., Peters J., Ganten D. Fulminant hypertension in transgenic rats harboring the Ren-2 gene. Nature 1990, 344:541-544.
66. Muñoz M.C., Giani J.F., Dominici F.P. Angiotensin-(1-7) stimulates the phosphorylation of Akt in rat extracardiac tissues in vivo via receptor Mas. Regul. Pept. 2010, 161:1-7.
67. NIDDK, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health: National Diabetes Information Clearinghouse. Reference available from: <> 2011 (accessed 15.03.11). http://diabetes.niddk.nih.gov/dm/pubs/statistics/#fast.
68. Nistala, Stump C.S. Skeletal muscle insulin resistance is fundamental to the cardiometabolic syndrome. J. Cardiometab. Syndr. 2006, 1:47-52.
69. Paolisso G., Gambardella A., Verza M., D'Amore A., Sgambato S., Varricchio M. ACE inhibition improves insulin-sensitivity in aged insulin-resistant hypertensive patients. J. Hum. Hypertens. 1992, 6:175-179.
70. Piedrola G., Novo E., Serrano-Gotarredona J., de Teresa M.L., Garcia-Robles R. Evolution of insulin resistance in coronary artery disease patients on four different pharmacological therapies. Postgrad. Med. J. 1999, 75:27-31.
71. Pollare T., Lithell H., Berne C. A comparison of the effects of hydrochlorothiazide and captopril on glucose and lipid metabolism in patients with hypertension. N. Engl. J. Med. 1989, 321:868-873.
72. Potashnik R., Bloch-Damti A., Bashan N. IRS1 degradation and increased serine phosphorylation cannot predict the degree of metabolic insulin resistance induced by oxidative stress. Diabetologia 2003, 46:639-648.
73. Probst W.C., Snyder L.A., Schuster D.I., Brosius J., Sealfon S.C. Sequence alignment of the G-protein coupled receptor superfamily. DNA Cell Biol. 1992, 11:1-20.
74. Reaven G.M. Pathophysiology of insulin resistance in human disease. Physiol. Rev. 1995, 75:473-486.
75. Richey J.M., Ader M., Moore D., Bergman R.N. Angiotensin II induces insulin resistance independent of changes in interstitial insulin. Am. J. Physiol. Endocrinol. Metab. 1999, 277:E920-E926.
76. Saengsirisuwan V., Perez F.R., Sloniger J.A., Maier T., Henriksen E.J. Interactions of exercise training and R-(+)-alpha-lipoic acid on insulin signaling in skeletal muscle of obese Zucker rats. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E529-E536.
77. Sampaio W.O., Souza dos Santos R.A., Faria-Silva R., da Mata Machado L.T., Schiffrin E.L., Touyz R.M. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt dependent pathways. Hypertension 2007, 49:185-192.
78. Sander M., Baden M., Djavidani B., Maser-Gluth C., Vecsei P., Mullins J. The role of the adrenal gland in hypertensive transgenic rat TGR(mREN2)27. Endocrinology 1992, 131:807-814.
79. Sano H., Kane S., Sano E., Miinea C.P., Asara J.M., Lane W.S., Garner C.W., Lienhard G.E. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 2003, 278:14599-14602.
80. Santos R.A.S., Silva A.C.S., Maric C., Silva D.M.R., Machado R.P., de Buhr I., Heringer-Walther S., Pinheiro S.V., Lopes M.T., Bader M., Mendes E.P., Lemos V.S., Campagnole-Santos M.J., Schultheiss H.P., Speth R., Walther T. Angiotensin-(1-7) is an endogenous ligand for the G protein coupled receptor Mas. Proc. Natl. Acad. Sci. USA 2003, 100:8258-8263.
81. Santos R.A., Ferreira A.J., Simões A.C., Silva E. Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis. Exp. Physiol. 2008, 93:519-527.
82. Shamiss A., Carroll J., Peleg E., Grossman E., Rosenthal T. The effect of enalapril with and without hydrochlorothiazide on insulin sensitivity and other metabolic abnormalities of hypertensive patients with NIDDM. Am. J. Hypertens. 1995, 8:276-281.
83. Shepherd P.R., Kahn B.B. Glucose transporters and insulin action-implications for insulin resistance and diabetes mellitus. N. Engl. J. Med. 1999, 341:248-257.
84. Shieh S.M., Sheu W.H.H., Shen D.D.C., Fuh M.M., Jeng C.Y., Jeng J.R., Chen Y.D., Reaven G.M. Improvements in metabolic risk factors for coronary heart disease associated with cilazapril treatment. Am. J. Hypertens. 1992, 5:506-510.
85. Shulman G.I. Cellular mechanisms of insulin resistance. J. Clin. Invest. 2000, 106:171-176.
86. Sloniger J.A., Saengsirisuwan V., Diehl C.J., Dokken B.B., Lailerd N., Lemieux A.M. J. S. Kim, E. J. Henriksen. Defective insulin signaling in skeletal muscle of the hypertensive TG(mREN2)27 rat. Am. J. Physiol. Endocrinol. Metab. 2005, 288:E1074-E1081.
87. Sloniger J.A., Saengsirisuwan V., Diehl C.J., Kim J.S., Henriksen E.J. Selective angiotensin II receptor antagonism enhances whole-body insulin sensitivity and muscle glucose transport in hypertensive TG(mREN2)27 rats. Metabolism 2005, 54:1659-1668.
88. Steen M.S., Foianini K.R., Youngblood E.B., Kinnick T.R., Jacob S., Henriksen E.J. Interactions of exercise training and ACE inhibition on insulin action in obese Zucker rats. J. Appl. Physiol. 1999, 86:2044-2051.
89. Suzuki M., Ikebuchi M., Yokota C., Shinozaki K., Harano Y. Normalization of insulin resistance in non-obese essential hypertension by cilazapril treatment. Clin. Exp. Hypertens. 1995, 17:1257-1268.
90. Taniguchi C.M., Brice Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell. Biol. 2006, 7:85-96.
91. Tipnis S.R., Hooper N.M., Hyde R., Karran E., Christie G., Turner A.J. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J. Biol. Chem. 2000, 275:33238-33243.
92. Uehara M., Kishikawa H., Isami S., Kisanuki K., Ohkubo Y., Miyamura N., Miyata T., Yano T., Shichiri M. Effect on insulin sensitivity of angiotensin converting enzyme inhibitors with or without a sulphydryl group: Bradykinin may improve insulin resistance in dogs and humans. Diabetologia 1994, 37:300-307.
93. Villar A.J., Pedersen R.A. Parental imprinting of the Mas protooncogene in mouse. Nat. Genet. 1994, 8:373-379.
94. Van den Meiracker A.H., Jan Danser A.H. Aliskiren: the first direct renin inhibitor for hypertension. Curr. Cardiol. Rep. 2007, 9:470-476.
95. Vicaut E., Hou X. Arteriolar constriction and local renin-angiotensin system in rat microcirculation. Hypertension 1993, 21:491-497.
96. Vuirinen-Makkola H., Yki-Järvinen H. Antihypertensive therapy with enalapril improves glucose storage and insulin sensitivity in hypertensive patients with non-insulin-dependent diabetes mellitus. Metabolism 1995, 44:85-89.
97. Wei Y., Sowers J.R., Nistala R., Gong H., Uptergrove G.M., Clark S.E., Morris E.M., Szary N., Manrique C., Stump C.S. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J. Biol. Chem. 2006, 281:35137-35146.
98. Wei Y., Whaley-Connell A.T., Chen K., Habibi J., Uptergrove G.M., Clark S.E., Stump C.S., Ferrario C.M., Sowers J.R. NADPH oxidase contributes to vascular inflammation, insulin resistance, and remodeling in the transgenic (mRen2) rat. Hypertension 2007, 50:384-391.
99. Wood J.M., Schnell C.R., Cumin F., Menard J., Webb R.L. Aliskiren, a novel, orally effective renin inhibitor, lowers blood pressure in marmosets and spontaneously hypertensive rats. J. Hypertens. 2005, 23:417-426.
100. Xu P., Sriramula S., Lazartigues E. ACE2/ANG-(1-7)/Mas pathway in the brain: the axis of good. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R804-R817.
101. Yu C., Chen Y., Cline G.W., Zhang D., Zong H., Wang Y., Bergeron R., Kim J.K., Cushman S.W., Cooney G.J., Atcheson B., White M.F., Kraegen E.W., Shulman G.I. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 2002, 277:50230-50236.
102. Yusuf S., Sleight P., Pogue J., Bosch J., Davies R., Dagenais G. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 2000, 342:145-153.
103. Zierath J.R., Krook A., Wallberg-Henriksson H. Insulin action and insulin resistance in human skeletal muscle. Diabetologia 2000, 43:821-835.