Skeletal muscle insulin resistance in salt-sensitive hypertension: Role of angiotensin II activation of NFκB

Cardiovascular Diabetology

Volumn 14, Issue 1, 2015, Pages

  Zhou, Ming Sheng ^a,b   Liu, Chang ^a   Tian, Runxia ^b   Nishiyama, Akira ^c   Raij, Leopoldo ^b,d  

^a JINZHOU MEDICAL UNIVERSITY   (China)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c KAGAWA UNIVERSITY   (Japan)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin II; Hypertension; Insulin resistance; NF B; Skeletal muscle

Indexed keywords

ANGIOTENSIN II; CANDESARTAN; DIPEPTIDYL CARBOXYPEPTIDASE; GLUCOSE TRANSPORTER 4; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B; PYRROLIDINE DITHIOCARBAMATE; REACTIVE OXYGEN METABOLITE; SN 50; TEMPOL; SALT INTAKE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; GENE; GENE EXPRESSION; GENE TARGETING; GLUCOSE INFUSION; GLUCOSE METABOLISM; HYPERTENSION; INCUBATION TIME; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; DAHL RAT; METABOLISM; PHYSIOLOGY; SALT INTAKE; SPRAGUE DAWLEY RAT; TOXICITY;

ANGIOTENSIN II; ANIMALS; HYPERTENSION; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; NF-KAPPA B; RATS; RATS, INBRED DAHL; RATS, SPRAGUE-DAWLEY; SODIUM CHLORIDE, DIETARY;

EID: 84928808967     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-015-0211-6     Document Type: Article

References (48)

1. Zhou MS, Wang A, Yu H. Link between insulin resistance and hypertension: What is the evidence from evolutionary biology? Diabetol Metab Syndr. 2014;6(1):12.
2. Ferrannini E, Cushman WC. Diabetes and hypertension: the bad companions. Lancet. 2012;380(9841):601-10.
3. Lastra-Lastra G, Sowers JR, Restrepo-Erazo K, Manrique-Acevedo C, Lastra-Gonzalez G. Role of aldosterone and angiotensin II in insulin resistance: an update. Clin Endocrinol (Oxf). 2009;71(1):1-6.
4. Chen J, Gu D, Huang J, Rao DC, Jaquish CE, Hixson JE, et al. Metabolic syndrome and salt sensitivity of blood pressure in non-diabetic people in China: a dietary intervention study. Lancet. 2009;373(9666):829-35.
5. Stolarz-Skrzypek K, Kuznetsova T, Thijs L, Tikhonoff V, Seidlerova J, Richart T, et al. Fatal and nonfatal outcomes, incidence of hypertension, and blood pressure changes in relation to urinary sodium excretion. JAMA. 2011;305(17):1777-85.
6. Lastra G, Dhuper S, Johnson MS, Sowers JR. Salt, aldosterone, and insulin resistance: impact on the cardiovascular system. Nat Rev Cardiol. 2010;7(10):577-84.
7. Zhou MS, Schulman IH, Zeng Q. Link between the renin-angiotensin system and insulin resistance: implications for cardiovascular disease. Vasc Med. 2012;17(5):330-41.
8. Van Gaal LF, Mertens IL, De Block CE. Mechanisms linking obesity with cardiovascular disease. Nature. 2006;444(7121):875-80.
9. Cooper SA, Whaley-Connell A, Habibi J, Wei Y, Lastra G, Manrique C, et al. Renin-angiotensin-aldosterone system and oxidative stress in cardiovascular insulin resistance. Am J Physiol Heart Circ Physiol. 2007;293(4):H2009-23.
10. Holland WL, Bikman BT, Wang LP, Yuguang G, Sargent KM, Bulchand S, et al. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J Clin Invest. 2011;121(5):1858-70.
11. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest. 1994;94(3):1172-9.
12. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP. 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(9):2158-69.
13. Zhou MS, Schulman IH, Raij L. Role of angiotensin II and oxidative stress in vascular insulin resistance linked to hypertension. Am J Physiol Heart Circ Physiol. 2009;296(3):H833-9.
14. Andreozzi F, Laratta E, Sciacqua A, Perticone F, Sesti G. Angiotensin II impairs the insulin signaling pathway promoting production of nitric oxide by inducing phosphorylation of insulin receptor substrate-1 on Ser312 and Ser616 in human umbilical vein endothelial cells. Circ Res. 2004;94(9):1211-8.
15. Zhou MS, Schulman IH, Raij L. Vascular inflammation, insulin resistance, and endothelial dysfunction in salt-sensitive hypertension: role of nuclear factor kappa B activation. J Hypertens. 2010;28(3):527-35.
16. Zhou MS, Hernandez Schulman I, Pagano PJ, Jaimes EA, Raij L. Reduced NAD(P)H oxidase in low renin hypertension: link among angiotensin II, atherogenesis, and blood pressure. Hypertension. 2006;47(1):81-6.
17. Kiechl S, Wittmann J, Giaccari A, Knoflach M, Willeit P, Bozec A, et al. Blockade of receptor activator of nuclear factor-kappaB (RANKL) signaling improves hepatic insulin resistance and prevents development of diabetes mellitus. Nat Med. 2013;19(3):358-63.
18. Reilly SM, Chiang SH, Decker SJ, Chang L, Uhm M, Larsen MJ, et al. An inhibitor of the protein kinases TBK1 and IKK-varepsilon improves obesity-related metabolic dysfunctions in mice. Nat Med. 2013;19(3):313-21.
19. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011;17(2):179-88.
20. Cai D, Yuan M, Frantz DF, Melendez PA, Hansen L, Lee J, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med. 2005;11(2):183-90.
21. Stump CS, Henriksen EJ, Wei Y, Sowers JR. The metabolic syndrome: role of skeletal muscle metabolism. Ann Med. 2006;38(6):389-402.
22. Nishiyama A, Yoshizumi M, Rahman M, Kobori H, Seth DM, Miyatake A, et al. Effects of AT1 receptor blockade on renal injury and mitogen-activated protein activity in Dahl salt-sensitive rats. Kidney Int. 2004;65(3):972-81.
23. Zhou MS, Adam AG, Jaimes EA, Raij L. In salt-sensitive hypertension, increased superoxide production is linked to functional upregulation of angiotensin II. Hypertension. 2003;42(5):945-51.
24. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med. 2005;11(2):191-8.
25. Ghosh S, Hayden MS. New regulators of NF-kappaB in inflammation. Nat Rev Immunol. 2008;8(11):837-48.
26. Underwood PC, Adler GK. The renin angiotensin aldosterone system and insulin resistance in humans. Curr Hypertens Rep. 2013;15(1):59-70.
27. Wei Y, Chen K, Whaley-Connell AT, Stump CS, Ibdah JA, Sowers JR. Skeletal muscle insulin resistance: role of inflammatory cytokines and reactive oxygen species. Am J Physiol Regul Integr Comp Physiol. 2008;294(3):R673-80.
28. Chu KY, Lau T, Carlsson PO, Leung PS. Angiotensin II type 1 receptor blockade improves beta-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes. 2006;55(2):367-74.
29. Liu M, Jing D, Wang Y, Liu Y, Yin S. Overexpression of angiotensin II type 2 receptor promotes apoptosis and impairs insulin secretion in rat insulinoma cells. Mol Cell Biochem. 2015;400(1-2):233-44.
30. Nasser M, Clere N, Botelle L, Javellaud J, Oudart N, Faure S, et al. Opposite effects of angiotensins receptors type 2 and type 4 on streptozotocin induced diabetes vascular alterations in mice. Cardiovasc Diabetol. 2014;13:40.
31. He J, Yang Z, Yang H, Wang L, Wu H, Fan Y, et al. Regulation of insulin sensitivity, insulin production, and pancreatic beta cell survival by angiotensin-(1-7) in a rat model of streptozotocin-induced diabetes mellitus. Peptides. 2015;64C:49-54.
32. Chang CH, Chang YC, Wu LC, Lin JW, Chuang LM, Lai MS. Different angiotensin receptor blockers and incidence of diabetes: a nationwide population-based cohort study. Cardiovasc Diabetol. 2014;13:91.
33. Abuissa H, Jones PG, Marso SP, O'Keefe Jr. JH. Angiotensin-converting enzyme inhibitors or angiotensin receptor blockers for prevention of type 2 diabetes: a meta-analysis of randomized clinical trials. J Am Coll Cardiol. 2005;46(5):821-6.
34. Schupp M, Janke J, Clasen R, Unger T, Kintscher U. Angiotensin type 1 receptor blockers induce peroxisome proliferator-activated receptor-gamma activity. Circulation. 2004;109(17):2054-7.
35. Jones A, Woods DR. Skeletal muscle RAS and exercise performance. Int J Biochem Cell Biol. 2003;35(6):855-66.
36. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, Stump CS. Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab. 2008;294(2):E345-51.
37. Wang N, Chai W, Zhao L, Tao L, Cao W, Liu Z. Losartan increases muscle insulin delivery and rescues insulin's metabolic action during lipid infusion via microvascular recruitment. Am J Physiol Endocrinol Metab. 2013;304(5):E538-45.
38. Pan Y, Qiao QY, Pan LH, Zhou DC, Hu C, Gu HF, et al. Losartan reduces insulin resistance by inhibiting oxidative stress and enhancing insulin signaling transduction. Exp Clin Endocrinol Diabetes. 2015;123(3):170-7.
39. Putnam K, Shoemaker R, Yiannikouris F, Cassis LA. The renin-angiotensin system: a target of and contributor to dyslipidemias, altered glucose homeostasis, and hypertension of the metabolic syndrome. Am J Physiol Heart Circ Physiol. 2012;302(6):H1219-30.
40. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem. 2006;281(46):35137-46.
41. De Boer MP, Meijer RI, Wijnstok NJ, Jonk AM, Houben AJ, Stehouwer CD, et al. Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation. 2012;19(1):5-18.
42. Clark MG. Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am J Physiol Endocrinol Metab. 2008;295(4):E732-50.
43. Bonner JS, Lantier L, Hasenour CM, James FD, Bracy DP, Wasserman DH. Muscle-specific vascular endothelial growth factor deletion induces muscle capillary rarefaction creating muscle insulin resistance. Diabetes. 2013;62(2):572-80.
44. Sriwijitkamol A, Christ-Roberts C, Berria R, Eagan P, Pratipanawatr T, DeFronzo RA, et al. Reduced skeletal muscle inhibitor of kappaB beta content is associated with insulin resistance in subjects with type 2 diabetes: reversal by exercise training. Diabetes. 2006;55(3):760-7.
45. Lu J, Ji J, Meng H, Wang D, Jiang B, Liu L, et al. The protective effect and underlying mechanism of metformin on neointima formation in fructose-induced insulin resistant rats. Cardiovasc Diabetol. 2013;12:58.
46. Ogihara T, Asano T, Katagiri H, Sakoda H, Anai M, Shojima N, et al. Oxidative stress induces insulin resistance by activating the nuclear factor-kappa B pathway and disrupting normal subcellular distribution of phosphatidylinositol 3-kinase. Diabetologia. 2004;47(5):794-805.
47. Jiang Y, Thakran S, Bheemreddy R, Ye EA, He H, Walker RJ, et al. Pioglitazone normalizes insulin signaling in the diabetic rat retina through reduction in tumor necrosis factor alpha and suppressor of cytokine signaling 3. J Biol Chem. 2014;289(38):26395-405.
48. De Filippo G, Rendina D, Moccia F, Rocco V, Campanozzi A. Interleukin-6, soluble interleukin-6 receptor/interleukin-6 complex and insulin resistance in obese children and adolescents. J Endocrinol Invest. 2014; Sep 23. [Epub ahead of print].