Insulin decreases atherosclerosis by inducing endothelin receptor B expression

JCI Insight

Volumn 1, Issue 6, 2016, Pages

  Park, Kyoungmin ^a   Mima, Akira ^a   Li, Qian ^a   Rask Madsen, Christian ^a   He, Pingnian ^b   Mizutani, Koji ^a   Katagiri, Sayaka ^a   Maeda, Yasutaka ^a   Wu, I Hsien ^a   Khamaisi, Mogher ^a   Preil, Simone Rordam ^c   Maddaloni, Ernesto ^a   Sørensen, Ditte ^a,c,d   Rasmussen, Lars Melholt ^c   Huang, Paul L ^a   King, George L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d DANISH DIABETES ACADEMY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85013277733     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.86574     Document Type: Article

References (45)

1. Bornfeldt KE, Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab. 2011; 14(5):575-585.
2. Rask-Madsen C, King GL. Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab. 2013; 17(1):20-33.
3. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. J Clin Invest. 1996; 97(11):2601-2610.
4. Rask-Madsen C, et al. Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice. Cell Metab. 2010; 11(5):379-389.
5. Tsuchiya K, et al. FoxOs integrate pleiotropic actions of insulin in vascular endothelium to protect mice from atherosclerosis. Cell Metab. 2012; 15(3):372-381.
6. Fernandez-Hernando C, et al. Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 2007; 6(6):446-457.
7. Jiang ZY, et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest. 1999; 104(4):447-457.
8. Fulton D, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 1999; 399(6736):597-601.
9. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999; 399(6736):601-605.
10. Zeng G, Quon MJ. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. J Clin Invest. 1996; 98(4):894-898.
11. Zeng G, et al. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation. 2000; 101(13):1539-1545.
12. Kuhlencordt PJ, et al. Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/ endothelial nitric oxide synthase double-knockout mice. Circulation. 2001; 104(4):448-454.
13. Despres JP, et al. Hyperinsulinemia as an independent risk factor for ischemic heart disease. N Engl J Med. 1996; 334(15):952-957.
14. Pyorala K. Relationship of glucose tolerance and plasma insulin to the incidence of coronary heart disease: results from two population studies in Finland. Diabetes Care. 1979; 2(2):131-141.
15. Kuboki K, et al. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation. 2000; 101(6):676-681.
16. Naruse K, et al. Activation of vascular protein kinase C-β inhibits Akt-dependent endothelial nitric oxide synthase function in obesity-associated insulin resistance. Diabetes. 2006; 55(3):691-698.
17. Rask-Madsen C, et al. Hyperinsulinemia does not change atherosclerosis development in apolipoprotein E null mice. Arterioscler Thromb Vasc Biol. 2012; 32(5):1124-1131.
18. Ozaki M, et al. Overexpression of endothelial nitric oxide synthase accelerates atherosclerotic lesion formation in apoE-deficient mice. J Clin Invest. 2002; 110(3):331-340.
19. Cybulsky MI, et al. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001; 107(10):1255-1262.
20. Ley K, Huo Y. VCAM-1 is critical in atherosclerosis. J Clin Invest. 2001; 107(10):1209-1210.
21. Cybulsky MI, Gimbrone MA Jr. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science. 1991; 251(4995):788-791.
22. Khan BV, Parthasarathy SS, Alexander RW, Medford RM. Modified low density lipoprotein and its constituents augment cytokine-activated vascular cell adhesion molecule-1 gene expression in human vascular endothelial cells. J Clin Invest. 1995; 95(3):1262-1270.
23. Eguchi S, Hirata Y, Imai T, Marumo F. Endothelin-1 as an autocrine growth factor for endothelial cells. J Cardiovasc Pharmacol. 1995; 26(suppl 3):S279-S283.
24. Dagassan PH, et al. Up-regulation of endothelin-B receptors in atherosclerotic human coronary arteries. J Cardiovasc Pharmacol. 1996; 27(1):147-153.
25. D'Orleans-Juste P, Labonte J, Bkaily G, Choufani S, Plante M, Honore JC. Function of the endothelin(B) receptor in cardiovascular physiology and pathophysiology. Pharmacol Ther. 2002; 95(3):221-238.
26. Park JY, et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes. 2000; 49(7):1239-1248.
27. Jiang ZY, et al. Endothelin-1 modulates insulin signaling through phosphatidylinositol 3-kinase pathway in vascular smooth muscle cells. Diabetes. 1999; 48(5):1120-1130.
28. Ishikawa K, et al. Biochemical and pharmacological profile of a potent and selective endothelin B-receptor antagonist, BQ-788. Proc Natl Acad Sci U S A. 1994; 91(11):4892-4896.
29. Chu TS, Peng Y, Cano A, Yanagisawa M, Alpern RJ. Endothelin(B) receptor activates NHE-3 by a Ca2+-dependent pathway in OKP cells. J Clin Invest. 1996; 97(6):1454-1462.
30. Hirata Y, et al. Endothelin receptor subtype B mediates synthesis of nitric oxide by cultured bovine endothelial cells. J Clin Invest. 1993; 91(4):1367-1373.
31. Deliu E, et al. Intracellular endothelin type B receptor-driven Ca2+ signal elicits nitric oxide production in endothelial cells. J Biol Chem. 2012; 287(49):41023-41031.
32. Kashiwagi S, et al. eNOS phosphorylation on serine 1176 affects insulin sensitivity and adiposity. Biochem Biophys Res Commun. 2013; 431(2):284-290.
33. Terasaka N, et al. ATP-binding cassette transporter G1 and high-density lipoprotein promote endothelial NO synthesis through a decrease in the interaction of caveolin-1 and endothelial NO synthase. Arterioscler Thromb Vasc Biol. 2010; 30(11):2219-2225.
34. Kubota T, et al. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab. 2011; 13(3):294-307.
35. Kubota T, et al. Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury. Circulation. 2003; 107(24):3073-3080.
36. Yanagisawa M, Kurihara H, Kimura S, Goto K, Masaki T. A novel peptide vasoconstrictor, endothelin, is produced by vascular endothelium and modulates smooth muscle Ca2+ channels. J Hypertens Suppl. 1988; 6(4):S188-191.
37. Tirapelli CR, et al. Functional characterization and expression of endothelin receptors in rat carotid artery: involvement of nitric oxide, a vasodilator prostanoid and the opening of K+ channels in ETB-induced relaxation. Br J Pharmacol. 2005; 146(6):903-912.
38. Luscher TF, Barton M. Endothelins and endothelin receptor antagonists: therapeutic considerations for a novel class of cardiovascular drugs. Circulation. 2000; 102(19):2434-2440.
39. Ohashi Y, et al. Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. J Clin Invest. 1998; 102(12):2061-2071.
40. Teppala S, Shankar A. Association between serum IGF-1 and diabetes among U. Diabetes Care. 2010; 33(10):2257-2259.
41. Stuart JA, Page MM. Plasma IGF-1 is negatively correlated with body mass in a comparison of 36 mammalian species. Mech Ageing Dev. 2010; 131(9):591-598.
42. Sandhu MS, Heald AH, Gibson JM, Cruickshank JK, Dunger DB, Wareham NJ. Circulating concentrations of insulin-like growth factor-I and development of glucose intolerance: a prospective observational study. Lancet. 2002; 359(9319):1740-1745.
43. Ansar S, et al. MAPK signaling pathway regulates cerebrovascular receptor expression in human cerebral arteries. BMC Neurosci. 2013; 14:12.
44. Li Q, et al. Induction of vascular insulin resistance and endothelin-1 expression and acceleration of atherosclerosis by the overexpression of protein kinase C-beta isoform in the endothelium. Circ Res. 2013; 113(4):418-427.
45. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3(6):1101-1108.