ENOS phosphorylation on serine 1176 affects insulin sensitivity and adiposity

Biochemical and Biophysical Research Communications

Volumn 431, Issue 2, 2013, Pages 284-290

  Kashiwagi, Satoshi ^a   Atochin, Dmitriy N ^a   Li, Qian ^a   Schleicher, Michael ^b   Pong, Terrence ^a   Sessa, William C ^b   Huang, Paul L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes; Endothelium; Insulin resistance; Metabolism; Nitric oxide; Obesity

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; SERINE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL REACTIVITY; BODY WEIGHT; ENERGY METABOLISM; GENE MUTATION; HYPERTENSION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ADIPOSITY; ANIMALS; BLOOD PRESSURE; GENE KNOCK-IN TECHNIQUES; GLUCOSE; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MUTATION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; SERINE; VASCULAR RESISTANCE; WEIGHT GAIN;

MUS;

EID: 84873430409     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.110     Document Type: Article

References (47)

1. Alberti K.G., Zimmet P.Z. Definition, diagnosis and classification of diabetes mellitus and its complications. Diabet. Med. 1998, 15:539-553.
2. Huang P.L. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol. Metab. 2009, 20:295-302.
3. Huang P.L. A comprehensive definition for metabolic syndrome. Dis. Models Mech. 2009, 2:231-237.
4. Hink U., Li H., Mollnau H., et al. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ. Res. 2001, 88:E14-E22.
5. Gimbrone M.A., Topper J.N., Nagel T., et al. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann. NY Acad. Sci. 2000, 902:230-239.
6. discussion 239-40.
7. Gimbrone M.A. Endothelial dysfunction and atherosclerosis. J. Card. Surg. 1989, 4:180-183.
8. Dudzinski D.M., Igarashi J., Greif D., et al. The regulation and pharmacology of endothelial nitric oxide synthase. Annu. Rev. Pharmacol. Toxicol. 2006, 46:235-276.
9. Huang P.L., Huang Z., Mashimo H., et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995, 377:239-242.
10. Freedman J.E., Sauter R., Battinelli E.M., et al. Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ. Res. 1999, 84:1416-1421.
11. Kuhlencordt P.J., Gyurko R., Han F., et al. Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation 2001, 104:448-454.
12. Lefer D.J., Jones S.P., Girod W.G., et al. Leukocyte-endothelial cell interactions in nitric oxide synthase-deficient mice. Am. J. Physiol. 1999, 276:H1943-H1950.
13. Moroi M., Zhang L., Yasuda T., et al. Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J. Clin. Invest. 1998, 101:1225-1232.
14. Murohara T., Asahara T., Silver M., et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 1998, 101:2567-2578.
15. Huang P.L. Unraveling the links between diabetes, obesity, and cardiovascular disease. Circ. Res. 2005, 96:1129-1131.
16. Wang Y., Marsden P.A. Nitric oxide synthases: gene structure and regulation. Adv. Pharmacol. 1995, 34:71-90.
17. Bode-Boger S.M., Boger R.H., Kienke S., et al. Elevated L-arginine/dimethylarginine ratio contributes to enhanced systemic NO production by dietary L-arginine in hypercholesterolemic rabbits. Biochem. Biophys. Res. Commun. 1996, 219:598-603.
18. Cooke J.P. Does ADMA cause endothelial dysfunction?. Arterioscler Thromb. Vasc. Biol. 2000, 20:2032-2037.
19. Cosentino F., Patton S., d'Uscio L.V., et al. Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats. J. Clin. Invest. 1998, 101:1530-1537.
20. Shaul P.W. Regulation of endothelial nitric oxide synthase: location, location, location. Annu. Rev. Physiol. 2002, 64:749-774.
21. Dimmeler S., Fleming I., Fisslthaler B., et al. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999, 399:601-605.
22. Fulton D., Gratton J.P., McCabe T.J., et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999, 399:597-601.
23. Chen Z.P., Mitchelhill K.I., Michell B.J., et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999, 443:285-289.
24. Hisamoto K., Ohmichi M., Kurachi H., et al. Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J. Biol. Chem. 2001, 276:3459-3467.
25. Kureishi Y., Luo Z., Shiojima I., et al. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat. Med. 2000, 6:1004-1010.
26. Montagnani M., Chen H., Barr V.A., et al. Insulin-stimulated activation of eNOS is independent of Ca2+ but requires phosphorylation by Akt at Ser(1179). J. Biol. Chem. 2001, 276:30392-30398.
27. Scotland R.S., Morales-Ruiz M., Chen Y., et al. Functional reconstitution of endothelial nitric oxide synthase reveals the importance of serine 1179 in endothelium-dependent vasomotion. Circ. Res. 2002, 90:904-910.
28. Vecchione C., Maffei A., Colella S., et al. Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway. Diabetes 2002, 51:168-173.
29. Chen H., Montagnani M., Funahashi T., et al. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem. 2003, 278:45021-45026.
30. Ouchi N., Kobayashi H., Kihara S., et al. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J. Biol. Chem. 2004, 279:1304-1309.
31. Atochin D.N., Wang A., Liu V.W., et al. The phosphorylation state of eNOS modulates vascular reactivity and outcome of cerebral ischemia in vivo. J. Clin. Invest. 2007, 117:1961-1967.
32. Kahn B.B., Flier J.S. Obesity and insulin resistance. J. Clin. Invest. 2000, 106:473-481.
33. Balon T.W., Nadler J.L. Evidence that nitric oxide increases glucose transport in skeletal muscle. J. Appl. Physiol. 1997, 82:359-363.
34. Higaki Y., Hirshman M.F., Fujii N., et al. Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 2001, 50:241-247.
35. McGrowder D., Ragoobirsingh D., Brown P. Modulation of glucose uptake in adipose tissue by nitric oxide-generating compounds. J. Biosci. 2006, 31:347-354.
36. Roy D., Perreault M., Marette A. Insulin stimulation of glucose uptake in skeletal muscles and adipose tissues in vivo is NO dependent. Am. J. Physiol. 1998, 274:E692-E699.
37. Tanaka T., Nakatani K., Morioka K., et al. Nitric oxide stimulates glucose transport through insulin-independent GLUT4 translocation in 3T3-L1 adipocytes. Eur. J. Endocrinol. 2003, 149:61-67.
38. Petrie J.R., Ueda S., Webb D.J., et al. Endothelial nitric oxide production and insulin sensitivity. A physiological link with implications for pathogenesis of cardiovascular disease. Circulation 1996, 93:1331-1333.
39. Steinberg H.O., Brechtel G., Johnson A., et al. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J. Clin. Invest. 1994, 94:1172-1179.
40. Steinberg H.O., Chaker H., Leaming R., et al. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J. Clin. Invest. 1996, 97:2601-2610.
41. Nisoli E., Clementi E., Moncada S., et al. Mitochondrial biogenesis as a cellular signaling framework. Biochem. Pharmacol. 2004, 67:1-15.
42. Nisoli E., Clementi E., Paolucci C., et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003, 299:896-899.
43. Duplain H., Burcelin R., Sartori C., et al. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 2001, 104:342-345.
44. Shankar R.R., Wu Y., Shen H.Q., et al. Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 2000, 49:684-687.
45. Cook S., Hugli O., Egli M., et al. Partial gene deletion of endothelial nitric oxide synthase predisposes to exaggerated high-fat diet-induced insulin resistance and arterial hypertension. Diabetes 2004, 53:2067-2072.
46. Cook S., Hugli O., Egli M., et al. Clustering of cardiovascular risk factors mimicking the human metabolic syndrome X in eNOS null mice. Swiss Med. Wkly. 2003, 133:360-363.
47. Schleicher M., Yu J., Murata T., et al. The Akt1-eNOS axis illustrates the specificity of kinase-substrate relationships in vivo. Sci. Signal. 2009, 2:ra41.