Insulin enhances the expression of the endothelial nitric oxide synthase in native endothelial cells: A dual role for Akt and AP-1

Nitric Oxide - Biology and Chemistry

Volumn 8, Issue 4, 2003, Pages 253-261

  Fisslthaler, Beate ^a   Benzing, Thomas ^a,b   Busse, Rudi ^a   Fleming, Ingrid ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Akt; AP 1; Endothelial nitric oxide synthase; Endothelium; Insulin; Sp1; Transcription factors

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CYCLIC GMP; INSULIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR SP1;

ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL INTERACTION; CONTROLLED STUDY; DNA BINDING; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

SUIDAE;

EID: 0041663621     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1089-8603(03)00042-9     Document Type: Article

References (51)

1. Whitehead J.P., Clark S.F., Urso B., James D.E. Signalling through the insulin receptor. Curr. Opin. Cell Biol. 12:2000;222-228.
2. Steinberg H.O., Brechtel G., Johnson A., Fineberg N., Baron A.D. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. J. Clin. Invest. 94:1994;1172-1179.
3. Taddei S., Virdis A., Mattei P., Natali A., Ferrannini E., Salvetti A. Effect of insulin on acetylcholine-induced vasodilation in normotensive subjects and patients with essential hypertension. Circulation. 92:1995;2911-2918.
4. Lembo G., Iaccarino G., Vecchione C., Barbato E., Izzo R., Fontana D., Trimarco B. Insulin modulation of an endothelial nitric oxide component present in the α2- and β-adrenergic responses in human forearm. J. Clin. Invest. 100:1997;2007-2014.
5. Chen Y.-L., Messina E.J. Dilation of isolated skeletal muscle arterioles by insulin is endothelium-dependent and nitric oxide mediated. Am. J. Physiol. 270:1996;H2120-H2124.
6. Laight D.W., Kaw A.V., Carrier M.J., Anggard E.E. Pharmacological modulation of endothelial function by insulin in the rat aorta. J. Pharm. Pharmacol. 50:1998;1117-1120.
7. Lembo G., Iaccarino G., Vecchione C., Barbato E., Morisco C., Monti F., Parrella L., Trimarco B. Insulin enhances endothelial α2-adrenergic vasorelaxation by a pertussis toxin mechanism. Hypertension. 30:1997;1128-1134.
8. 2+ level and contraction in the rat aorta. Circ. Res. 77:1995;673-678.
9. 2+ influx and contraction in vascular smooth muscle. Circulation. 92:1995;1597-1603.
10. 2+ store in porcine coronary artery smooth muscle. Diabetes. 45:1996;876-889.
11. Hasdai D., Rizza R.A., Holmes D.R. Jr., Richardson D.M., Cohen P., Lerman A. Insulin and insulin-like growth factor-I cause coronary vasorelaxation in vitro. Hypertension. 32:1998;228.
12. Cardillo C., Kilcoyne C.M., Nambi S.S., Cannon R.O., Quon M.J., Panza J.A. Vasodilator response to systemic but not to local hyperinsulinemia in the human forearm. Hypertension. 32:1998;740-745.
13. Ueda S., Petrie J.R., Cleland S.J., Elliott H.L., Connell J.M.C. The vasodilating effect of insulin is dependent on local glucose uptake: a double blind, placebo-controlled study. J. Clin. Endocrinol. Metab. 83:1998;2126-2131.
14. Zeng G., Quon M.J. Insulin-stimulated production of nitric oxide is inhibited by wortmannin - direct measurement in vascular endothelial cells. J. Clin. Invest. 98:1996;894-898.
15. Zeng G., Nystrom F.H., Ravichandran L.V., Cong L.-N., Kirby M., Mostowski H., Quon M.J. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation. 101:2000;1539-1545.
16. Bar R.S., Boes M. Distinct receptors for IGF-I, IGF-II, and insulin are present on bovine capillary endothelial cells and large vessel endothelial cells. Biochem. Biophys. Res Commun. 124:1984;203-209.
17. Randriamboavonjy V., Busse R., Fleming I. 20-HETE-induced contraction of small coronary arteries depends on the activation of Rho-kinase. Hypertension. 41:2003;801-806.
18. Busse R., Lamontagne D. Endothelium-derived bradykinin is responsible for the increase in calcium produced by angiotensin-converting enzyme inhibitors in human endothelial cells. Naunyn Schmiedebergs Arch. Pharmacol. 344:1991;126-129.
19. Fleming I., Fisslthaler B., Busse R. Calcium signaling in endothelial cells involves activation of tyrosine kinases and leads to activation of MAP kinase. Circ. Res. 76:1995;522-529.
20. 2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress. Circ. Res. 82:1998;686-695.
21. Chao T.-S.O., Byron K.L., Lee K.-M., Villereal M., Rosner M.R. Activation of MAP kinases by calcium-dependent and calcium-independent pathways. J. Biol. Chem. 267:1992;19876-19883.
22. Zeiher A.M., Fisslthaler B., Schray-Utz B., Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ. Res. 76:1995;980-986.
23. Bouloumié A., Schini-Kerth V.B., Busse R. Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardiovasc. Res. 41:1999;773-780.
24. Bertrand F., Philippe C., Antoine P.-J., Baud L., Groyer A., Capeau J., Cherqui G. Insulin activates nuclear factor κB in mammalian cells through a Raf-1-mediated pathway. J. Biol. Chem. 270:1995;24435-24441.
25. Romashkova J.A., Makarov S.S. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 401:1999;86-90.
26. Ozes O.N., mayo L.D., Gustin J.A., Pfeffer S.R., Pfeffer L.M., Donner D.B. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature. 401:1999;82-85.
27. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R., Zeiher A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 399:1999;601-605.
28. Fulton D., Gratton J.-P., Mccabe T.J., Fontana J., Fujio Y., Walsh K., Franke T.F., Papapetropoulos A., Sessa W.C. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 399:1999;597-601.
29. Li H., Wallerath T., Förstermann U. Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide. 7:2002;132-147.
30. Wang X.L., Wang J. Endothelial nitric oxide synthase gene sequence variations and vascular disease. Mol. Genet. Metab. 70:2000;241-251.
31. Förstermann U., Boissel J.-P., Kleinert H. Expressional control of the "constitutive" isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12:1998;773-790.
32. Ranjan V., Xiao Z., Diamond S.L. Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. Am. J. Physiol. 269:1995;H550-H555.
33. Uematsu M., Ohara Y., Navas J.P., Nishida K., Murphy T.J., Alexander R.W., Nerem R.M., Harrison D.G. Regulation of endothelial cell nitric oxide synthase mRNA by shear stress. Am. J. Physiol. 269:1995;C1371-C1378.
34. Papapetropoulos A., García-Cardena G., Madri J.A., Sessa W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100:1997;3131-3139.
35. Kuboki K., Jiang Z.Y., Takahara N., Ha S.W., Igarashi M., Yamauchi T., Feener E.P., Herbert T.P., Rhodes C.J., King G.L. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo. Circulation. 101:2000;676-681.
36. Zhang R., Min W., Sessa W.C. Functional analysis of the human endothelial nitric oxide synthase promoter. Sp1 and GATA factors are necessary for basal transcription in endothelial cells. J. Biol. Chem. 270:1995;15320-15326.
37. Tang J.-L., Zembowicz A., Xu X.-M., Wu K.K. Role of SP1 in transcriptional activation of human nitric oxide synthase type III gene. Biochem. Biophys. Res. Commun. 213:1995;673-680.
38. Kamakura S., Moriguchi T., Nishida E. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274:2000;26563-26571.
39. Scott P.H., Lawrence J.C. Insulin activates a PD 098059-sensitive kinase that is involved in the regulation of p70(S6K) and PHAS-I. FEBS Lett. 409:1997;171-176.
40. Reiners J.J., Lee J.-Y., Clift R.E., Dudley D.T., Myrand S.P. PD98059 is an equipotent antagonist of the aryl hydrocarbon receptor and inhibitor of mitogen-activated protein kinase kinase. Mol. Pharmacol. 53:1998;438-445.
41. Karantzoulis-Fegaras F., Antoniou H., Lai S.L., Kulkarni G., D'Abreo C., Wong G.K., Miller T.L., Chan Y., Atkins J., Wang Y., Marsden P.A. Characterization of the human endothelial nitric-oxide synthase promoter. J. Biol. Chem. 274:1999;3076-3093.
42. Navarro-Antolin J., Hernandez-Perera O., Lopez-Ongil S., Rodriguez-Puyol M., Rodriguez-Puyol D., Lamas S. CsA and FK506 up-regulate eNOS expression: role of reactive oxygen species and AP-1. Kidney Int. 68:1998;20-24.
43. Navarro-Antolin J., Rey-Campos J., Lamas S. Transcriptional induction of endothelial nitric oxide gene by cyclosporine A. A role for activator protein-1. J. Biol. Chem. 275:2000;3075-3080.
44. Nagel T., Resnick N., Dewey C.F. Jr., Gimbrone M.A. Jr. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler. Thromb. Vasc. Biol. 19:1999;1825-1834.
45. Myers P.R., Minor R.L., Guerra R., Bates J.N., Harrison D.G. Vasorelaxant properties of the endothelium-derived relaxing factor more closely resembles S-nitrosocysteine than nitric oxide. Nature. 345:1990;161-163.
46. Vicent D., Ilany J., Kondo T., Naruse K., Fisher S.J., Kisanuki Y.Y., Bursell S., Yanagisawa M., King G.L., Kahn C.R. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J. Clin. Invest. 111:2003;1373.
47. Pieper G.M. Review of alterations in endothelial nitric oxide production in diabetes. Hypertension. 31:1998;1047-1060.
48. Sobrevia L., Mann G.E. Dysfunction of the endothelial nitric oxide signalling pathway in diabetes and hyperglycaemia. Exp. Physiol. 82:1997;432-452.
49. Guzik T.J., Mussa S., Gastaldi D., Sadowski J., Ratnatunga C., Pillai R., Channon K.M. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation. 105:2002;1656-1662.
50. Kobayashi T., Kamata K. Short-term insulin treatment and aortic expressions of IGF-1 receptor and VEGF mRNA in diabetic rats. Am. J. Physiol. Heart Circ. Physiol. 283:2002;H1761-H1768.
51. Busse R., Fleming I. Nitric oxide, nitric oxide synthase and hypertensive vascular disease. Curr. Hypertens. Rep. 1:1999;88-95.