Dissociation of endothelial nitric oxide synthase phosphorylation and activity in uterine artery endothelial cells

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 290, Issue 4, 2006, Pages

  Cale, Jacqueline M ^a   Bird, Ian M ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b MERITER HOSPITAL   (United States)

Author keywords

Bovine aortic endothelial cells; Calmodulin; Ovine; Pregnancy

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ADENOSINE TRIPHOSPHATE; PHORBOL 13 ACETATE 12 MYRISTATE;

ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CONTROLLED STUDY; DNA POLYMORPHISM; ENDOTHELIUM CELL; GENETIC TRANSFECTION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; UTERINE ARTERY; ANIMAL; ARTERY; CELL CULTURE; CELL STRAIN COS1; CERCOPITHECUS; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; SHEEP; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; UTERUS; VASCULARIZATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ARTERIES; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FEMALE; MUTAGENESIS, SITE-DIRECTED; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN BINDING; SHEEP; STRUCTURE-ACTIVITY RELATIONSHIP; TETRADECANOYLPHORBOL ACETATE; UTERUS;

EID: 33646081055     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00942.2005     Document Type: Article

References (56)

1. Bauer PM, Fulton D, Boo YC, Sorescu GP, Kemp BE, Jo H, and Sessa WC. Compensatory phosphorylation and protein-protein interactions revealed by loss of function and gain of function mutants of multiple serine phosphorylation sites in endothelial nitric-oxide synthase. J Biol Chem 278: 14841-14849, 2003.
2. Bird IM, Sullivan JA, Di T, Cale JM, Zhang L, Zheng J, and Magness RR. Pregnancy-dependent changes in cell signaling underlie changes in differential control of vasodilator production in uterine artery endothelial cells. Endocrinology 141: 1107-1117, 2000.
3. Bird IM, Zhang L, and Magness RR. Possible mechanisms underlying pregnancy-induced changes in uterine artery endothelial function. Am J Physiol Regul Integr Comp Physiol 284: R245-R258, 2003.
4. Bodin P and Burnstock G. Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J Cardiovasc Pharmacol 38: 900-908, 2001.
5. 635 by a protein kinase A-dependent mechanism. Am J Physiol Heart Circ Physiol 283: H1819-H1828, 2002.
6. Boo YC, Sorescu GP, Bauer PM, Fulton D, Kemp BE, Harrison DG, Sessa WC, and Jo H. Endothelial NO synthase phosphorylated at SER635 produces NO without requiring intracellular calcium increase. Free Radic Biol Med 35: 729-741, 2003.
7. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL, and Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res 89: 866-873, 2001.
8. Cale JM, Tsoi SC, Toppe M, Grummer MA, Ochiai M, Magness RR, and Bird IM. Molecular cloning of ovine endothelial nitric oxide synthase and expression in COS-7 cells. J Soc Gynecol Investig 12: 156-168, 2005.
9. Chen BC, Lin LL, and Lin WW. Protein kinase C epsilon-dependent pathway of extracellular signal-regulated protein kinase activation by P2Y1 and P2Y2 purinoceptors that activate cytosolic phospholipase A2 in endothelial cells. Eur J Pharmacol 373: 101-110, 1999.
10. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, and Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443: 285-289, 1999.
11. Chu S and Bohlen HG. High concentration of glucose inhibits glomerular endothelial eNOS through a PKC mechanism. Am J Physiol Renal Physiol 287: F384-F392, 2004.
12. 2+ sensitivity of endothelial nitric oxide synthase as well as cytosolic phospholipase A(2). Endocrinology 142: 3014-3026, 2001.
13. Dimmeler S, Dernbach E, and Zeiher AM. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 477: 258-262, 2000.
14. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, and Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
15. 2+/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 88: E68-E75, 2001.
16. Fontana J, Fulton D, Chen Y, Fairchild TA, McCabe TJ, Fujita N, Tsuruo T, and Sessa WC. Domain mapping studies reveal that the M domain of hsp90 serves as a molecular scaffold to regulate Akt-dependent phosphorylation of endothelial nitric oxide synthase and NO release. Circ Res 90: 866-873, 2002.
17. Fulton D, Babbitt R, Zoellner S, Fontana J, Acevedo L, McCabe TJ, Iwakiri Y, and Sessa WC. Targeting of endothelial nitric-oxide synthase to the cytoplasmic face of the Golgi complex or plasma membrane regulates Akt- versus calcium-dependent mechanisms for nitric oxide release. J Biol Chem 279: 30349-30357, 2004.
18. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, and Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601, 1999.
19. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, and Sessa WC. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272: 25437-25440, 1997.
20. Gifford SM, Cale JM, Tsoi S, Magness RR, and Bird IM. Pregnancy-specific changes in uterine artery endothelial cell signaling in vivo are both programmed and retained in primary culture. Endocrinology 144: 3639-3650, 2003.
21. Gonzalez E, Kou R, Lin AJ, Golan DE, and Michel T. Subcellular targeting and agonist-induced site-specific phosphorylation of endothelial nitric-oxide synthase. J Biol Chem 277: 39554-39560, 2002.
22. Gratton JP, Fontana J, O'Connor DS, Garcia-Cardena G, McCabe TJ, and Sessa WC. Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro. Evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J Biol Chem 275: 22268-22272, 2000.
23. Greif DM, Kou R, and Michel T. Site-specific dephosphorylation of endothelial nitric oxide synthase by protein phosphatase 2A: evidence for crosstalk between phosphorylation sites. Biochemistry 41: 15845-15853, 2002.
24. Harris MB, Blackstone MA, Sood SG, Li C, Goolsby JM, Venema VJ, Kemp BE, and Venema RC. Acute activation and phosphorylation of endothelial nitric oxide synthase by HMG-CoA reductase inhibitors. Am J Physiol Heart Circ Physiol 287: H560-H566, 2004.
25. Harris MB, Ju H, Venema VJ, Liang H, Zou R, Michell BJ, Chen ZP, Kemp BE, and Venema RC. Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J Biol Chem 276: 16587-16591, 2001.
26. Hellermann GR and Solomonson LP. Calmodulin promotes dimerization of the oxygenase domain of human endothelial nitric-oxide synthase. J Biol Chem 272: 12030-12034, 1997.
27. Hisamoto K, Ohmichi M, Kanda Y, Adachi K, Nishio Y, Hayakawa J, Mabuchi S, Takahashi K, Tasaka K, Miyamoto Y, Taniguchi N, and Murata Y. Induction of endothelial nitric-oxide synthase phosphorylation by the raloxifene analog LY117018 is differentially mediated by Akt and extracellular signal-regulated protein kinase in vascular endothelial cells. J Biol Chem 276: 47642-47649, 2001.
28. Kou R, Greif D, and Michel T. Dephosphorylation of endothelial nitric-oxide synthase by vascular endothelial growth factor. Implications for the vascular responses to cyclosporin A. J Biol Chem 277: 29669-29673, 2002.
29. Kublickiene KR, Lindblom B, Kruger K, and Nisell H. Preeclampsia: evidence for impaired shear stress-mediated nitric oxide release in uterine circulation. Am J Obstet Gynecol 183: 160-166, 2000.
30. Lane P and Gross SS. Disabling a C-terminal autoinhibitory control element in endothelial nitric-oxide synthase by phosphorylation provides a molecular explanation for activation of vascular NO synthesis by diverse physiological stimuli. J Biol Chem 277: 19087-19094, 2002.
31. Lin MI, Fulton D, Babbitt R, Fleming I, Busse R, Pritchard KA Jr, and Sessa WC. Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production. J Biol Chem 278: 44719-44726, 2003.
32. Liu J, Garcia-Cardena G, and Sessa WC. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry 35: 13277-13281, 1996.
33. Lungu AO, Jin ZG, Yamawaki H, Tanimoto T, Wong C, and Berk BC. Cyclosporin A inhibits flow-mediated activation of endothelial nitric-oxide synthase by altering cholesterol content in caveolae. J Biol Chem 279: 48794-48800, 2004.
34. 2+-calmodulin. Biochemistry 35: 14651-14658, 1996.
35. McCabe TJ, Fulton D, Roman LJ, and Sessa WC. Enhanced electron flux and reduced calmodulin dissociation may explain "calcium-independent" eNOS activation by phosphorylation. J Biol Chem 275: 6123-6128, 2000.
36. McHugh D, Sharp EM, Scheuer T, and Catterall WA. Inhibition of cardiac L-type calcium channels by protein kinase C phosphorylation of two sites in the N-terminal domain. Proc Natl Acad Sci USA 97: 12334-12338, 2000.
37. Michel JB, Feron O, Sase K, Prabhakar P, and Michel T. Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem 272: 25907-25912, 1997.
38. Michell BJ, Chen Z, Tiganis T, Stapleton D, Katsis F, Power DA, Sim AT, and Kemp BE. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem 276: 17625-17628, 2001.
39. Michell BJ, Griffiths JE, Mitchelhill KI, Rodriguez-Crespo I, Tiganis T, Bozinovski S, de Montellano PR, Kemp BE, and Pearson RB. The Akt kinase signals directly to endothelial nitric oxide synthase. Curr Biol 9: 845-848, 1999.
40. Michell BJ, Harris MB, Chen ZP, Ju H, Venema VJ, Blackstone MA, Huang W, Venema RC, and Kemp BE. Identification of regulatory sites of phosphorylation of the bovine endothelial nitric-oxide synthase at serine 617 and serine 635. J Biol Chem 277: 42344-42351, 2002.
41. Montagnani M, Chen H, Barr VA, and Quon MJ. Insulin-stimulated activation of eNOS is independent of Ca2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 276: 30392-30398, 2001.
42. Partovian C, Zhuang Z, Moodie K, Lin M, Ouchi N, Sessa WC, Walsh K, and Simons M. PKCalpha activates eNOS and increases arterial blood flow in vivo. Circ Res 97: 482-487, 2005.
43. Rizzo V, McIntosh DP, Oh P, and Schnitzer JE. In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J Biol Chem 273: 34724-34729, 1998.
44. Ryan US, Avdonin PV, Posin EY, Popov EG, Danilov SM, and Tkachuk VA. Influence of vasoactive agents on cytoplasmic free calcium in vascular endothelial cells. J Appl Physiol 65: 2221-2227, 1988.
45. Scotland RS, Morales-Ruiz M, Chen Y, Yu J, Rudic RD, Fulton D, Gratton JP, and Sessa WC. Functional reconstitution of endothelial nitric oxide synthase reveals the importance of serine 1179 in endothelium-dependent vasomotion. Circ Res 90: 904-910, 2002.
46. Shaul PW, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson RG, and Michel T. Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 271: 6518-6522, 1996.
47. Sullivan JA, Grummer MA, Yi FX, and Bird IM. Pregnancy-enhanced eNOS activation in Uterine artery endothelial cells. Endocrinology. In Press.
48. Summers BA, Overholt JL, and Prabhakar NR. Augmentation of L-type calcium current by hypoxia in rabbit carotid body glomus cells: evidence for a PKC-sensitive pathway. J Neurophysiol 84: 1636-1644, 2000.
49. Takahashi S and Mendelsohn ME. Calmodulin-dependent and -independent activation of endothelial nitric-oxide synthase by heat shock protein 90. J Biol Chem 278: 9339-9344, 2003.
50. Tanimoto T, Jin ZG, and Berk BC. Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J Biol Chem 277: 42997- 43001, 2002.
51. Thors B, Halldorsson H, and Thorgeirsson G. Thrombin and histamine stimulate endothelial nitric-oxide synthase phosphorylation at Ser1177 via an AMPK mediated pathway independent of PI3K-Akt. FEBS Lett 573: 175-180, 2004.
52. Weiner C, Liu KZ, Thompson L, Herrig J, and Chestnut D. Effect of pregnancy on endothelium and smooth muscle: their role in reduced adrenergic sensitivity. Am J Physiol Heart Circ Physiol 261: H1275-H1283, 1991.
53. Weiner CP, Martinez E, Chestnut DH, and Ghodsi A. Effect of pregnancy on uterine and carotid artery response to norepinephrine, epinephrine, and phenylephrine in vessels with documented functional endothelium. Am J Obstet Gynecol 161: 1605-1610, 1989.
54. Weiner CP, Thompson LP, Liu KZ, and Herrig JE. Pregnancy reduces serotonin-induced contraction of guinea pig uterine and carotid arteries. Am J Physiol Heart Circ Physiol 263: H1764-H1769, 1992.
55. i and intracellular NO production in freshly isolated uterine artery endothelial cells: effects of ovarian cycle and pregnancy. Am J Physiol Regul Integr Comp Physiol 288: R140-R148, 2005.
56. Zemojtel T, Scheele JS, Martasek P, Masters BS, Sharma VS, and Magde D. Role of the interdomain linker probed by kinetics of CO ligation to an endothelial nitric oxide synthase mutant lacking the calmodulin binding peptide (residues 503-517 in bovine). Biochemistry 42: 6500-6506, 2003.