Endothelial nitric oxide synthase uncoupling: A novel pathway in OSA induced vascular endothelial dysfunction

Respiratory Physiology and Neurobiology

Volumn 207, Issue , 2015, Pages 40-47

  Varadharaj, Saradhadevi ^a,b   Porter, Kyle ^a   Pleister, Adam ^a   Wannemacher, Jacob ^a   Sow, Angela ^a   Jarjoura, David ^a   Zweier, Jay L ^a,b   Khayat, Rami N ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Endothelial dysfunction; Hypertension; Nitric oxide; Obstructive sleep apnea

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; OXYGEN; SUPEROXIDE; TETRAHYDROBIOPTERIN; BIOPTERIN; ENZYME INHIBITOR; SAPROPTERIN;

ADULT; ARTICLE; CARDIOVASCULAR RISK; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN TISSUE; MALE; MICROVASCULATURE; PATHOGENESIS; PROTEIN CONTENT; PROTEIN FUNCTION; SLEEP DISORDERED BREATHING; VASCULAR ENDOTHELIUM; ANALOGS AND DERIVATIVES; CARDIOVASCULAR DISEASES; COMPLICATION; DRUG EFFECTS; ENDOTHELIUM; METABOLISM; MIDDLE AGED; PATHOLOGY; POSITIVE END EXPIRATORY PRESSURE; PROCEDURES; SLEEP APNEA, OBSTRUCTIVE;

ADULT; BIOPTERIN; CARDIOVASCULAR DISEASES; CONTINUOUS POSITIVE AIRWAY PRESSURE; ENDOTHELIUM; ENZYME INHIBITORS; FEMALE; HUMANS; MALE; MIDDLE AGED; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; SLEEP APNEA, OBSTRUCTIVE;

EID: 84920453525     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2014.12.012     Document Type: Article

References (53)

1. Agewall S., Henareh L., Kublickiene K. Endothelial function in conduit and resistance arteries in men with coronary disease. Atherosclerosis 2006, 184:130-136.
2. Antoniades C., Shirodaria C., Warrick N., Cai S., de Bono J., Lee J., Leeson P., Neubauer S., Ratnatunga C., Pillai R., Refsum H., Channon K.M. 5-Methyltetrahydrofolate rapidly improves endothelial function and decreases superoxide production in human vessels: effects on vascular tetrahydrobiopterin availability and endothelial nitric oxide synthase coupling. Circulation 2006, 114:1193-1201.
3. Arnet U.A., McMillan A., Dinerman J.L., Ballermann B., Lowenstein C.J. Regulation of endothelial nitric-oxide synthase during hypoxia. J. Biol. Chem. 1996, 271:15069-15073.
4. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. U.S.A. 1977, 74:3203-3207.
5. Bao G., Randhawa P.M., Fletcher E.C. Acute blood pressure elevation during repetitive hypocapnic and eucapnic hypoxia in rats. J. Appl. Physiol. (1985) 1997, 82:1071-1078.
6. Biondi R., Ambrosio G., De Pascali F., Tritto I., Capodicasa E., Druhan L.J., Hemann C., Zweier J.L. HPLC analysis of tetrahydrobiopterin and its pteridine derivatives using sequential electrochemical and fluorimetric detection: application to tetrahydrobiopterin autoxidation and chemical oxidation. Arch. Biochem. Biophys. 2012, 520:7-16.
7. Brooks D., Horner R.L., Kozar L.F., Render-Teixeira C.L., Phillipson E.A. Obstructive sleep apnea as a cause of systemic hypertension. Evidence from a canine model. J. Clin. Invest. 1997, 99:106-109.
8. Cardounel A.J., Cui H., Samouilov A., Johnson W., Kearns P., Tsai A.L., Berka V., Zweier J.L. Evidence for the pathophysiological role of endogenous methylarginines in regulation of endothelial NO production and vascular function. J. Biol. Chem. 2007, 282:879-887.
9. Chen C.A., Wang T.Y., Varadharaj S., Reyes L.A., Hemann C., Talukder M.A., Chen Y.R., Druhan L.J., Zweier J.L. S-Glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 2010, 468:1115-1118.
10. Clarkson P., Celermajer D.S., Powe A.J., Donald A.E., Henry R.M., Deanfield J.E. Endothelium-dependent dilatation is impaired in young healthy subjects with a family history of premature coronary disease. Circulation 1997, 96:3378-3383.
11. Corretti M.C., Anderson T.J., Benjamin E.J., Celermajer D., Charbonneau F., Creager M.A., Deanfield J., Drexler H., Gerhard-Herman M., Herrington D., Vallance P., Vita J., Vogel R. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J. Am. Coll. Cardiol. 2002, 39:257-265.
12. Cunnington C., Van Assche T., Shirodaria C., Kylintireas I., Lindsay A.C., Lee J.M., Antoniades C., Margaritis M., Lee R., Cerrato R., Crabtree M.J., Francis J.M., Sayeed R., Ratnatunga C., Pillai R., Choudhury R.P., Neubauer S., Channon K.M. Systemic and vascular oxidation limits the efficacy of oral tetrahydrobiopterin treatment in patients with coronary artery disease. Circulation 2012, 125:1356-1366.
13. Dumitrescu C., Biondi R., Xia Y., Cardounel A.J., Druhan L.J., Ambrosio G., Zweier J.L. Myocardial ischemia results in tetrahydrobiopterin (BH4) oxidation with impaired endothelial function ameliorated by BH4. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15081-15086.
14. Efremova L.V., Alekseeva A.Y., Konkova M.S., Kostyuk S.V., Ershova E.S., Smirnova T.D., Konorova I.L., Veiko N.N. Extracellular DNA affects NO content in human endothelial cells. Bull. Exp. Biol. Med. 2010, 149:196-200.
15. El Solh A.A., Saliba R., Bosinski T., Grant B.J., Berbary E., Miller N. Allopurinol improves endothelial function in sleep apnoea: a randomised controlled study. Eur. Respir. J. 2006, 27:997-1002.
16. Fletcher E.C., Bao G., Li R. Renin activity and blood pressure in response to chronic episodic hypoxia. Hypertension 1999, 34:309-314.
17. Fletcher E.C., Lesske J., Behm R., Miller C.C., Stauss H., Unger T. Carotid chemoreceptors, systemic blood pressure, and chronic episodic hypoxia mimicking sleep apnea. J. Appl. Physiol. (1985) 1992, 72:1978-1984.
18. Fletcher E.C., Lesske J., Culman J., Miller C.C., Unger T. Sympathetic denervation blocks blood pressure elevation in episodic hypoxia. Hypertension 1992, 20:612-619.
19. Fletcher E.C., Lesske J., Qian W., Miller C.C., Unger T. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension 1992, 19:555-561.
20. Gozal D., Kheirandish-Gozal L., Serpero L.D., Sans Capdevila O., Dayyat E. Obstructive sleep apnea and endothelial function in school-aged nonobese children: effect of adenotonsillectomy. Circulation 2007, 116:2307-2314.
21. Grebe M., Eisele H.J., Weissmann N., Schaefer C., Tillmanns H., Seeger W., Schulz R. Antioxidant vitamin C improves endothelial function in obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 2006, 173:897-901.
22. Hurshman A.R., Krebs C., Edmondson D.E., Huynh B.H., Marletta M.A. Formation of a pterin radical in the reaction of the heme domain of inducible nitric oxide synthase with oxygen. Biochemistry 1999, 38:15689-15696.
23. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:9265-9269.
24. Ip M.S., Tse H.F., Lam B., Tsang K.W., Lam W.K. Endothelial function in obstructive sleep apnea and response to treatment. Am. J. Respir. Crit. Care Med. 2004, 169:348-353.
25. Jelic S., Le Jemtel T.H. Inflammation, oxidative stress, and the vascular endothelium in obstructive sleep apnea. Trends Cardiovasc. Med. 2008, 18:253-260.
26. Kaczmarek E., Bakker J.P., Clarke D.N., Csizmadia E., Kocher O., Veves A., Tecilazich F., O'Donnell C.P., Ferran C., Malhotra A. Molecular biomarkers of vascular dysfunction in obstructive sleep apnea. PLoS ONE 2013, 8:e70559.
27. Kato M., Roberts-Thomson P., Phillips B.G., Haynes W.G., Winnicki M., Accurso V., Somers V.K. Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea. Circulation 2000, 102:2607-2610.
28. Kuzkaya N., Weissmann N., Harrison D.G., Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J. Biol. Chem. 2003, 278:22546-22554.
29. Lim M.H., Xu D., Lippard S.J. Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nat. Chem. Biol. 2006, 2:375-380.
30. Lind L., Berglund L., Larsson A., Sundstrom J. Endothelial function in resistance and conduit arteries and 5-year risk of cardiovascular disease. Circulation 2011, 123:1545-1551.
31. Marcus N.J., Li Y.L., Bird C.E., Schultz H.D., Morgan B.J. Chronic intermittent hypoxia augments chemoreflex control of sympathetic activity: role of the angiotensin II type 1 receptor. Respir. Physiol. Neurobiol. 2010, 171:36-45.
32. Marin J.M., Carrizo S.J., Vicente E., Agusti A.G. Long-term cardiovascular outcomes in men with obstructive sleep apnoea-hypopnoea with or without treatment with continuous positive airway pressure: an observational study. Lancet 2005, 365:1046-1053.
33. Moller D.S., Lind P., Strunge B., Pedersen E.B. Abnormal vasoactive hormones and 24-hour blood pressure in obstructive sleep apnea. Am. J. Hypertens. 2003, 16:274-280.
34. Ozaki M., Kawashima S., Yamashita T., Hirase T., Namiki M., Inoue N., Hirata K., Yasui H., Sakurai H., Yoshida Y., Masada M., Yokoyama M. Overexpression of endothelial nitric oxide synthase accelerates atherosclerotic lesion formation in apoE-deficient mice. J. Clin. Invest. 2002, 110:331-340.
35. Park J.B., Charbonneau F., Schiffrin E.L. Correlation of endothelial function in large and small arteries in human essential hypertension. J. Hypertens. 2001, 19:415-420.
36. Patt B.T., Jarjoura D., Haddad D.N., Sen C.K., Roy S., Flavahan N.A., Khayat R.N. Endothelial dysfunction in the microcirculation of patients with obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 2010, 182:1540-1545.
37. Peng Y.J., Overholt J.L., Kline D., Kumar G.K., Prabhakar N.R. Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10073-10078.
38. Peppard P.E., Young T., Palta M., Skatrud J. Prospective study of the association between sleep-disordered breathing and hypertension. N. Engl. J. Med. 2000, 342:1378-1384.
39. Philippi N.R., Bird C.E., Marcus N.J., Olson E.B., Chesler N.C., Morgan B.J. Time course of intermittent hypoxia-induced impairments in resistance artery structure and function. Respir. Physiol. Neurobiol. 2010, 170:157-163.
40. Phillips S.A., Olson E.B., Morgan B.J., Lombard J.H. Chronic intermittent hypoxia impairs endothelium-dependent dilation in rat cerebral and skeletal muscle resistance arteries. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H388-H393.
41. Schmidt P.P., Lange R., Gorren A.C., Werner E.R., Mayer B., Andersson K.K. Formation of a protonated trihydrobiopterin radical cation in the first reaction cycle of neuronal and endothelial nitric oxide synthase detected by electron paramagnetic resonance spectroscopy. J. Biol. Inorg. Chem. 2001, 6:151-158.
42. Schreiber F., Beutler M., Enning D., Lamprecht-Grandio M., Zafra O., Gonzalez-Pastor J.E., de Beer D. The role of nitric-oxide-synthase-derived nitric oxide in multicellular traits of Bacillus subtilis 3610: biofilm formation, swarming, and dispersal. BMC Microbiol. 2011, 11:111.
43. Shi W., Wang X., Shih D.M., Laubach V.E., Navab M., Lusis A.J. Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase. Circulation 2002, 105:2078-2082.
44. Somers V.K., Dyken M.E., Clary M.P., Abboud F.M. Sympathetic neural mechanisms in obstructive sleep apnea. J. Clin. Invest. 1995, 96:1897-1904.
45. Suwaidi J.A., Hamasaki S., Higano S.T., Nishimura R.A., Holmes D.R., Lerman A. Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation 2000, 101:948-954.
46. Takemoto M., Sun J., Hiroki J., Shimokawa H., Liao J.K. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation 2002, 106:57-62.
47. Vasquez-Vivar J., Martasek P., Whitsett J., Joseph J., Kalyanaraman B. The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem. J. 2002, 362:733-739.
48. Wang P., Zweier J.L. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J. Biol. Chem. 1996, 271:29223-29230.
49. Wilson P.W., D'Agostino R.B., Levy D., Belanger A.M., Silbershatz H., Kannel W.B. Prediction of coronary heart disease using risk factor categories. Circulation 1998, 97:1837-1847.
50. Worthley M.I., Kanani R.S., Sun Y.H., Sun Y., Goodhart D.M., Curtis M.J., Anderson T.J. Effects of tetrahydrobiopterin on coronary vascular reactivity in atherosclerotic human coronary arteries. Cardiovasc. Res. 2007, 76:539-546.
51. Xie A., Skatrud J.B., Crabtree D.C., Puleo D.S., Goodman B.M., Morgan B.J. Neurocirculatory consequences of intermittent asphyxia in humans. J. Appl. Physiol. 2000, 89:1333-1339.
52. Yang C., Talukder M.A., Varadharaj S., Velayutham M., Zweier J.L. Early ischaemic preconditioning requires Akt- and PKA-mediated activation of eNOS via serine1176 phosphorylation. Cardiovasc. Res. 2013, 97:33-43.
53. Yuan Z.M., Chen B.Y., Wang P.X., Li S.Y., Chen Y.L., Dong L.X. Changes of angiotensin II and its receptor during the development of chronic intermittent hypoxia-induced hypertension in rats. Zhonghua Jie He He Hu Xi Za Zhi 2004, 27:577-580.