Cyclooxygenases 1 and 2 differentially regulate blood pressure and cerebrovascular responses to acute and chronic intermittent hypoxia: Implications for sleep Apnea

Journal of the American Heart Association

Volumn 3, Issue 3, 2014, Pages

  Beaudin, Andrew E ^a   Pun, Matiram ^a   Yang, Christina ^a   Nicholl, David D M ^a   Steinback, Craig D ^a   Slater, Donna M ^a   Wynne Edwards, Katherine E ^b,c   Hanly, Patrick J ^a,b,c,d   Ahmed, Sofia B ^a,b   Poulin, Marc J ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d FOOTHILLS HOSPITAL   (Canada)

Author keywords

Blood pressure; Cerebrovascular circulation; Intermittent hypoxia; Obstructive sleep apnea; Prostaglandins

Indexed keywords

CELECOXIB; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; INDOMETACIN; PLACEBO; PROSTAGLANDIN E2; THROMBOXANE A2; CYCLOOXYGENASE 2 INHIBITOR; PROSTACYCLIN; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN SYNTHASE INHIBITOR; PYRAZOLE DERIVATIVE; SULFONAMIDE;

ACUTE INTERMITTENT HYPOXIA; ADULT; AGED; ARTICLE; BLOOD PRESSURE REGULATION; BRAIN BLOOD FLOW; CHRONIC INTERMITTENT HYPOXIA; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; ELEVATED BLOOD PRESSURE; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; INTERMITTENT HYPOXIA; MALE; MORBIDITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SLEEP DISORDERED BREATHING; ANOXIA; BLOOD PRESSURE; BRAIN CIRCULATION; DRUG EFFECTS; HEART RATE; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; URINE;

ADULT; ANOXIA; BLOOD PRESSURE; CELECOXIB; CEREBROVASCULAR CIRCULATION; CROSS-OVER STUDIES; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYCLOOXYGENASE INHIBITORS; DINOPROST; DINOPROSTONE; DOUBLE-BLIND METHOD; EPOPROSTENOL; FEMALE; HEART RATE; HUMANS; INDOMETHACIN; MALE; MIDDLE AGED; PYRAZOLES; SLEEP APNEA, OBSTRUCTIVE; SULFONAMIDES; THROMBOXANE A2;

EID: 84925497687     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.000875     Document Type: Article

References (64)

1. Punjabi NM. The epidemiology of adult obstructive sleep apnea. Proc Am Thorac Soc. 2008;5:136-143.
2. Somers VK, White DP, Amin R, Abraham WT, Costa F, Culebras A, Daniels S, Floras JS, Hunt CE, Olson LJ, Pickering TG, Russell R, Woo M, Young T. Sleep apnea and cardiovascular disease: an american Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing. In Collaboration with the National Heart, Lung, and Blood Institute National Center on Sleep Disorders Research (National Institutes of Health). Circulation. 2008;118:1080-1111.
3. Tamisier R, Pepin JL, Remy J, Baguet JP, Taylor JA, Weiss JW, Levy P. 14 nights of intermittent hypoxia elevate daytime blood pressure and sympathetic activity in healthy humans. Eur Respir J. 2011;37:119-128.
4. Foster GE, Hanly PJ, Ahmed SB, Beaudin AE, Pialoux V, Poulin MJ. Intermittent hypoxia increases arterial blood pressure in humans through a reninangiotensin-system dependent mechanism. Hypertension. 2010;56:369-377.
5. Foster GE, Brugniaux JV, Pialoux V, Duggan CT, Hanly PJ, Ahmed SB, Poulin MJ. Cardiovascular and cerebrovascular responses to acute hypoxia following exposure to intermittent hypoxia in healthy humans. J Physiol. 2009; 587:3287-3299.
6. Ryan S, Taylor CT, McNicholas WT. Systemic inflammation: a key factor in the pathogenesis of cardiovascular complications in obstructive sleep apnoea syndrome? Thorax. 2009;64:631-636.
7. Lavie L. Oxidative stress and inflammation in OSA. Sleep Apnoea. European Respiratory Society Journals Ltd; 2010:360-380.
8. Ricciotti E, FitzGerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol. 2011;31:986-1000.
9. Smyth EM, Grosser T, Wang M, Yu Y, FitzGerald GA. Prostanoids in health and disease. J Lipid Res. 2009;50(suppl):S423-S428.
10. Pickard JD, Mackenzie ET. Inhibition of prostaglandin synthesis and the response of baboon cerebral circulation to carbon dioxide. Nat New Biol. 1973;245:187-188.
11. Wennmalm Å, Eriksson S, Wahren J. Effect of indomethacin on basal and carbon dioxide stimulated cerebral blood flow in man. Clin Physiol. 1981;1:227-234.
12. Coxib and traditional NSAID Trialists' (CNT) Collaboration, Bhala N, Emberson J, Merhi A, Abramson S, Arber N, Baron JA, Bombardier C, Cannon C, Farkouh ME, Fitzgerald GA, Goss P, Halls H, Hawk E, Hawkey C, Hennekens C, Hochberg M, Holland LE, Kearney PM, Laine L, Lanas A, Lance P, Laupacis A, Oates J, Patrono C, Schnitzer TJ, Solomon S, Tugwell P, Wilson K, Wittes J, Baigent C. Vascular and upper gastrointestinal effects of non-steroidal antiinflammatory drugs: meta-analyses of individual participant data from randomised trials. Lancet. 2013;382:769-779.
13. Grosser T, Fries S, FitzGerald GA. Biological basis for the cardiovascular consequences of cox-2 inhibition: therapeutic challenges and opportunities. J Clin Invest. 2006;116:4-15.
14. Mitchell JA, Warner TD. Reply to ricciotti et al.: evidence for vascular cox isoforms. Proc Natl Acad Sci USA. 2013; 110:E184
15. Ricciotti E, Yu Y, Grosser T, Fitzgerald GA. Cox-2, the dominant source of prostacyclin. Proc Natl Acad Sci USA. 2013;110:E183.
16. Kirkby NS, Lundberg MH, Harrington LS, Leadbeater PD, Milne GL, Potter CM, Al-Yamani M, Adeyemi O, Warner TD, Mitchell JA. Cyclooxygenase-1, not cyclooxygenase-2, is responsible for physiological production of prostacyclin in the cardiovascular system. Proc Natl Acad Sci USA. 2012;109:17597-17602.
17. Nacher M, Farre R, Montserrat JM, Torres M, Navajas D, Bulbena O, Serrano-Mollar A. Biological consequences of oxygen desaturation and respiratory effort in an acute animal model of obstructive sleep apnea (OSA). Sleep Med. 2009;10:892-897.
18. Gautier-Veyret E, Arnaud C, Bäck M, Pépin J-L, Petri MH, Baguet J-P, Tamisier R, Lévy P, Stanke-Labesque F. Intermittent hypoxia-activated cyclooxygenase pathway: role in atherosclerosis. Eur Respir J. 2013;42:404-413.
19. Issa FG, Morrison D, Hadjuk E, Iyer A, Feroah T, Remmers JE. Digital monitoring of sleep-disordered breathing using snoring sound and arterial oxygen saturation. Am Rev Respir Dis. 1993;148:1023-1029.
20. Vazquez JC, Tsai WH, Flemons WW, Masuda A, Brant R, Hajduk E, Whitelaw WA, Remmers JE. Automated analysis of digital oximetry in the diagnosis of obstructive sleep apnoea. Thorax. 2000;55:302-307.
21. Stichtenoth DO, Marhauer V, Tsikas D, Gutzki FM, Frolich JC. Effects of specific COX-2-inhibition on renin release and renal and systemic prostanoid synthesis in healthy volunteers. Kidney Int. 2005;68:2197-2207.
22. Collop NA, Anderson WM, Boehlecke B, Claman D, Goldberg R, Gottlieb DJ, Hudgel D, Sateia M, Schwab R. Portable Monitoring Task Force of the American Academy of Sleep M. Clinical guidelines for the use of unattended portable monitors in the diagnosis of obstructive sleep apnea in adult patients. Portable Monitoring Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med. 2007;3:737-747.
23. Nieto FJ, Young TB, Lind BK, Shahar E, Samet JM, Redline S, D'Agostino RB, Newman AB, Lebowitz MD, Pickering TG. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep heart health study. JAMA. 2000;283:1829-1836.
24. Shoback DM, Williams GH, Swartz SL, Davies RO, Hollenberg NK. Time course and effect of sodium intake on vascular and hormonal responses to enalapril (MK 421) in normal subjects. J Cardiovasc Pharmacol. 1983;5:1010-1018.
25. Chidambaram M, Duncan JA, Lai VS, Cattran DC, Floras JS, Scholey JW, Miller JA. Variation in the renin angiotensin system throughout the normal menstrual cycle. J Am Soc Nephrol. 2002;13:446-452.
26. Seifarth C, Trenkel S, Schobel H, Hahn EG, Hensen J. Influence of antihypertensive medication on aldosterone and renin concentration in the differential diagnosis of essential hypertension and primary aldosteronism. Clin Endocrinol (Oxf). 2002;57:457-465.
27. Lix LM, Keselman JC, Keselman HJ. Consequences of assumption violations revisited: a quantitative review of alternatives to the one-way analysis of variance "f" test. Rev Educ Res. 1996;66:579-619.
28. Glass GV, Peckham PD, Sanders JR. Consequences of failure to meet assumptions underlying the fixed effects analyses of variance and covariance. Rev Educ Res. 1972;42:237-288.
29. Harwell MR, Rubinstein EN, Hayes WS, Olds CC. Summarizing monte carlo results in methodological research: the one-and two-factor fixed effects anova cases. J Educ Behav Stat. 1992;17:315-339.
30. Alderman MH. Salt, blood pressure, and human health. Hypertension. 2000;36:890-893.
31. Kahraman L, Thach BT. Inhibitory effects of hyperthermia on mechanisms involved in autoresuscitation from hypoxic apnea in mice: a model for thermal stress causing sids. J Appl Physiol. 2004;97:669-674.
32. Tanaka T, Okamura T, Miura K, Kadowaki T, Ueshima H, Nakagawa H, Hashimoto T. A simple method to estimate populational 24-h urinary sodium and potassium excretion using a casual urine specimen. J Hum Hypertens. 2002;16:97-103.
33. Catella-Lawson F, McAdam B, Morrison BW, Kapoor S, Kujubu D, Antes L, Lasseter KC, Quan H, Gertz BJ, FitzGerald GA. Effects of specific inhibition of cyclooxygenase-2 on sodium balance, hemodynamics, and vasoactive eicosanoids. J Pharmacol Exp Ther. 1999;289:735-741.
34. Yu Y, Ricciotti E, Scalia R, Tang S, Grant G, Yu Z, Landesberg G, Crichton I, Wu W, Puré E, Funk C, FitzGerald G. Vascular COX-2 modulates blood pressure and thrombosis in mice. Sci Transl Med. 2012; 4:132ra154
35. McAdam BF, Catella-Lawson F, Mardini IA, Kapoor S, Lawson JA, FitzGerald GA. Systemic biosynthesis of prostacyclin by cyclooxygenase (COX)-2: the human pharmacology of a selective inhibitor of COX-2. Proc Natl Acad Sci USA. 1999;96:272-277.
36. Bao G, Metreveli N, Li R, Taylor A, Fletcher EC. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J Appl Physiol. 1997;83:95-101.
37. Fletcher EC, Orolinova N, Bader M. Blood pressure response to chronic episodic hypoxia: the renin-angiotensin system. J Appl Physiol. 2002;92:627-633.
38. Linz D, Hohl M, Nickel A, Mahfoud F, Wagner M, Ewen S, Schotten U, Maack C, Wirth K, Böhm M. Effect of renal denervation on neurohumoral activation triggering atrial fibrillation in obstructive sleep apnea. Hypertension. 2013;62:767-774.
39. Linz D, Mahfoud F, Schotten U, Ukena C, Neuberger HR, Wirth K, Bohm M. Renal sympathetic denervation suppresses postapneic blood pressure rises and atrial fibrillation in a model for sleep apnea. Hypertension. 2012;60:172-178.
40. Pialoux V, Foster GE, Ahmed SB, Beaudin AE, Hanly PJ, Poulin MJ. Losartan abolishes oxidative stress induced by intermittent hypoxia in humans. J Physiol. 2011;589:5529-5537.
41. Rajagopalan S, Kurz S, Munzel T, TarpeyM, Freeman BA, Griendling KK, Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane nadh/nadph oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest. 1996;97:1916-1923.
42. Young W, Mahboubi K, Haider A, Li I, Ferreri NR. Cyclooxygenase-2 is required for tumor necrosis factor-α-and angiotensin II-mediated proliferation of vascular smooth muscle cells. Circ Res. 2000;86:906-914.
43. Hu ZW, Kerb R, Shi XY, Wei-Lavery T, Hoffman BB. Angiotensin II increases expression of cyclooxygenase-2: implications for the function of vascular smooth muscle cells. J Pharmacol Exp Ther. 2002;303:563-573.
44. Campbell WB, Graham RM, Jackson EK. Role of renal prostaglandins in sympathetically mediated renin relase in the rat. J Clin Invest. 1979;64:448-456.
45. Harris RC. Interactions between COX-2 and the renin-angiotensin system in the kidney. Acta Physiol Scand. 2003;177:423-427.
46. Hurwitz S, Cohen RJ, Williams GH. Diurnal variation of aldosterone and plasma renin activity: timing relation to melatonin and cortisol and consistency after prolonged bed rest. J Appl Physiol. 1985;2004:1406-1414.
47. Andresen J, Shafi NI, Bryan RM Jr. Endothelial influences on cerebrovascular tone. J Appl Physiol. 2006;100:318-327.
48. Osuka K, Suzuki Y, Watanabe Y, Dogan A, Takayasu M, Shibuya M, Yoshida J. Vasodilator effects on canine basilar artery induced by intracisternal interleukin-1 beta. J Cereb Blood Flow Metab. 1997;17:1337-1345.
49. Nadjar A, Tridon V, May MJ, Ghosh S, Dantzer R, Amedee T, Parnet P. NFkappaB activates in vivo the synthesis of inducible cox-2 in the brain. J Cereb Blood Flow Metab. 2005;25:1047-1059.
50. Rivest S. What is the cellular source of prostaglandins in the brain in response to systemic inflammation? Facts and controversies. Mol Psychiatry. 1999;4:500-507.
51. Ryan S, Taylor CT, McNicholas WT. Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation. 2005;112:2660-2667.
52. FitzGerald GA, Patrono C. The coxibs, selective inhibitors of cyclooxygenase-2. N Engl J Med. 2001;345:433-442.
53. Mitchell JA, Akarasereenont P, Thiemermann C, Flower RJ, Vane JR. Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc Natl Acad Sci USA. 1993;90:11693-11697.
54. Capra V, Back M, Barbieri SS, Camera M, Tremoli E, Rovati GE. Eicosanoids and their drugs in cardiovascular diseases: focus on atherosclerosis and stroke. Med Res Rev. 2013;33:364-438.
55. Krieger J, Benzoni D, Sforza E, Sassard J. Urinary excretion of prostanoids during sleep in obstructive sleep apnoea patients. Clin Exp Pharmacol Physiol. 1991;18:551-555.
56. Kimura H, Niijima M, Abe Y, Edo H, Sakabe H, Kojima A, Hasako K, Masuyama S, Tatsumi K, Kuriyama T. Compensatory excretion of prostacyclin and thromboxane metabolites in obstructive sleep apnea syndrome. Intern Med. 1998;37:127-133.
57. Somers VK, Dyken ME, Clary MP, Abboud FM. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest. 1995;96:1897-1904.
58. Neri Serneri GG, Gensini GF, Abbate R, Prisco D, Rogasi PG, Castellani S, Casolo GC, Matucci M, Fantini F, Donato MD, Dabizzi RP. Spontaneous and cold pressor test-induced prostaglandin biosynthesis by human heart. Am Heart J. 1985; 110:50-55
59. Neri Serneri GG, Castellani S, Scarti L, Trotta F, Chen JL, Carnovali M, Poggesi L, Masotti G. Repeated sympathetic stimuli elicit the decline and disappearance of prostaglandin modulation and an increase of vascular resistance in humans. Circ Res. 1990; 67:580-588
60. Morgan BJ, Denahan T, Ebert TJ. Neurocirculatory consequences of negative intrathoracic pressure vs. asphyxia during voluntary apnea. J Appl Physiol. 1993;74:2969-2975.
61. Fletcher EC, Lesske J, Qian W, Miller CC III, Unger T. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension. 1992;19:555-561.
62. Tamisier R, Gilmartin GS, Launois SH, Pepin JL, Nespoulet H, Thomas R, Levy P, Weiss JW. A new model of chronic intermittent hypoxia in humans: effect on ventilation, sleep, and blood pressure. J Appl Physiol. 2009;107:17-24.
63. Hinojosa-Laborde C, Mifflin SW. Sex differences in blood pressure response to intermittent hypoxia in rats. Hypertension. 2005;46:1016-1021.
64. Warner TD, Mitchell JA. Cox-2 selectivity alone does not define the cardiovascular risks associated with non-steroidal anti-inflammatory drugs. Lancet. 2008;371:270-273.