Mechanisms of sympathetic activation and blood pressure elevation by intermittent hypoxia

Respiratory Physiology and Neurobiology

Volumn 174, Issue 1-2, 2010, Pages 156-161

  Prabhakar, Nanduri R ^a   Kumar, Ganesh K ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Apneas; Baro receptors; Carotid body; Hypoxia; Sleep apneas; Vasoactive mediators

Indexed keywords

APNEA; CHEMORECEPTOR REFLEX; COMORBIDITY; HUMAN; HYPERTENSION; HYPOXIA; PREMATURITY; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; REVIEW; SLEEP DISORDERED BREATHING; SYMPATHETIC TONE;

ANIMALS; ANOXIA; BAROREFLEX; BLOOD PRESSURE; CAROTID BODY; CATECHOLAMINES; DISEASE MODELS, ANIMAL; ENDOTHELINS; HUMANS; HYPERTENSION; RENIN-ANGIOTENSIN SYSTEM; SLEEP APNEA SYNDROMES; SYMPATHETIC NERVOUS SYSTEM;

EID: 78049387065     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2010.08.021     Document Type: Review

References (61)

1. Allahdadi K.J., Cherng T.W., Pai H., Silva A.Q., Walker B.R., Nelin L.D., Kanagy N.L. Endothelin type A receptor antagonist normalizes blood pressure in rats exposed to eucapnic intermittent hypoxia. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H434-H440.
2. Bao G., Metreveli N., Li R., Taylor A., Fletcher E.C. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J. Appl. Physiol. 1997, 83:95-101.
3. Bonsignore M.R., Parati G., Insalaco G., Marrone O., Castiglioni P., Romano S., Di Rienzo M., Mancia G., Bonsignore G. Continuous positive airway pressure treatment improves baroreflex control of heart rate during sleep in severe obstructive sleep apnea syndrome. Am. J. Respir. Crit. Care Med. 2002, 166:279-286.
4. Braga V.A., Soriano R.N., Machado B.H. Sympathoexcitatory response to peripheral chemoreflex activation is enhanced in juvenile rats exposed to chronic intermittent hypoxia. Exp. Physiol. 2006, 91:1025-1031.
5. Carlson J.T., Hedner J.A., Elam M., Ejnell H., Sellgren J., Wallin G. Augmented resting sympathetic activity in awake patients with obstructive sleep apnea. Chest 1993, 103:1763-1768.
6. Cooper V.L., Elliott M.W., Pearson S.B., Taylor C.M., Mohammed M.M., Hainsworth R. Daytime variability of baroreflex function in patients with obstructive sleep apnoea: implications for hypertension. Exp. Physiol. 2007, 92:391-398.
7. Cutler M.J., Swift N.M., Keller D.M., Wasmund W.L., Smith M.L. Hypoxia-mediated prolonged elevation of sympathetic nerve activity after periods of intermittent hypoxic apnea. J. Appl. Physiol. 2004, 96:754-761.
8. Dick T.E., Hsieh Y.H., Wang N., Prabhakar N.R. Acute intermittent hypoxia increases both phrenic and sympathetic nerve activities in the rat. Exp. Physiol. 2007, 92:87-97.
9. Fletcher E.C. Physiological consequences of intermittent hypoxia: systemic blood pressure. J. Appl. Physiol. 2001, 90:1600-1605.
10. Fletcher E.C., Miller J., Schaaf J.W., Fletcher J.G. Urinary catecholamines before and after tracheostomy in patients with obstructive sleep apnea and hypertension. Sleep 1987, 10:35-44.
11. Fletcher E.C., Orolinova N., Bader M. Blood pressure response to chronic episodic hypoxia: the renin-angiotensin system. J. Appl. Physiol. 2002, 92:627-633.
12. Garcia-Rio F., Racionero M.A., Pino J.M., Martinez I., Ortuno F., Villasante C., Villamor J. Sleep apnea and hypertension. Chest 2000, 117:1417-1425.
13. Gjorup P.H., Sadauskiene L., Wessels J., Nyvad O., Strunge B., Pedersen E.B. Abnormally increased endothelin-1 in plasma during the night in obstructive sleep apnea: relation to blood pressure and severity of disease. Am. J. Hypertens. 2007, 20:44-52.
14. Greenberg H.E., Sica A., Batson D., Scharf S.M. Chronic intermittent hypoxia increases sympathetic responsiveness to hypoxia and hypercapnia. J. Appl. Physiol. 1999, 86:298-305.
15. Grimpen F., Kanne P., Schulz E., Hagenah G., Hasenfuss G., Andreas S. Endothelin-1 plasma levels are not elevated in patients with obstructive sleep apnoea. Eur. Respir. J. 2000, 15:320-325.
16. Gu H., Lin M., Liu J., Gozal D., Scrogin K.E., Wurster R.D., Chapleau M.W., Ma X., Cheng Z.J. Selective impairment of central mediation of baroreflex in anesthetized young-adult Fischer 344 rats following chronic intermittent hypoxia. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2809-H2818.
17. Hedner J.A., Ejnell H., Sellgren J., Hedner T., Wallin G. Is high and fluctuating muscle nerve sympathetic activity in the sleep apnoea syndrome of pathogenetic importance for the development of hypertension?. J. Hypertens. (Suppl.) 1988, 6:5529-5531.
18. Hedner J.A., Wilcox I., Laks L., Grunstein R.R., Sullivan C.E. A specific and potent pressor effect of hypoxia in patients with sleep apnea. Am. Rev. Respir. Dis. 1992, 146:1240-1245.
19. Hornyak M., Cejnar M., Elam M., Matousek M., Wallin B.G. Sympathetic muscle nerve activity during sleep in man. Brain 1991, 114(Pt 3):1281-1295.
20. Howard P.G., Plumpton C., Davenport A.P. Anatomical localization and pharmacological activity of mature endothelins and their precursors in human vascular tissue. J. Hypertens. 1992, 10:1379-1386.
21. Huang J., Lusina S., Xie T., Ji E., Xiang S., Liu Y., Weiss J.W. Sympathetic response to chemostimulation in conscious rats exposed to chronic intermittent hypoxia. Respir. Physiol. Neurobiol. 2009, 166:102-106.
22. Imadojemu V.A., Mawji Z., Kunselman A., Gray K.S., Hogeman C.S., Leuenberger U.A. Sympathetic chemoreflex responses in obstructive sleep apnea and effects of continuous positive airway pressure therapy. Chest 2007, 131:1406-1413.
23. Jordan W., Reinbacher A., Cohrs S., Grunewald R.W., Mayer G., Rüther E., Rodenbeck A. Obstructive sleep apnea: plasma endothelin-1 precursor but not endothelin-1 levels are elevated and decline with nasal continuous positive airway pressure. Peptides 2005, 26:1654-1660.
24. Kanagy N.L., Walker B.R., Nelin L.D. Role of endothelin in intermittent hypoxia-induced hypertension. Hypertension 2001, 37:511-515.
25. Kumar G.K., Rai V., Sharma S.D., Ramakrishnan D.P., Peng Y.J., Souvannakitti D., Prabhakar N.R. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. J. Physiol. 2006, 575:229-239.
26. Kuri B.A., Khan S.A., Chan S.A., Prabhakar N.R., Smith C.B. Increased secretory capacity of mouse adrenal chromaffin cells by chronic intermittent hypoxia: involvement of protein kinase C. J. Physiol. 2007, 584:313-319.
27. Lai C.J., Yang C.C., Hsu Y.Y., Lin Y.N., Kuo T.B. Enhanced sympathetic outflow and decreased baroreflex sensitivity are associated with intermittent hypoxia-induced systemic hypertension in conscious rats. J. Appl. Physiol. 2006, 100:1974-1982.
28. Leuenberger U., Jacob E., Sweer L., Waravdekar N., Zwillich C., Sinoway L. Surges of muscle sympathetic nerve activity during obstructive apnea are linked to hypoxemia. J. Appl. Physiol. 1995, 79:581-588.
29. Lusina S.J., Kennedy P.M., Inglis J.T., McKenzie D.C., Ayas N.T., Sheel A.W. Long-term intermittent hypoxia increases sympathetic activity and chemosensitivity during acute hypoxia in humans. J. Physiol. 2006, 575(Pt 3):961-970.
30. 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.
31. Marrone O., Riccobono L., Salvaggio A., Mirabella A., Bonanno A., Bonsignore M.R. Catecholamines and blood pressure in obstructive sleep apnea syndrome. Chest 1993, 103:722-727.
32. 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.
33. Monahan K.D., Leuenberger U.A., Ray C.A. Effect of repetitive hypoxic apnoeas on baroreflex function in humans. J. Physiol. 2006, 574(Pt 2):605-613.
34. Morgan B.J., Crabtree D.C., Palta M., Skatrud J.B. Combined hypoxia and hypercapnia evokes long-lasting sympathetic activation in humans. J. Appl. Physiol. 1995, 79:205-213.
35. Narkiewicz K., Somers V.K. The sympathetic nervous system and obstructive sleep apnea: implications for hypertension. J. Hypertens. 1997, 15:1613-1619.
36. Narkiewicz K., van de Borne P.J., Montano N., Dyken M.E., Phillips B.G., Somers V.K. Contribution of tonic chemoreflex activation to sympathetic activity and blood pressure in patients with obstructive sleep apnea. Circulation 1998, 97:943-945.
37. Okada H., Iwase S., Mano T., Sugiyama Y., Watanabe T. Changes in muscle sympathetic nerve activity during sleep in humans. Neurology 1991, 41:1961-1966.
38. Pawar A., Nanduri J., Yuan G., Khan S.A., Wang N., Kumar G.K., Prabhakar N.R. Reactive oxygen species-dependent endothelin signaling is required for augmented hypoxic sensory response of the neonatal carotid body by intermittent hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R735-R742.
39. 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.
40. Peng Y.J., Yuan G., Ramakrishnan D., Sharma S.D., Bosch-Marce M., Kumar G.K., Semenza G.L., Prabhakar N.R. Heterozygous HIF-1alpha deficiency impairs carotid body-mediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia. J. Physiol. 2006, 577:705-716.
41. Peng Y.J., Nanduri J., Yuan G., Wang N., Deneris E., Pendyala S., Natarajan V., Kumar G.K., Prabhakar N.R. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J. Neurosci. 2009, 29:4903-4910.
42. Peng Y.J., Raghuraman G., Wang N., Nanduri J., Kumar G.K., Prabhakar N.R. Up-regulation of endothelin-1 mediates chronic intermittent hypoxia-evoked down-regulation of carotid baro-receptor activity. Am. J. Respir. Crit. Care Med. 2010, 181:A4198.
43. 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.
44. Phillips B.G., Narkiewicz K., Pesek C.A., Haynes W.G., Dyken M.E., Somers V.K. Effects of obstructive sleep apnea on endothelin-1 and blood pressure. J. Hypertens. 1999, 17:61-66.
45. Prabhakar N.R. Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J. Appl. Physiol. 2001, 90:1986-1994.
46. Prabhakar N.R., Peng Y.J. Effect of two paradigms of chronic intermittent hypoxia on carotid body sensory activity. J. Appl. Physiol. 2004, 96:1236-1242.
47. Prabhakar N.R., Dick T.E., Nanduri J., Kumar G.K. Systemic, cellular and molecular analysis of chemoreflex-mediated sympathoexcitation by chronic intermittent hypoxia. Exp. Physiol. 2007, 92:39-44.
48. Prabhakar N.R., Peng Y.J., Jacono F.J., Kumar G.K., Dick T.E. Cardiovascular alterations by chronic intermittent hypoxia: importance of carotid body chemoreflexes. Clin. Exp. Pharmacol. Physiol. 2005, 32:447-449.
49. Rey S., Del Rio R., Alcayaga J., Iturriaga R. Chronic intermittent hypoxia enhances cat chemosensory and ventilatory responses to hypoxia. J. Physiol. 2004, 560(Pt 2):577-586.
50. Rey S., Del Rio R., Iturriaga R. Contribution of endothelin-1 to the enhanced carotid body chemosensory responses induced by chronic intermittent hypoxia. Brain Res. 2006, 1086:152-159.
51. Saarelainen S., Seppala E., Laasonen K., Hasan J. Circulating endothelin-1 in obstructive sleep apnea. Endothelium 1997, 5:115-118.
52. Sica A.L., Greenberg H.E., Ruggiero D.A., Scharf S.M. Chronic-intermittent hypoxia: a model of sympathetic activation in the rat. Respir. Physiol. 2000, 121:173-184.
53. Smith M.L., Niedermaier O.N., Hardy S.M., Decker M.J., Strohl K.P. Role of hypoxemia in sleep apnea-induced sympathoexcitation. J. Auton. Nerv. Syst. 1996, 56:184-190.
54. Somers V.K., Dyken M.E., Mark A.L., Abboud F.M. Sympathetic-nerve activity during sleep in normal subjects. N. Engl. J. Med. 1993, 328:303-307.
55. 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.
56. Souvannakitti D., Kumar G.K., Fox A., Prabhakar N.R. Neonatal intermittent hypoxia leads to long-lasting facilitation of acute hypoxia-evoked catecholamine secretion from rat chromaffin cells. J. Neurophysiol. 2009, 101:2837-2846.
57. 2+ channels and ryanodine receptors mediate the augmented exocytosis of catecholamines from intermittent hypoxia treated neonatal rat chromaffin cells. J. Neurosci. 2010, 30:10763-10772.
58. Suzuki M., Otsuka K., Guilleminault C. Long-term nasal continuous positive airway pressure administration can normalize hypertension in obstructive sleep apnea patients. Sleep 1993, 16:545-549.
59. 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.
60. Zamarron-Sanz C., Ricoy-Galbaldon J., Gude-Sampedro F., Riveiro-Riveiro A. Plasma levels of vascular endothelial markers in obstructive sleep apnea. Arch. Med. Res. 2006, 37:552-555.
61. Zoccal D.B., Simms A.E., Bonagamba L.G., Braga V.A., Pickering A.E., Paton J.F., Machado B.H. Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J. Physiol. 2008, 586:3253-3265.