Angiotensin II type 1a receptors in subfornical organ contribute towards chronic intermittent hypoxia-associated sustained increase in mean arterial pressure

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 5, 2015, Pages H435-H446

  Saxena, Ashwini ^a   Little, Joel T ^a   Nedungadi, T Prashant ^a   Cunningham, J Thomas ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Angiotensin receptor; AT1aR; Chronic intermittent hypoxia; Obstructive sleep apnea; Subfornical organ

Indexed keywords

ANGIOTENSIN 1A RECEPTOR; GREEN FLUORESCENT PROTEIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR FOSB; ANGIOTENSIN 1 RECEPTOR;

ADENO ASSOCIATED VIRUS; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING RATE; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; FOREBRAIN; GENETIC CODE; HEART RATE; HYPERTENSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PREOPTIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEREOTAXIS; SUBFORNICAL ORGAN; TELEMETRY; ANIMAL; ANOXIA; BLOOD PRESSURE; COMPLICATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; SLEEP DISORDERED BREATHING; SPRAGUE DAWLEY RAT;

ANIMALS; ANOXIA; BLOOD PRESSURE; HYPERTENSION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; SLEEP APNEA SYNDROMES; SUBFORNICAL ORGAN;

EID: 84965191111     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00747.2014     Document Type: Article

References (55)

1. Allen AM. Angiotensin AT1 receptor-mediated excitation of rat carotid body chemoreceptor afferent activity. J Physiol 510: 773–781, 1998.
2. Aschauer DF, Kreuz S, Rumpel S. Analysis of transduction efficiency, tropism and axonal transport ofAAVserotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLos One 8: e76310. doi:10.1371/journal.pone.0076310.eCollection0072013, 2013.
3. Bartlett JS, Samulski RJ, McCown TJ. Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther 9: 1181–1186, 1998.
4. Carlson JT, Hedner J, Elam M, Ejnell H, Sellgren J, Wallin BG. Augmented resting sympathetic activity in awake patients with obstructive sleep apnea. Chest 103: 1763–1768, 1993.
5. Carreno FR, Walch JD, Dutta M, Nedungadi TP, Cunningham JT. Brain-derived neurotrophic factor-tyrosine kinase B pathway mediates NMDA receptor NR2B subunit phosphorylation in the supraoptic nuclei following progressive dehydration. J Neuroendocrinol 23: 894–905, 2011.
6. Ciriello J, Rosas-Arellano MP, Solano-Flores LP. Direct projections to subfornical organ from catecholaminergic neurons in the caudal nucleus of the solitary tract. Brain Res 726: 227–232, 1996.
7. Cunningham JT, Knight WD, Mifflin SW, Nestler EJ. An essential role for DeltaFosB in the median preoptic nucleus in the sustained hypertensive effects of chronic intermittent hypoxia. Hypertension 60: 179–187, 2012.
8. Cunningham JT, Nedungadi TP, Walch JD, Nestler EJ, Gottlieb HB. DeltaFosB in the supraoptic nucleus contributes to hyponatremia in rats with cirrhosis. Am J Physiol Regul Integr Comp Physiol 303: R177–R185, 2012
9. da Silva AQ, Fontes MA, Kanagy NL. Chronic infusion of angiotensin receptor antagonists in the hypothalamic paraventricular nucleus prevents hypertension in a rat model of sleep apnea. Brain Res 1368: 231–238, 2011
10. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International Union of Pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52: 415–472, 2000.
11. Dempsey JA, Veasey SC, Morgan BJ, O’Donnell CP. Pathophysiology of sleep apnea. Physiol Rev 90: 47–112, 2010.
12. Dernaika TA, Kinasewitz GT, Tawk MM. Effects of nocturnal continuous positive airway pressure therapy in patients with resistant hypertension and obstructive sleep apnea. J Clin Sleep Med 5: 103–107, 2009.
13. Ferguson AV, Bains JS. Electrophysiology of the circumventricular organs. Front Neuroendocrinol 17: 440–475, 1996.
14. Fletcher EC. Effect of episodic hypoxia on sympathetic activity and blood pressure. Respir Physiol 119: 189–197, 2000.
15. Fletcher EC. Physiological consequences of intermittent hypoxia: systemic blood pressure. J Appl Physiol 90: 1600–1605, 2001.
16. Fletcher EC, Bao G, Li R. Renin activity and blood pressure in response to chronic episodic hypoxia. Hypertension 34: 309–314, 1999.
17. Fletcher EC, Lesske J, Qian W, Miller CC 3rd, Unger T. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension 19: 555–561, 1992.
18. Fletcher EC, Orolinova N, Bader M. Blood pressure response to chronic episodic hypoxia: the renin-angiotensin system. J Appl Physiol 92: 627–633, 2002.
19. Gonzaga CC, Gaddam KK, Ahmed MI, Pimenta E, Thomas SJ, Harding SM, Oparil S, Cofield SS, Calhoun DA. Severity of obstructive sleep apnea is related to aldosterone status in subjects with resistant hypertension. J Clin Sleep Med 6: 363–368, 2010.
20. Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, Cunningham JT. Differential effects of water and saline intake on water deprivationinduced c-Fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 290: R1251–R1261, 2006.
21. Grobe JL, Xu D, Sigmund CD. An intracellular renin-angiotensin system in neurons: fact, hypothesis, or fantasy. Physiology 23: 187–193, 2008.
22. Hein L. Genetic deletion and overexpression of angiotensin II receptors. J Mol Med 76: 756–763, 1998.
23. Hendel MD, Collister JP. Contribution of the subfornical organ to angiotensin II-induced hypertension. Am J Physiol Heart Circ Physiol 288: H680–H685, 2005.
24. Iwai N, Inagami T. Identification of two subtypes in the rat type I angiotensin II receptor. FEBS Lett 298: 257–260, 1992.
25. Knight WD, Little JT, Carreno FR, Toney GM, Mifflin SW, Cunningham JT. Chronic intermittent hypoxia increases blood pressure and expression of FosB/ΔFosB in central autonomic regions. Am J Physiol Regul Integr Comp Physiol 301: R131–R139, 2011.
26. Knight WD, Saxena A, Shell B, Nedungadi TP, Mifflin SW, Cunningham JT. Central losartan attenuates increases in arterial pressure and expression of FosB/ΔFosB along the autonomic axis associated with chronic intermittent hypoxia. Am J Physiol Regul Integr Comp Physiol 305: R1051–R1058, 2013.
27. Lam SY, Liu Y, Ng KM, Liong EC, Tipoe GL, Leung PS, Fung ML. Upregulation of a local renin-angiotensin system in the rat carotid body during chronic intermittent hypoxia. Exp Physiol 99: 220–231, 2014.
28. Marcus NJ, Li YL, Bird CE, Schultz HD, Morgan BJ. Chronic intermittent hypoxia augments chemoreflex control of sympathetic activity: role of the angiotensin II type 1 receptor. Respir Physiol Neurobiol 171: 36–45, 2010.
29. Marcus NJ, Philippi NR, Bird CE, Li YL, Schultz HD, Morgan BJ. Effect of AT 1 receptor blockade on intermittent hypoxia-induced endothelial dysfunction. Respir Physiol Neurobiol 183: 67–74, 2012.
30. McKinley MJ, Albiston AL, Allen AM, Mathai ML, May CN, McAllen RM, Oldfield BJ, Mendelsohn FA, Chai SY. The brain renin-angiotensin system: location and physiological roles. Int J Biochem Cell Biol 35: 901–918, 2003.
31. Miselis RR, Shapiro RE, Hand PJ. Subfornical organ efferents to neural systems for control of body water. Science 205: 1022–1025, 1979.
32. Narkiewicz K, Kato M, Phillips BG, Pesek CA, Davison DE, Somers VK. Nocturnal continuous positive airway pressure decreases daytime sympathetic traffic in obstructive sleep apnea. Circulation 100: 2332–2335, 1999.
33. Narkiewicz K, Somers VK. Sympathetic nerve activity in obstructive sleep apnoea. Acta Physiol Scand 177: 385–390, 2003.
34. Nedungadi TP, Carreno FR, Walch JD, Bathina CS, Cunningham JT. Region-specific changes in transient receptor potential vanilloid channel expression in the vasopressin magnocellular system in hepatic cirrhosisinduced hyponatraemia. J Neuroendocrinol 24: 642–652, 2012.
35. Nedungadi TP, Cunningham JT. Differential regulation of TRPC4 in the vasopressin magnocellular system by water deprivation and hepatic cirrhosis in the rat. Am J Physiol Regul Integr Comp Physiol 306: R304–R314, 2014.
36. Nedungadi TP, Dutta M, Bathina CS, Caterina MJ, Cunningham JT. Expression and distribution of TRPV2 in rat brain. Exp Neurol 237: 223–237, 2012.
37. Okcay A, Somers VK, Caples SM. Obstructive sleep apnea and hypertension. J Clin Hypertens (Greenwich) 10: 549–555, 2008.
38. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1997.
39. Peng YJ, Overholt JL, Kline D, Kumar GK, Prabhakar NR. Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc Natl Acad Sci USA 100: 10073–10078, 2003.
40. Peng YJ, Prabhakar NR. Effect of two paradigms of chronic intermittent hypoxia on carotid body sensory activity. J Appl Physiol 96: 1236–1242; discussion 1196, 2004.
41. Prabhakar NR, Jacono FJ. Cellular and molecular mechanisms associated with carotid body adaptations to chronic hypoxia. High Alt Med Biol 6: 112–120, 2005.
42. Prabhakar NR, Kumar GK. Mechanisms of sympathetic activation and blood pressure elevation by intermittent hypoxia. Respir Physiol Neurobiol 174: 156–161, 2010.
43. Sakai K, Agassandian K, Morimoto S, Sinnayah P, Cassell MD, Davisson RL, Sigmund CD. Local production of angiotensin II in the subfornical organ causes elevated drinking. J Clin Invest 117: 1088–1095, 2007.
44. Salegio EA, Samaranch L, Kells AP, Mittermeyer G, San Sebastian W, Zhou S, Beyer J, Forsayeth J, Bankiewicz KS. Axonal transport of adeno-associated viral vectors is serotype-dependent. Gene Ther 20: 348–352, 2013.
45. Simpson JB, Routtenberg A. Subfornical organ: site of drinking elicitation by angiotensin II. Science 181: 1172–1175, 1973.
46. Sinnayah P, Lazartigues E, Sakai K, Sharma RV, Sigmund CD, Davisson RL. Genetic ablation of angiotensinogen in the subfornical organ of the brain prevents the central angiotensinergic pressor response. Circ Res 99: 1125–1131, 2006.
47. Sinnayah P, Lindley TE, Staber PD, Cassell MD, Davidson BL, Davisson RL. Selective gene transfer to key cardiovascular regions of the brain: comparison of two viral vector systems. Hypertension 39: 603–608, 2002.
48. Sinnayah P, Lindley TE, Staber PD, Davidson BL, Cassell MD, Davisson RL. Targeted viral delivery of Cre recombinase induces conditional gene deletion in cardiovascular circuits of the mouse brain. Physiol Genomics 18: 25–32, 2004.
49. Stocker SD, Cunningham JT, Toney GM. Water deprivation increases Fos immunoreactivity in PVN autonomic neurons with projections to the spinal cord and rostral ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 287: R1172–R1183, 2004.
50. Stocker SD, Hunwick KJ, Toney GM. Hypothalamic paraventricular nucleus differentially supports lumbar and renal sympathetic outflow in water-deprived rats. J Physiol 563: 249–263, 2005.
51. Thomas WG, Qian H, Smith NJ. When 6 is 9: “uncoupled” AT1 receptors turn signalling on its head. Cell Mol Life Sci 61: 2687–2694, 2004.
52. Thomopoulos C, Michalopoulou H, Kasiakogias A, Kefala A, Makris T. Resistant hypertension and obstructive sleep apnea: the sparring partners. Int J Hypertens 2011: 947246, 2011.
53. Weisinger RS, Denton DA, Di Nicolantonio R, Hards DK, McKinley MJ, Oldfield B, Osborne PG. Subfornical organ lesion decreases sodium appetite in the sodium-depleted rat. Brain Res 526: 23–30, 1990.
54. Yuan ZM, Chen BY, Wang PX, Li SY, Chen YL, Dong LX. [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 27: 577–580, 2004.
55. Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 95: 210–216, 2004.