Exercise training normalizes the blunted central component of the baroreflex in rats with heart failure: Role of the PVN

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 2, 2013, Pages

  Patel, Kaushik P ^a   Salgado, Helio C ^b   Liu, Xuefei ^a   Zheng, Hong ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

aminobutyric acid receptor; Aortic depressor nerve; Blood pressure; Paraventricular nucleus; Sympathetic outflow

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; BICUCULLINE;

AORTA NERVE; ARTICLE; EXERCISE; HEART FAILURE; HEART RATE; MEAN ARTERIAL PRESSURE; NERVE STIMULATION; PARAVENTRICULAR THALAMIC NUCLEUS; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYMPATHETIC NERVE;

Γ-AMINOBUTYRIC ACID RECEPTOR; AORTIC DEPRESSOR NERVE; BLOOD PRESSURE; PARAVENTRICULAR NUCLEUS; SYMPATHETIC OUTFLOW;

ANIMALS; ARTERIAL PRESSURE; BAROREFLEX; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EXERCISE THERAPY; GABA ANTAGONISTS; HEART FAILURE; HEART RATE; HEMODYNAMICS; KIDNEY; MALE; MICROINJECTIONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECOVERY OF FUNCTION; REFLEX, ABNORMAL; SEDENTARY LIFESTYLE; SYMPATHETIC NERVOUS SYSTEM; TIME FACTORS;

EID: 84880173126     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00009.2013     Document Type: Article

References (53)

1. Barrett CJ, Guild SJ, Ramchandre R, Malpas SC. Baroreceptor denervation prevents sympathoinhibition during angiotensin II-induced hypertension. Hypertension 46: 168-172, 2005.
2. Bennett T, Gardiner SM. Involvement of vasopressin in cardiovascular regulation. Cardiovasc Res 19: 57-68, 1985.
3. Brändle M, Patel KP, Wang W, Zucker IH. Hemodynamic and norepinephrine responses to pacing-induced heart failure in conscious sinoaorticdenervated dogs. J Appl Physiol 81: 1855-1862, 1996.
4. Claassen DE, Morgan DA, Hirai T, Kenney MJ. Nonuniform sympathetic nerve responses after sustained elevation in arterial pressure. Am J Physiol Regul Integr Comp Physiol 271: R1264-R1269, 1996.
5. Cowley AWJ, Guyton AC. Baroreceptor reflex effects on transient and steady-state hemodynamics of salt-loading hypertension in dogs. Circ Res 36: 536-546, 1975.
6. Diz DI, Garcia-Espinosa MA, Gegick S, Tommasi EN, Ferrario CM, Ann Tallant E, Chappell MC, Gallagher KP. Injections of angiotensinconverting enzyme 2 inhibitor MLN4760 into nucleus tractus solitarii reduce baroreceptor reflex sensitivity for heart rate control in rats. Exp Physiol 93: 694-700, 2008.
7. Feng Y, Yue X, Xia H, Bindom SM, Hickman PJ, Filipeanu CM, Wu G, Lazartigues E. Angiotensin-converting enzyme 2 overexpression in the subfornical organ prevents the angiotensin II-mediated pressor and drinking responses and is associated with angiotensin II type 1 receptor downregulation. Circ Res 102: 729-736, 2008.
8. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Sympathoexcitation by central ANG II: roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. Am J Physiol Heart Circ Physiol 288: H2271-H2279, 2005.
9. Guo GB, Abboud FM. Angiotensin II attenuates baroreflex control of heart rate and sympathetic activity. Am J Physiol Heart Circ Physiol 246: H80-H89, 1984.
10. Haselton JR, Goering J, Patel KP. Parvocellular neurons of the paraventricular nucleus are involved in the reduction in renal nerve discharge during isotonic volume expansion. J Auton Nerv Syst 50: 1-11, 1994.
11. Hasser EM, Bishop VS, Hay M. Interactions between vasopressin and baroreflex control of the sympathetic nervous system. Clin Exp Pharmacol Physiol 24: 102-108, 1997.
12. Huang R, Dillon G. Functional characterization of GABAA receptors in neonatal hypothalamic brain slice. Neuroscience 88: 1655-1663, 2002.
13. Iellamo F, Legramante JM, Massaro M, Raimondi G, Galante A. Effects of a residential exercise training on baroreflex sensitivity and heart rate variability in patients with coronary artery disease: a randomized, controlled study. Circulation 102: 2588-2592, 2000.
14. Jung R, Dibner-Dunlap ME, Gilles MA, Thames MD. Cardiorespiratory reflex control in rats with left ventricular dysfunction. Am J Physiol Heart Circ Physiol 268: H218-H225, 1995.
15. Kajekar R, Chen CY, Mutoh T, Bonham AC. GABAA receptor activation at medullary sympathetic neurons contributes to postexercise hypotension. Am J Physiol Heart Circ Physiol 282: H1615-H1624, 2002.
16. Kannan H, Yamashita H. Connections of neurons in the region of the nucleus tractus solitarius with the hypothalamic paraventricular nucleus: their possible involvement in neural control of the cardiovascular system in rats. Brain Res 329: 205-212, 1985.
17. Kar S, Gao L, Zucker IH. Exercise training normalizes ACE and ACE2 in the brain of rabbits with pacing-induced heart failure. J Appl Physiol 108: 923-932, 2010.
18. Kleiber AC, Zheng H, Schultz HD, Peuler JD, Patel KP. Exercise training normalizes enhanced glutamate-mediated sympathetic activation from the PVN in heart failure. Am J Physiol Regul Integr Comp Physiol 294: R1863-R1872, 2008.
19. Komine H, Sugawara J, Hayashi K, Yoshizawa M, Yokoi T. Regular endurance exercise in young men increases arterial baroreflex sensitivity through neural alteration of baroreflex arc. J Appl Physiol 106: 1499-1505, 2009.
20. Krieger EM, Da Silva GJ, Negrao CE. Effects of exercise training on baroreflex control of the cardiovascular system. Ann NY Acad Sci 940: 338-347, 2001.
21. La Rovere MT, Bersano C, Gnemmi M, Specchia G, Schwartz PJ. Exercise-induced increase in baroreflex sensitivity predicts improved prognosis after myocardial infarction. Circulation 106: 945-949, 2002.
22. Levett JM, Marinelli CC, Lund DD, Pardini BJ, Nader S, Scott BD, Augelli NV, Kerber RE, Schmid PG Jr. Effects of β-blockade on neurohumoral responses and neurochemical markers in pacing-induced heart failure. Am J Physiol Heart Circ Physiol 266: H468-H475, 1994.
23. Liu JL, Irvine S, Reid IA, Patel KP, Zucker IH. Chronic exercise reduces sympathetic nerve activity in rabbits with pacing-induced heart failure-a role for angiotensin II. Circulation 102: 1854-1862, 2000.
24. Liu JL, Kulakofsky J, Zucker IH. Exercise training enhances baroreflex control of heart rate by a vagal mechanism in rabbits with heart failure. J Appl Physiol 92: 2403-2408, 2002.
25. Lovick TA, Coote JH. Electrophysiological properties of paraventriculospinal neurones in the rat. Brain Res 454: 123-130, 1988.
26. Lovick TA, Malpas S, Mahoney MT. Renal vasodilatation in respone to acute volume load is attenuated following lesions of parvocellular neurones in the paraventricular nucleus in rats. J Auton Nerv Syst 43: 247-256, 1993.
27. McDonald MP, Sanfilippo AJ, Savard GK. Baroreflex function and cardiac structure with moderate endurance training in normotensive men. J Appl Physiol 74: 2469-2477, 1993.
28. Musch TI, Terrell JA. Skeletal muscle blood flow abnormalities in rats with a chronic myocardial infarction: rest and exercise. Am J Physiol Heart Circ Physiol 262: H411-H419, 1992.
29. O'Connor CM, Whellan DJ, Lee KL, Keteyian SJ, Cooper LS, Ellis SJ, Leifer ES, Kraus WE, Kitzman DW, Blumenthal JA, Rendall DS, Miller NH, Fleg JL, Schulman KA, McKelvie RS, Zannad F, Pina IL, Investigators HA. Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 301: 1439-1450, 2009.
30. Osbron JW, Jacob F, Guzman P. A neural set point for the long-term control of arterial pressure: beyond the arterial baroreceptor reflex. Am J Physiol Regul Integr Comp Physiol 288: R846-R855, 2005.
31. Packer M. Neurohormonal interactions and adaptations in congestive heart failure. Circulation 77: 721-730, 1988.
32. Page MC, Cassaglia PA, Brooks VL. GABA in the paraventricular nucleus tonically suppresses baroreflex function: alterations during pregnancy. Am J Physiol Regul Integr Comp Physiol 300: R1452-R1458, 2011.
33. Pan YX, Gao L, Wang WZ, Zheng H, Liu D, patel KP, Zucker IH, Wang W. Exercise training prevents arterial baroreflex dysfunction in rats treated with central angiotensin II. Hypertension 49: 519-527, 2007.
34. Patel KP. Role of paraventrivular nucleus in mediating sympathetic outflow in heart failure. Heart Failure Rev 5: 73-86, 2000.
35. Patel KP, Schmid PG. Role of the paraventricular nucleus (PVH) in baroreflex-mediated changes in lumbar sympathetic nerve activity and heart rate. J Auton Nerv Syst 22: 211-219, 1988.
36. Patel KP, Zhang PL, Krukoff TL. Alterations in brain hexokinase activity associated with heart failure in rats. Am J Physiol Regul Integr Comp Physiol 265: R923-R928, 1993.
37. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Orlando, FL: Academic, 1986.
38. Rondon E, Brasileiro-Santos MS, Moreira ED, Rondon MU, Mattos KC, Coelho MA, Silva GJ, Brum PC, Fiorino P, Irigoyen MC, Krieger EM, Middlekauff HR, Negrao CE. Exercise training improves aortic depressor nerve sensitivity in rats with ischemia-induced heart failure. Am J Physiol Heart Circ Physiol 291: H2801-H2806, 2006.
39. Roveda F, Middlekauff HR, Rondon MU, Reis SF, Souza M, Nastari L, Barretto AC, Krieger EM, Negrao CE. The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial. J Am Coll Cardiol 42: 854-860, 2003.
40. Shafton AD, Ryan A, Badoer E. Neurons in the hypothalamic paraventricular nucleus send collaterals to the spinal cord and to the rostral ventrolateral medulla in the rat. Brain Res 801: 239-243, 1998.
41. Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD. A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res 491: 156-162, 1989.
42. Sun SY, Wang W, Zucker IH, Schultz HD. Enhanced activity of carotid body chemoreceptors in rabbits with heart failure: role of nitric oxide. J Appl Physiol 86: 1273-1282, 1999.
43. Vahid-Ansari F, Leenen FHH. Pattern of neuronal activation in rats with CHF after myocardial infarction. Am J Physiol Heart Circ Physiol 275: H2140-H2146, 1998.
44. Wang Y, Patel KP, Cornish KG, Channon KM, Zucker IH. nNOS gene transfer to RVLM improves baroreflex function in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 285: H1660-H1667, 2003.
45. Yamazato M, Yamazato Y, Sun C, Diez-Freire C, Raizada MK. Overexpression of angiotensin-converting enzyme 2 in the rostral ventrolateral medulla causes long-term decrease in blood pressure in the spontaneously hypertensive rats. Hypertension 49: 926-931, 2007.
46. Zhang K, Li YF, Patel KP. Reduced endogenous GABA-mediated inhibition in the PVN on renal nerve discharge in rats with heart failure. Am J Physiol Regul Integr Comp Physiol 282: R1006-R1015, 2002.
47. Zhang ZH, Francis J, Weiss RM, Felder RB. The renin-angiotensinaldosterone system excites hypothalamic paraventricular nucleus neurons in heart failure. Am J Physiol Heart Circ Physiol 283: H423-H433, 2002.
48. Zheng H, Li YF, Zucker IH, Patel KP. Exercise training improves renal excretory responses to acute volume expansion in rats with heart failure. Am J Physiol Renal Physiol 291: F1148-F1156, 2006.
49. Zheng H, Li YF, Cornish KG, Zucker IH, Patel KP. Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure. Am J Physiol Heart Circ Physiol 288: H2332-H2341, 2005.
50. Zheng H, Liu X, Patel KP. Angiotensin-converting enzyme 2 overexpression improves central nitric oxide mediated sympathetic outflow in chronic heart failure. Am J Physiol Heart Circ Physiol 301: H2402-H2412, 2011.
51. Zheng H, Sharma NM, Liu X, Patel KP. Exercise training normalizes enhanced sympathetic activation from the paraventricular nucleus in chronic heart failure: role of angiotensin II. Am J Physiol Regul Integr Comp Physiol 303: R387-R394, 2012.
52. Zhu GQ, Gao L, Patel KP, Zucker IH, Wang W. ANG II in the paraventricular nucleus potentiates the cardiac sympathetic afferent reflex in rats with heart failure. J Appl Physiol 97: 1746-1754, 2004.
53. Zucker IH, Wang W, Brändle M, Schultz HD, Patel KP. Neural regulation of sympathetic nerve activity in heart failure. Prog Cardiovasc Dis 37: 397-414, 1995.