Central mechanisms for exercise training-induced reduction in sympatho-excitation in chronic heart failure

Autonomic Neuroscience: Basic and Clinical

Volumn 188, Issue , 2015, Pages 44-50

  Haack, Karla K V ^a   Zucker, Irving H ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Angiotensin II; Nitric oxide; Oxidative stress; Physical activity; Sympathetic nerve activity

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

EXCITATION; EXERCISE; FEEDBACK SYSTEM; HEART FAILURE; HUMAN; MUSCLE SYMPATHETIC NERVE ACTIVITY; NONHUMAN; OXIDATIVE STRESS; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ADRENERGIC SYSTEM; BRAIN; CHRONIC DISEASE; KINESIOTHERAPY; METABOLISM; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; QUALITY OF LIFE;

ANGIOTENSIN II; BRAIN; CHRONIC DISEASE; EXERCISE THERAPY; HEART FAILURE; HUMANS; NITRIC OXIDE; OXIDATIVE STRESS; QUALITY OF LIFE; SYMPATHETIC NERVOUS SYSTEM;

EID: 84922896891     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2014.10.015     Document Type: Review

References (96)

1. Ahmad T., Fiuzat M., Mark D.B., Neely B., Neely M., Kraus W.E., Kitzman D.W., Whellan D.J., Donahue M., Zannad F., Pina I.L., Adams K., O'Connor C.M., Felker G.M. The effects of exercise on cardiovascular biomarkers in patients with chronic heart failure. Am. Heart J. 2014, 167:193-202. (e191).
2. Belardinelli R., Georgiou D., Cianci G., Purcaro A. Randomized, controlled trial of long-term moderate exercise training in chronic heart failure - effects on functional capacity, quality of life, and clinical outcome. Circulation 1999, 99:1173-1182.
3. Biancardi V.C., Son S.J., Ahmadi S., Filosa J.A., Stern J.E. Circulating angiotensin II gains access to the hypothalamus and brain stem during hypertension via breakdown of the blood-brain barrier. Hypertension 2014, 63:572-579.
4. Campese V.M., Ye S., Zhong H., Yanamadala V., Ye Z., Chiu J. Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H695-H703.
5. Chan S.H., Chan J.Y. Brain stem oxidative stress and its associated signaling in the regulation of sympathetic vasomotor tone. J. Appl. Physiol. 2012, 113:1921-1928.
6. Chicco A.J., McCune S.A., Emter C.A., Sparagna G.C., Rees M.L., Bolden D.A., Marshall K.D., Murphy R.C., Moore R.L. Low-intensity exercise training delays heart failure and improves survival in female hypertensive heart failure rats. Hypertension 2008, 51:1096-1102.
7. Chua T.P., Coats A.J.S. The role of peripheral chemoreflex in chronic congestive heart failure. Congest. Heart Fail. 1997, 3:22-28.
8. Chua T.P., Clark A.L., Amadi A.A., Coats A.J.S. Relation between chemosensitivity and the ventilatory response to exercise in chronic heart failure. J. Am. Coll. Cardiol. 1996, 27:650-657.
9. Chugh S.S., Chua T.P., Coats A.J.S. Peripheral chemoreflex in chronic heart failure: friend and foe. Am. Heart J. 1996, 132:900-904.
10. Coats A.J., Adamopoulos S., Radaelli A., McCance A., Meyer T.E., Bernardi L., Solda P.L., Davey P., Ormerod O., Forfar C. Controlled trial of physical training in chronic heart failure. Exercise performance, hemodynamics, ventilation, and autonomic function. Circulation 1992, 85:2119-2131.
11. Colombo R., Mazzuero G., Spinatonda G., Lanfranchi P., Giannuzzi P., Ponikowski P., Coats A.J.S., Minuco G. Comparison between spectral analysis and the phenylephrine method for the assessment of baroreflex sensitivity in chronic heart failure. Clic. Sci. 1999, 97:503-507.
12. Conraads V.M., Beckers P., Bosmans J., De Clerck L.S., Stevens W.J., Vrints C.J., Brutsaert D.L. Combined endurance/resistance training reduces plasma TNF-alpha receptor levels in patients with chronic heart failure and coronary artery disease. Eur. Heart J. 2002, 23:1854-1860.
13. Downing J., Balady G.J. The role of exercise training in heart failure. J. Am. Coll. Cardiol. 2011, 58:561-569.
14. Drexler H., Faude F., Hoing S., Just H. Blood flow distribution within skeletal muscle during exercise in the presence of chronic heart failure: effect of milrinone. Circulation 1987, 76(6):1344-1352.
15. Eckberg D.L., Drabinsky M., Braunwald E. Defective cardiac parasympathetic control in patients with heart disease. N. Engl. J. Med 1971, 285:877-883.
16. Ellenbogen K.A., Mohanty P.K., Szentpetery S., Thames M.D. Arterial baroreflex abnormalities in heart failure. Reversal after orthotopic cardiac transplantation. Circulation 1989, 79:51-58.
17. Feng Y., Xia H., Cai Y., Halabi C.M., Becker L.K., Santos R.A., Speth R.C., Sigmund C.D., Lazartigues E. Brain-selective overexpression of human angiotensin-converting enzyme type 2 attenuates neurogenic hypertension. Circ. Res. 2010, 106:373-382.
18. Ferguson D.W., Abboud F.M., Mark A.L. Selective impairment of baroreflex mediated vasoconstrictor responses in patients with ventricular dysfunction. Circulation 1984, 69:451-460.
19. Ferguson D.W., Berg W.J., Roach P.J., Oren R.M., Mark A.L., Kempf J.S. Effects of heart failure on baroreflex control of sympathetic neural activity. Am. J. Cardiol. 1992, 69:523-531.
20. Fraga R., Franco F.G., Roveda F., de Matos L.N., Braga A.M., Rondon M.U., Rotta D.R., Brum P.C., Barretto A.C., Middlekauff H.R., Negrao C.E. Exercise training reduces sympathetic nerve activity in heart failure patients treated with carvedilol. Eur. J. Heart Fail. 2007, 9:630-636.
21. Gao L., Wang W., Li Y.L., Schultz H.D., Liu D., Cornish K.G., Zucker I.H. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ. Res. 2004, 95:937-944.
22. Gao L., Zhu Z., Zucker I.H., Wang W. Cardiac sympathetic afferent stimulation impairs baroreflex control of renal sympathetic nerve activity in rats. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H1706-H1711.
23. Gao L., Schultz H.D., Patel K.P., Zucker I.H., Wang W. Augmented input from cardiac sympathetic afferents inhibits baroreflex in rats with heart failure. Hypertension 2005, 45:1173-1181.
24. Gao L., Wang W., Li Y.L., Schultz H.D., Liu D.M., Cornish K.G., Zucker I.H. Sympathoexcitation by central ANG II: roles for AT 1 receptor upregulation and NAD(P)H oxidase in RVLM. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H2271-H2279.
25. Gao L., Pan Y.X., Wang W.Z., Li Y.L., Schultz H.D., Zucker I.H., Wang W. Cardiac sympathetic afferent stimulation augments the arterial chemoreceptor reflex in anesthetized rats. J. Appl. Physiol. 2007, 102:37-43.
26. Gao L., Wang W., Liu D., Zucker I.H. Exercise training normalizes sympathetic outflow by central antioxidant mechanisms in rabbits with pacing-induced chronic heart failure. Circulation 2007, 115:3095-3102.
27. Gao L., Wang W.Z., Wang W., Zucker I.H. Imbalance of angiotensin receptor expression and function in the RVLM: potential mechanism for sympathetic overactivity in heart failure. Hypertension 2008, 52:708-714.
28. Gielen S., Adams V., Mobius-Winkler S., Linke A., Erbs S., Yu J., Kempf W., Schubert A., Schuler G., Hambrecht R. Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J. Am. Coll. Cardiol. 2003, 42:861-868.
29. Haack K.K., Engler C.W., Papoutsi E., Pipinos I.I., Patel K.P., Zucker I.H. Parallel changes in neuronal AT1R and GRK5 expression following exercise training in heart failure. Hypertension 2012, 60:354-361.
30. Hagerman I., Tyni-Lenn R., Gordon A. Outcome of exercise training on the long-term burden of hospitalisation in patients with chronic heart failure. A retrospective study. Int. J. Cardiol. 2005, 98:487-491.
31. Hambrecht R., Gielen S., Linke A., Fiehn E., Yu J., Walther C., Schoene N., Schuler G. Effects of exercise training on left ventricular function and peripheral resistance in patients with chronic heart failure. JAMA 2000, 283:3095-3101.
32. Hunt S.A., Abraham W.T., Chin M.H., Feldman A.M., Francis G.S., Ganiats T.G., Jessup M., Konstam M.A., Mancini D.M., Michl K., Oates J.A., Rahko P.S., Silver M.A., Stevenson L.W., Yancy C.W., Antman E.M., Smith S.C., Adams C.D., Anderson J.L., Faxon D.P., Fuster V., Halperin J.L., Hiratzka L.F., Jacobs A.K., Nishimura R., Ornato J.P., Page R.L., Riegel B. ACC/AHA 2005 Guideline update for the diagnosis and management of chronic heart failure in the adult: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2005, 112:e154-e235.
33. Ito D., Ito O., Mori N., Cao P., Suda C., Muroya Y., Hao K., Shimokawa H., Kohzuki M. Exercise training upregulates nitric oxide synthases in the kidney of rats with chronic heart failure. Clin. Exp. Pharmacol. Physiol. 2013, 40:617-625.
34. Just H. Peripheral adaptations in congestive heart failure: a review. Am. J. Med. 1991, 90(Suppl. 5B):5B23S-25B26S.
35. Kar S., Gao L., Zucker I.H. Exercise training normalizes ACE and ACE2 in the brain of rabbits with pacing-induced heart failure. J. Appl. Physiol. 2010, 108:923-932.
36. Kar S., Gao L., Belatti D.A., Curry P.L., Zucker I.H. Central angiotensin (1-7) enhances baroreflex gain in conscious rabbits with heart failure. Hypertension 2011, 58:627-634.
37. Keteyian S.J., Leifer E.S., Houston-Miller N., Kraus W.E., Brawner C.A., O'Connor C.M., Whellan D.J., Cooper L.S., Fleg J.L., Kitzman D.W., Cohen-Solal A., Blumenthal J.A., Rendall D.S., Pina I.L. Relation between volume of exercise and clinical outcomes in patients with heart failure. J. Am. Coll. Cardiol. 2012, 60:1899-1905.
38. Kingwell B.A. Nitric oxide-mediated metabolic regulation during exercise: effects of training in health and cardiovascular disease. FASEB J. 2000, 14:1685-1696.
39. Kleiber A.C., Zheng H., Schultz H.D., Peuler J.D., Patel K.P. Exercise training normalizes enhanced glutamate-mediated sympathetic activation from the PVN in heart failure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1863-R1872.
40. Kumar A., Takada Y., Boriek A.M., Aggarwal B.B. Nuclear factor-kB: its role in health and disease. J. Mol. Med. 2004, 82:434-448.
41. Kuru O., Senturk U.K., Kocer G., Ozdem S., Baskurt O.K., Cetin A., Yesilkaya A., Gunduz F. Effect of exercise training on resistance arteries in rats with chronic NOS inhibition. J. Appl. Physiol. 2009, 107:896-902.
42. La Rovere M.T., Pinna G.D., Maestri R., Robbi E., Caporotondi A., Guazzotti G., Sleight P., Febo O. Prognostic implications of baroreflex sensitivity in heart failure patients in the beta-blocking era. J. Am. Coll. Cardiol. 2009, 53:193-199.
43. LeMaitre J.P., Harris S., Fox K.A., Denvir M. Change in circulating cytokines after 2 forms of exercise training in chronic stable heart failure. Am. Heart J. 2004, 147:100-105.
44. Li Y.L., Ding Y., Agnew C., Schultz H.D. Exercise training improves peripheral chemoreflex function in heart failure rabbits. J. Appl. Physiol. 2008, 105:782-790.
45. Liu J.L., Irvine S., Reid I.A., Patel K.P., Zucker I.H. Chronic exercise reduces sympathetic nerve activity in rabbits with pacing-induced heart failure: a role for angiotensin II. Circulation 2000, 102:1854-1862.
46. Liu J.L., Kulakofsky J., Zucker I.H. Exercise training enhances baroreflex control of heart rate by a vagal mechanism in rabbits with heart failure. J. Appl. Physiol. 2002, 92:2403-2408.
47. Llewellyn T., Zheng H., Liu X., Xu B., Patel K.P. Median preoptic nucleus and subfornical organ drive renal sympathetic nerve activity via a glutamatergic mechanism within the paraventricular nucleus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302:R424-R432.
48. Ma R., Zucker I.H., Wang W. Reduced NO enhances the central gain of cardiac sympathetic afferent reflex in dogs with heart failure. Am. J. Physiol. 1999, 276:H19-H26.
49. Magnusson G. Factors Limiting Exercise Capacity in Heart Failure: Effects of Local Muscle Training 1995, 1-44. Karolinska Institute, Stockholm, Sweden.
50. Mancia G., Seravalle G., Giannattasio C., Bossi M., Preti L., Cattaneo B.M., Grassi G. Reflex cardiovascular control in congestive heart failure. Am. J. Cardiol. 1992, 69:17G-23G.
51. Mayhan W.G., Arrick D.M., Patel K.P., Sun H. Exercise training normalizes impaired NOS-dependent responses of cerebral arterioles in type 1 diabetic rats. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H1013-H1020.
52. McDonald C.D., Burch G.E., Walsh J.J. Prolonged bed rest in the treatment of idiopathic cardiomyopathy. Am. J. Med. 1972, 52:41-50.
53. McKelvie R.S. Exercise training in patients with heart failure: clinical outcomes, safety, and indications. Heart Fail. Rev. 2008, 13:3-11.
54. Mohanty P.K., Arrowood J.A., Ellenbogen K.A., Thames M.D. Neurohumoral and hemodynamic effects of lower body negative pressure in patients with congestive heart failure. Am. Heart J. 1989, 118:78-85.
55. Mousa T.M., Liu D., Cornish K.G., Zucker I.H. Exercise training enhances baroreflex sensitivity by an angiotensin II-dependent mechanism in chronic heart failure. J. Appl. Physiol. 2008, 104:616-624.
56. Musch T.I., Moore R.L., Smaldone P.G., Riedy M., Zelis R. Cardiac adaptations to endurance training in rats with a chronic myocardial infarction. J. Appl. Physiol. 1989, 66(2):712-719.
57. Negraõ C.E., Middlekauff H.R. Adaptations in autonomic function during exercise training in heart failure. Heart Fail. Rev. 2008, 13:51-60.
58. Negraõ C.E., Middlekauff H.R. Exercise training in heart failure: reduction in angiotensin II, sympathetic nerve activity, and baroreflex control. J. Appl. Physiol. 2008, 104:577-578.
59. Nunes R.B., Alves J.P., Kessler L.P., Dal Lago P. Aerobic exercise improves the inflammatory profile correlated with cardiac remodeling and function in chronic heart failure rats. Clinics (Sao Paulo) 2013, 68:876-882.
60. O'Connor C.M., Whellan D.J., Lee K.L., Keteyian S.J., Cooper L.S., Ellis S.J., Leifer E.S., Kraus W.E., Kitzman D.W., Blumenthal J.A., Rendall D.S., Miller N.H., Fleg J.L., Schulman K.A., McKelvie R.S., Zannad F., Pina I.L. Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 2009, 301:1439-1450.
61. Parmley W.W. Pathophysiology and current therapy of congestive heart failure. J. Am. Coll. Cardiol. 1989, 13:771-785.
62. Patel K.P., Zhang K., Zucker I.H., Krukoff T.L. Decreased gene expression of neuronal nitric oxide synthase in hypothalamus and brainstem of rats in heart failure. Brain Res. 1996, 734:109-115.
63. Patel K.P., Zhang P.L., Carmines P.K. Neural influences on renal responses to acute volume expansion in rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 1996, 271:H1441-H1448.
64. Patel K.P., Zhang K., Kenney M.J., Weiss M., Mayhan W.G. Neuronal expression of Fos protein in the hypothalamus of rats with heart failure. Brain Res. 2000, 865:27-34.
65. Piepoli M.F., Capucci A. Exercise training in heart failure: effect on morbidity and mortality. Int. J. Cardiol. 2000, 73:3-6.
66. Pina I.L., Apstein C.S., Balady G.J., Belardinelli R., Chaitman B.R., Duscha B.D., Fletcher B.J., Fleg J.L., Myers J.N., Sullivan M.J. Exercise and heart failure: a statement from the American Heart Association Committee on exercise, rehabilitation, and prevention. Circulation 2003, 107:1210-1225.
67. Pliquett R.U., Cornish K.G., Patel K.P., Schultz H.D., Peuler J.D., Zucker I.H. Amelioration of depressed cardiopulmonary reflex control of sympathetic nerve activity by short-term exercise training in male rabbits with heart failure. J. Appl. Physiol. 2003, 95:1883-1888.
68. Ponikowski P., Chua T.P., Pepoli M., Ondusova D., Webb-Peplie K., Harrington D., Anker S.D., Volterrani M., Colombo R., Mazzuero G., Giordano A., Coats A.J.S. Augmented peripheral chemosensitivity as a potential input to baroreflex impairment and autonomic imbalance in chronic heart failure. Circulation 1997, 96:2586-2594.
69. Rengo G., Pagano G., Parisi V., Femminella G.D., de Lucia C., Liccardo D., Cannavo A., Zincarelli C., Komici K., Paolillo S., Fusco F., Koch W.J., Perrone Filardi P., Ferrara N., Leosco D. Changes of plasma norepinephrine and serum N-terminal pro-brain natriuretic peptide after exercise training predict survival in patients with heart failure. Int. J. Cardiol. 2014, 171:384-389.
70. Riley M., Elborn J.S., Bell N., Stanford C.F., Nicholls D.P. Substrate utilization during exercise in chronic heart failure. Clin. Sci. 1990, 79:89-95.
71. Rosenwinkel E.T., Bloomfield D.M., Arwady M.A., Goldsmith R.L. Exercise and autonomic function in health and cardiovascular disease. Cardiol. Clin. 2001, 19:369-387.
72. Roveda F., Middlekauff H.R., Rondon M.U., Reis S.F., Souza M., Nastari L., Barretto A.C., Krieger E.M., Negrao C.E. The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial. J. Am. Coll. Cardiol. 2003, 42:854-860.
73. Scalvini S., Volterrani M., Zanelli E., Pagani M., Mazzuero G., Coats A.J., Giordano A. Is heart rate variability a reliable method to assess autonomic modulation in left ventricular dysfunction and heart failure? Assessment of autonomic modulation with heart rate variability. Int. J. Cardiol. 1998, 67:9-17.
74. Schultz H.D., Li Y.L. Carotid body function in heart failure. Respir. Physiol. Neurobiol. 2007, 157:171-185.
75. Smart N., Marwick T.H. Exercise training for patients with heart failure: a systematic review of factors that improve mortality and morbidity. Am. J. Med. 2004, 116:693-706.
76. Smart N.A., Steele M. The effect of physical training on systemic proinflammatory cytokine expression in heart failure patients: a systematic review. Congest. Heart Fail. 2011, 17:110-114.
77. Sun S.Y., Wang W., Zucker I.H., Schultz H.D. Enhanced peripheral chemoreflex function in conscious rabbits with pacing-induced heart failure. J. Appl. Physiol. 1999, 86(4):1264-1272.
78. Sun S.Y., Zucker I.H., Wang W., Schultz H.D. Enhanced activity of carotid body chemoreceptors in rabbits with heart failure: role of nitric oxide. J. Appl. Physiol. 1999, 86(4):1273-1282.
79. Wang Y., Golledge J. Neuronal nitric oxide synthase and sympathetic nerve activity in neurovascular and metabolic systems. Curr. Neurovasc. Res. 2013, 10:81-89.
80. Wang W., Zucker I.H. Cardiac sympathetic afferent reflex in dogs with congestive heart failure. Am. J. Physiol. 1996, 271:R751-R756.
81. Wang H.J., Zhang F., Zhang Y., Gao X.Y., Wang W., Zhu G.Q. AT 1 receptor in paraventricular nucleus mediates the enhanced cardiac sympathetic afferent reflex in rats with chronic heart failure. Auton. Neurosci. Basic Clin. 2004, 121:56-63.
82. Wang W.Z., Gao L., Pan Y.X., Zucker I.H., Wang W. Differential effects of cardiac sympathetic afferent stimulation on neurons in the nucleus tractus solitarius. Neurosci. Lett. 2006, 409:146-150.
83. Xiao L., Gao L., Lazartigues E., Zucker I.H. Brain-selective overexpression of angiotensin-converting enzyme 2 attenuates sympathetic nerve activity and enhances baroreflex function in chronic heart failure. Hypertension 2011, 58:1057-1065.
84. Yousufuddin M., Shamim W., Chambers J.S., Henein M., Amin F.R., Anker S.D., Kemp M., Hooper J., Coats A.J.S. Superiority of endothelin-1 over norepinephrine in exercise-induced alterations of the conduit artery tone of the non-exercised arm in patients with chronic heart failure. Int. J. Cardiol. 2000, 73:15-25.
85. Zanzinger J., Czachurski J. Chronic oxidative stress in the RVLM modulates sympathetic control of circulation in pigs. Pflugers Arch. - Eur. J. Physiol. 2000, 439:489-494.
86. Zhang K., Zucker I.H., Patel K.P. Altered number of diaphorase (NOS) positive neurons in the hypothalamus of rats with heart failure. Brain Res. 1998, 786:219-225.
87. Zhang K., Li Y.F., Patel K.P. Blunted nitric oxide-mediated inhibition of renal nerve discharge within PVN of rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H995-H1004.
88. Zheng H., Li Y.F., Cornish K.G., Zucker I.H., Patel K.P. Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H2332-H2341.
89. Zheng H., Li Y.F., Zucker I.H., Patel K.P. Exercise training improves renal excretory responses to acute volume expansion in rats with heart failure. Am. J. Physiol. Ren. Physiol 2006, 291:F1148-F1156.
90. Zheng H., Liu X., Li Y., Sharma N.M., Patel K.P. Gene transfer of neuronal nitric oxide synthase to the paraventricular nucleus reduces the enhanced glutamatergic tone in rats with chronic heart failure. Hypertension 2011, 58:966-973.
91. Zheng H., Liu X., Patel K.P. Angiotensin-converting enzyme 2 overexpression improves central nitric oxide-mediated sympathetic outflow in chronic heart failure. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H2402-H2412.
92. Zhu G.Q., Patel K.P., Zucker I.H., Wang W. Microinjection of ANG II into the paraventricular nucleus enhances cardiac sympathetic afferent reflex in rats. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H2039-H2045.
93. Zhu G.Q., Gao L., Li Y.F., Patel K.P., Zucker I.H., Wang W. AT 1 receptor mRNA antisense normalizes enhanced cardiac sympathetic afferent reflex in rats with chronic heart failure. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H1828-H1835.
94. Zhu G.Q., Gao L., Patel K.P., Zucker I.H., Wang W. ANG II in the paraventricular nucleus potentiates the cardiac sympathetic afferent reflex in rats with heart failure. J. Appl. Physiol. 2004, 97:1746-1754.
95. Zhu G.Q., Gao X.Y., Zhang F., Wang W. Reduced nitric oxide in the rostral ventrolateral medulla enhances cardiac sympathetic afferent reflex in rats with chronic heart failure. Sheng Li Xue Bao 2004, 56:47-53.
96. Zucker I.H. Cardiac and baroreflex control of the circulation in heart failure. Heart Failure Mechanisms and Management 1991, 45-55. Springer-Verlag, Berlin, Heidelberg. B.S. Lewis, A. Kimichi (Eds.).