Exercise training normalizes ACE and ACE2 in the brain of rabbits with pacing-induced heart failure

Journal of Applied Physiology

Volumn 108, Issue 4, 2010, Pages 923-932

  Kar, Sumit ^a   Gao, Lie ^a   Zucker, Irving H ^a  

^a NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Angiotensin (1 7); Angiotensin converting enzyme; Central nervous system; Sympathetic nerve activity; angiotensin II

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE; MESSENGER RNA;

ADRENERGIC SYSTEM; ANIMAL; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL HEART PACEMAKER; BRAIN; CHRONIC DISEASE; CYTOLOGY; DISEASE MODEL; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENETICS; HEART FAILURE; HEART PACING; HEMODYNAMICS; MALE; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; RABBIT;

ANIMALS; BRAIN; CARDIAC PACING, ARTIFICIAL; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; GENE EXPRESSION; HEART FAILURE; HEMODYNAMICS; MALE; MICROSCOPY, FLUORESCENCE; NEURONS; PACEMAKER, ARTIFICIAL; PEPTIDYL-DIPEPTIDASE A; PHYSICAL CONDITIONING, ANIMAL; RABBITS; RNA, MESSENGER; SYMPATHETIC NERVOUS SYSTEM;

EID: 77950591072     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00840.2009     Document Type: Article

References (57)

1. 1. Allen RG, Tresini M. Oxidative stress and gene regulation. Free Radic. Biol Med 28: 463-499, 2000. (Pubitemid 30110662)
2. Arai T, Yasuda Y, Takaya T, Toshima S, Kashiki Y, Yoshimi N, Shibayama M, Fujiwara H. ACE inhibitors and reduction of the risk of pneumonia in elderly people. Am J Hypertens 13: 1050-1051, 2000.
3. Averill DB, Ishiyama Y, Chappell MC, Ferrarlo CM. Cardiac angiotensin-(1-7) in ischemic cardiomyopathy. Circulation 108: 2141-2146, 2003.
4. Belardinelli R, Georgiern D, Scocco V, Barstow TJ, Purcaro A. Low intensity exercise training in patients with chronic heart failure. J Am Coll, Cardiol 26: 975-982, 1995.
5. Benter IF, Yousif MH, Anim JT, Cojocel C, Diz DI. Angiotensin-(1-7) prevents development of severe hypertension and end-organ damage in spontaneously hypertensive rats treated with L-NAME. Am J Physiol Heart Circ Physiol 290: H684-H691, 2006.
6. Brum PC, Da Silva GJ, Moreira ED, Ida F, Negrao CE, Krieger EM. Exercise training increases baroreceptor gain sensitivity in normal and hypertensive rats. Hypertension 36: 1018-1022, 2000.
7. Caldwell PR, Seegal BC, Hsu KC, Das M, Soffer RL. AngiotensinConverting enzyme: vascular endothelial localization. Science 191: 1050-1051, 1976.
8. Chappell MC, Brosnihan KB, Diz Dl, Ferrarlo CM. Identification of angiotensin-(1-7) in rat brain. Evidence for differential processing of angiotensin peptides. J Biol Chem 264: 16518-16523, 1989.
9. Chennaoui M, Drogou C, Gomez-Merino D. Effects of physical training on IL-Iß, IL-6 and IL-lra concentrations in various brain areas of the rat. Eur Cytokine Netw 19: 8-14, 2008.
10. 10. Danser AH, van Kesteren CA, Bax WA, Tavenier M, Derkx FH, Saxena PR, Schalekamp MA. Prorenin, renin, angiotensinogen, and angiotensin-converting enzyme in normal and failing human, hearts. Evidence for renin binding. Circulation 96: 220-226, 1997. (Pubitemid 27298424)
11. Diz DI, Garcia-Espinosa MA, Gallagher PE, Ganten D, Ferrarlo CM, Averill DB. Angiotensin-(l-7) and baroreflex function in nucleus tractus solitarii of (mRen2)27 transgenic rats. J Cardiovasc Pharmacol 51: 542-548, 2008.
12. 12. Doobay MF, Taiman LS, Obr TD, Tian X, Davissen RL, Lazartigues E. Differential expression of neuronal A.CE2 in transgenic mice with overexpression of the brain renin-angiotensin system. Am J Physiol Regul, Integr Comp Physiol 292: R373-R381, 2007. (Pubitemid 46089851)
13. 13. Fabris B, Jackson B, Kohzuki M, Perich R, Johnston CI. Increased cardiac angiotensin-converting enzyme in rats with chronic heart failure. Clin Exp Pharmacol Physiol 17: 309-314, 1990. (Pubitemid 20151437)
14. Falkenhahn M, Franke F, Bohle RM, Zhu YC, Stauss HM, Bachmann S, Danilov S, Unger T. Cellular distribution of angiotensin-converting enzyme after myocardial infarction. Hypertension 25: 219-226, 1995.
15. Felix JVC, Michelini LC. Training-induced pressure fall in spontaneously hypertensive rats is associated with reduced angiotensinogen mRNA expression within the nucleus tractus Solitarii. Hypertension 50: 780-785, 2007.
16. 16. 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. (Pubitemid 351457863)
17. Ferrario CM. Myocardial infarction increases ACE2 expression in rat and humans. Eur Heart J 26: 1141, 2005.
18. Filho AG, Ferreira AJ, Santos SH, Neves SR, Silva Camargos ER, Becker LK, Belchior HA, as-Peixoto MF, Pinheiro SV, Santos RA. Selective increase of angiotensin(1-7) and its receptor in hearts of spontaneously hypertensive rats subjected to physical training. Exp Physiol 93: 589-598, 2008.
19. KB activation. Free Radie Biol Med 22: 1115-1126, 1997.
20. Floras JS. Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure. J Am Coll Cardiol 22: 72A-84A, 1993.
21. Francis GS. Neurohumoral mechanisms involved in congestive heart failure. Am J Cardiol, 55: 15A-21A, 1985.
22. 22. Francis J, Chu Y, Johnson AK, Weiss RM, Felder RB. Acute myocardial infarction induces hypothalamic cytokine synthesis. Am J Physiol, Heart Circ Physiol 286: H2264-H2271, 2004. (Pubitemid 38685242)
23. Gallagher FE, Chappell MC, Diz DI, Ferrario CM, Tallant EA. Characterization of brain AC.E2: evidence for a secreted form of the enzyme. Hypertension 98: 195, 2004.
24. Gallagher PE, Chappell MC, Ferrario CM, Tallant EA. Distinct roles for ANG II and ANG-(1-7) in the regulation of angiotensin-converting enzyme 2 in rat astrocytes. Am J Physiol Cell Physiol 290: C420-C426, 2006.
25. 25. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ Res 95: 937-944, 2004. (Pubitemid 39435009)
26. 26. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Simvastatin therapy normalizes sympathetic neural control in experimental heart failure: roles of angiotensin II type 1 receptors and NAD(P)H oxidase. Circulation 112: 1763-1770, 2005. (Pubitemid 41368152)
27. 27. Gao L, Wang W, Liu D, Zucker IH. Exercise training normalizes sympathetic outflow by central antioxidant mechanisms in rabbits with pacing-induced chronic heart failure. Circulation 115: 3095-3102, 2007. (Pubitemid 46957475)
28. 28. Geyssant A, Geelen G, Denis C, Allevard AM, Vincent M, Jarsaillon E, Bizollon CA, Lacour JR, Gharib C. Plasma vasopressin, renin activity, and aldosterone: effect of exercise and training. Eur J Appl Physiol Occup Physiol 46: 21-30, 1981. (Pubitemid 11146714)
29. 29. Grobe JL, Mecca AP, Lingis M, Shenoy V, Bolton TA, Machado JM, Speth RC, Raizada MK, Katovich MJ. Prevention of angiotensin II-induced cardiac remodeling by angiotensin-(1-7). Am J Physiol Heart Circ Physiol 292: H736-H742, 2007. (Pubitemid 46246920)
30. 30. Hespel P, Lijnen Van Hoof R, Fagard R, Goossens W, Lissens W, Moerman E, Amery A. Effects of physical endurance training on the plasma renin-angiotensin-aldosterone system in normal man. J Endocrinol 443-449, 1988. (Pubitemid 18067627)
31. Hirsch AT, Talsness CE, Schunkert H, Paul M, Dzau VJ. Tissuespecific activation of cardiac angiotensin converting enzyme in experimental heart failure. Circ Res 69: 475-482, 1991.
32. 33. Koka V, Huang XR, Chung ACK, Wang W, Truong LD, Lan HY. Angiotensin II up-regulates angiotensin I-converting enzyme (ACE), but down-regulates ACE2 via the AT1-ERK/p38 MAP kinase pathway. Am J Pathol 172: 1174-1183, 2008. (Pubitemid 351671532)
33. 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.
34. 35. 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. (Pubitemid 34666365)
35. 36. 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. (Pubitemid 36379330)
36. Mears S. The importance of exercise training in patients with chronic heart failure. Nurs Stand 20: 41-47, 2006.
37. Miura M, Reis DJ. A blood pressure response from fastigial nucleus and its relay pathway in brainstem. Am J Physiol 219: 1330-1336, 1970.
38. 39. Mousa TM, Liu D, Cornish KG, Zucker IH. Exercise training enhances baroreflex sensitivity by an angiotensin II-dependent mechanism, in chronic heart failure. J Appl Physiol 104: 616-624, 2008. (Pubitemid 351468788)
39. 40. Murakami H, Liu JL, Zucker IH. Angiotensin II blockade [corrected] enhances baroreflex control of sympathetic outflow in heart failure. Hypertension 29: 564-569, 1997. (Pubitemid 27074719)
40. 41. Nonotte I, Laliberte MF, Gannoun-Zaki L, Bali JP, Chevillard C, Laliberte F. Localization of angiotensin-converting enzyme (ACE) mRNA in rabbit gastric mucosa by in situ hybridization. J Histochem Cytochem 42: 197-201, 1994. (Pubitemid 24042236)
41. 42. Ohrui T, Tomita N, Sato-Nakagawa T, Matsui T, Maruyama M, Niwa K, Arai H, Sasaki H. Effects of brain-penetrating ACE inhibitors on Alzheimer disease progression. Neurology 63: 1324-1325, 2004. (Pubitemid 39350046)
42. Palkovits M, Brownstein M. Microdissection of brain areas by the punch technique. Brain Microdissection Techniques: Methods in the Neurosciences, edited by Cuello AC. Chichester, UK: Wiley, 1983, p. 1-36.
43. Paton JF, Wang S, Poison JW, Kasparov S. Signalling across the blood brain barrier by angiotensin II: novel implications for neurogenic hypertension. J Mol Med 86: 705-710, 2008.
44. Pereira MG, Ferreira JCB, Bueno CR, Mattos KC, Rosa KT, Irigoyen MC, Oliveira EM, Krieger JE, Brum PC. Exercise training reduces cardiac angiotensin II levels and prevents cardiac dysfunction in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Eur J Appl Physiol 105: 843-850, 2009.
45. Pinto YM, Desmet BGJL, Vangilst WH, Scholtens E, Monnink S, Degraeff PA, Wesseling H. Selective and time-related activation of the cardiac renin-angiotensin system after experimental heart failure-relation to ventricular function and morphology. Cardiovasc Res 27: 1933-1938, 1993.
46. 47. Prabakaran P, Xiao X, Dimitrov DS. A model of the ACE2 structure and function as a SARS-CoV receptor. Biochem Biophys Res Commun 314: 235-241, 2004. (Pubitemid 38058393)
47. Reid IA. Interactions between ANG II, sympathetic nervous system, and baroreceptor reflexes in regulation of blood pressure. Am J Physiol, Endocrinol Metab 262: E763-E778, 1992.
48. Santos RAS, Ferreira AJ, Silva ACE. Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis. Exp Physiol 93: 519-527, 2008.
49. Sen CK. Antioxidant and redox regulation, of cellular signaling: introduction. Med Sci Sports Exercise 33: 368-370, 2001.
50. 51. Studer R, Reinecke H, Muller B, Holtz J, Just H, Drexler H. Increased angiotensin-I converting enzyme gene expression in the failing human heart. Quantification by competitive RNA polymerase chain reaction. J Clin Invest 94: 301-310, 1994. (Pubitemid 24218105)
51. 1receptor and ACE densities after myocardial infarct in rats. Am J Physiol Heart Circ Physiol 286: H1665-H1671, 2004.
52. 53. Towler P, Staker B, Prasad SG, Menon S, Tang J, Parsons T, Ryan D, Fisher M, Williams D, Dales NA, Patane MA, Pantoliano MW. ACE2 X-ray structures reveal a large hinge-bending motion important for inhibitor binding and catalysis. J Biol Chem 279: 17996-18007, 2004. (Pubitemid 38560569)
53. 54. Yamazato M, Yamazato Y, Sun CW, ez-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. (Pubitemid 351664196)
54. 55. Yoshimura R, Sato T, Kawada T, Shishido T, Inagaki M, Miyano H, Nakahara T, Miyashita H, Takaki H, Tatewaki T, Yanagiya Y, Sugimachi M, Sunagawa K. Increased brain angiotensin receptor in rats with chronic high-output heart failure. J Card Fail 6: 66-72, 2000. (Pubitemid 30161419)
55. 56. Yu Y, Wei SG, Zhang ZH, Gomez-Sanchez E, Weiss RM, Felder RB. Does aldosterone upregulate the brain renin-angiotensin system in rats with heart failure? Hypertension 51: 727-733, 2008. (Pubitemid 351301527)
56. 57. Zisman LS, Keller RS, Weaver B, Lin QS, Speth R, Bristow MR, Canver CC. Increased angiotensin-(1-7)-forming activity in failing human heart ventricles. Evidence for upregulation of the angiotensin-converting enzyme homologue ACE2. Circulation 108: 1707-1712, 2003. (Pubitemid 37243658)
57. Zucker IH. Brain angiotensin II: new insights into its role in sympathetic regulation. Circ Res 90: 503-505, 2002.