Elevated mitochondrial superoxide contributes to enhanced chemoreflex in heart failure rabbits

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 2, 2010, Pages

  Ding, Yanfeng ^a   Li, Yu Long ^a   Zimmerman, Matthew C ^a   Schultz, Harold D ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Adenoviral vector; Carotid body; Chronic heart failure; Mitochondrial superoxide levels; Superoxide dismutase

Indexed keywords

MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDE;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID BODY; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; HEART FAILURE; MALE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYMPATHETIC NERVE;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CAROTID BODY; FLUORESCENT ANTIBODY TECHNIQUE; GENE TRANSFER TECHNIQUES; HEART FAILURE; HEART FUNCTION TESTS; KIDNEY; MALE; MITOCHONDRIA, HEART; POTASSIUM CHANNELS; RABBITS; REFLEX; SUPEROXIDE DISMUTASE; SUPEROXIDES; SYMPATHETIC NERVOUS SYSTEM;

EID: 75449111112     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00629.2009     Document Type: Article

References (48)

1. 2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am J Physiol Heart Circ Physiol 294: H570-H578, 2008.
2. Chan SHH, Wu KLH, Chang AYW, Tai MH, Chan JYH. Oxidative impairment of mitochondrial electron transport chain complexes in rostral ventrolateral medulla contributes to neurogenic hypertension. Hypertension 53: 217-227, 2009.
3. Chandel NS, Schumacker PT. Cellular oxygen sensing by mitochondria: old questions, new insight. J Appl Physiol 88: 1880-1889, 2000.
4. Chua TP, Ponikowski P, Webb-Peploe K, Harrington D, Anker SD, Piepoli M, Coats AJ. Clinical characteristics of chronic heart failure patients with an augmented peripheral chemoreflex. Eur Heart J 18: 480-486, 1997.
5. Chugh SS, Chua TP, Coats AJS. Peripheral chemoreflex in chronic heart failure: friend and foe. Am Heart J 132: 900-904, 1996.
6. Ding Y, Li YL, Schultz HD. Downregulation of carbon monoxide as well as nitric oxide contributes to peripheral chemoreflex hypersensitivity in heart failure rabbits. J Appl Physiol 105: 14-23, 2008.
7. Ding Y, Li YL, Zimmerman MC, Davisson RL, Schultz HD. Role of CuZn superoxide dismutase on carotid body function in heart failure rabbits. Cardiovasc Res 81: 678-685, 2009.
8. Doughan AK, Harrison DG, Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102: 488-496, 2008.
9. Esler M, Kaye D, Lambert G, Esler D, Jennings G. Adrenergic nervous system in heart failure. Am J Cardiol 80: 7L-14L, 1997.
10. Floras JS. Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure. J Am Coll Cardiol 22: 72A-84A, 1993.
11. 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.
12. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74: 829-898, 1994.
13. Harrison DG, Gongora MC. Oxidative stress and hypertension. Med Clin North Am 93: 621-635, 2009.
14. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE. Mitochondria and reactive oxygen species. Free Radic Biol Med 47: 333-343, 2009.
15. Li YL, Gao L, Zucker IH, Schultz HD. NADPH oxidase-derived superoxide anion mediates angiotensin II-enhanced carotid body chemoreceptor sensitivity in heart failure rabbits. Cardiovasc Res 75: 546-554, 2007.
16. Li YL, Li YF, Liu D, Cornish KG, Patel KP, Zucker IH, Channon KM, Schultz HD. Gene transfer of neuronal nitric oxide synthase to carotid body reverses enhanced chemoreceptor function in heart failure rabbits. Circ Res 97: 260-267, 2005.
17. Li YL, Schultz HD. Enhanced sensitivity of Kv channels to hypoxia in the rabbit carotid body in heart failure: role of angiotensin II. J Physiol (Lond) 575: 215-227, 2006.
18. Li YL, Schultz HD. Role of NADPH oxidase-derived superoxide anion on angiotensin II-enhanced sensitivity of potassium channels to hypoxia in carotid body of congestive heart failure rabbit (Abstract). FASEB J 21: 910.12, 2007.
19. Li YL, Sun SY, Overholt JL, Prabhakar NR, Rozanski GJ, Zucker IH, Schultz HD. Attenuated outward potassium currents in carotid body glomus cells of heart failure rabbit: involvement of nitric oxide. J Physiol (Lond) 555: 219-229, 2004.
20. Li YL, Xia XH, Zheng H, Gao L, Li YF, Liu D, Patel KP, Wang W, Schultz HD. Angiotensin II enhances carotid body chemoreflex control of sympathetic outflow in chronic heart failure rabbits. Cardiovasc Res 71: 129-138, 2006.
21. Lopez-Barneo J, Pardal R, Ortega-Saenz P. Cellular mechanism of oxygen sensing. Annu Rev Physiol 63: 259-287, 2001.
22. Mark AL. Sympathetic dysregulation in heart failure: mechanisms and therapy. Clin Cardiol 18: I3-I8, 1995.
23. Mukhopadhyay P, Rajesh M, Hasko G, Hawkins BJ, Madesh M, Pacher P. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2: 2295-2301, 2007.
24. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1-13, 2009.
25. Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver. Cu,Zn-SOD in mitochondria. J Biol Chem 276: 38388-38393, 2001.
26. Ponikowski P, Chua TP, Piepoli M, Banasiak W, Anker SD, Szelemej R, Molenda W, Wrabec K, Capucci A, Coats AJS. Ventilatory response to exercise correlates with impaired heart rate variability in patients with chronic congestive heart failure. Am J Cardiol 82: 338-344, 1998.
27. Ponikowski P, Chua TP, Piepoli M, Ondusova D, Webb-Peploe K, Harrington D, Anker SD, Volterrani M, Colombo R, Mazzuero G, Giordano A, Coats AJS. Augmented peripheral chemosensitivity as a potential input to baroreflex impairment and autonomic imbalance in chronic heart failure. Circulation 96: 2586-2594, 1997.
28. Prabhakar NR. Neurotransmitters in the carotid body. Adv Exp Med Biol 360: 57-69, 1994.
29. Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci USA 103: 15038-15043, 2006.
30. Robinson KM, Janes MS, Beckman JS. The selective detection of mitochondrial superoxide by live cell imaging. Nat Protoc 3: 941-947, 2008.
31. Schultz HD, Li YL, Ding Y. Arterial chemoreceptors and sympathetic nerve activity: implications for hypertension and heart failure. Hypertension 50: 6-13, 2007.
32. Schultz HD, Sun SY. Chemoreflex function in heart failure. Heart Fail Rev 5: 45-56, 2000.
33. Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 1147: 37-52, 2008.
34. 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.
35. Sun SY, Wang W, Zucker IH, Schultz HD. Enhanced peripheral chemoreflex function in conscious rabbits with pacing-induced heart failure. J Appl Physiol 86: 1264-1272, 1999.
36. 2 are key components of hypoxia-sensing in neonatal rat adrenomedullary chromaffin cells. Neuroscience 145: 130-141, 2007.
37. Ward JPT. Oxygen sensors in context. Biochim Biophys Acta 1777: 1-14, 2008.
38. Waypa GB, Chandel NS, Schumacker PT. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ Res 88: 1259-1266, 2001.
39. Waypa GB, Guzy R, Mungai PT, Mack MM, Marks JD, Roe MW, Schumacker PT. Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells. Circ Res 99: 970-978, 2006.
40. Weir EK, Lopez-Barneo J, Buckler KJ, Archer SL. Acute oxygen-sensing mechanisms. N Engl J Med 353: 2042-2055, 2005.
41. Wyatt CN, Buckler KJ. The effect of mitochondrial inhibitors on membrane currents in isolated neonatal rat carotid body type I cells. J Physiol 556: 175-191, 2004.
42. + current in CATH.a neurons. FASEB J 22: lb150, 2008.
43. Zanetti M, Sato J, Katusic ZS, O'Brien T. Gene transfer of superoxide dismutase isoforms reverses endothelial dysfunction in diabetic rabbit aorta. Am J Physiol Heart Circ Physiol 280: H2516-H2523, 2001.
44. Zimmerman MC, Oberley LW, Flanagan SW. Mutant SOD1-induced neuronal toxicity is mediated by increased mitochondrial superoxide levels. J Neurochem 102: 609-618, 2007.
45. Zimmerman MC, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, Spitz DR, Davisson RL. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 91: 1038-1045, 2002.
46. Zucker IH, Schultz HD, Li YF, Wang Y, Wang W, Patel KP. The origin of sympathetic outflow in heart failure: the roles of angiotensin II and nitric oxide. Prog Biophys Mol Biol 84: 217-232, 2004.
47. Zucker IH, Schultz HD, Patel KP, Wang W, Gao L. Regulation of central angiotensin type 1 receptors and sympathetic outflow in heart failure. Am J Physiol Heart Circ Physiol 297: H1557-H1566, 2009.
48. Zucker IH, Wang W, Brandle M, Schultz HD, Patel KP. Neural regulation of sympathetic nerve activity in heart failure. Prog Cardiovasc Dis 37: 397-414, 1995.