Differential effects of superoxide and hydrogen peroxide on myogenic signaling, membrane potential, and contractions of mouse renal afferent arterioles

American Journal of Physiology - Renal Physiology

Volumn 310, Issue 11, 2016, Pages F1197-F1205

  Li, Lingli ^a   Lai, En Yin ^b   Wellstein, Anton ^c   Welch, William J ^a   Wilcox, Christopher S ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

Chloride channels; Potassium channels; Protein kinase C; Protein kinase G; Reactive oxygen species; Renal autoregulation

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; APAMIN; CATALASE; CHARYBDOTOXIN; GLIBENCLAMIDE; HYDROGEN PEROXIDE; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LINOPIRDINE; N(G) NITROARGININE METHYL ESTER; NIFEDIPINE; OXYGEN; PARAQUAT; PEG CATALASE; PEGORGOTEIN; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; SAPONIN; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; KIDNEY; KIDNEY FUNCTION; MALE; MEMBRANE CHANNEL; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PERFUSION PRESSURE; PRIORITY JOURNAL; RENAL AFFERENT ARTERIOLE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; ARTERIOLE; DRUG EFFECTS; METABOLISM; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; ARTERIOLES; HYDROGEN PEROXIDE; MALE; MEMBRANE POTENTIALS; MICE; MUSCLE, SMOOTH, VASCULAR; PARAQUAT; REACTIVE OXYGEN SPECIES; SUPEROXIDES; VASOCONSTRICTION;

EID: 84984619720     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00575.2015     Document Type: Article

References (56)

1. Alapati VR, McKenzie C, Blair A, Kenny D, MacDonald A, Shaw AM. Mechanisms of U46619- and 5-HT-induced contraction of bovine pulmonary arteries: role of chloride ions. Br J Pharmacol 151: 1224–1234, 2007.
2. Araujo M, Wilcox CS. Oxidative stress in hypertension: role of the kidney. Antioxid Redox Signal 20: 74–101, 2014.
3. Baumgarten CM, Clemo HF. Swelling-activated chloride channels in cardiac physiology and pathophysiology. Progr Biophys Mol Biol 82: 25–42, 2003.
4. ·−on the plasma membrane in vascular endothelial cells. Am J Physiol Heart Circ Physiol 289: H2379–H2386, 2005.
5. Burgoyne JR, Oka S, Ale-Agha N, Eaton P. Hydrogen peroxide sensing and signaling by protein kinases in the cardiovascular system. Antioxid Redox Signal 18: 1042–1052, 2013.
6. Burke M, Pabbidi MR, Farley J, Roman RJ. Molecular mechanisms of renal blood flow autoregulation. Curr Vasc Pharmacol 12: 845–858, 2014.
7. Carlstrom M, Lai EY, Ma Z, Steege A, Patzak A, Eriksson UJ, Lundberg JO, Wilcox CS, Persson AE. Superoxide dismutase 1 limits renal microvascular remodeling and attenuates arteriole and blood pressure responses to angiotensin II via modulation of nitric oxide bioavailability. Hypertension 56: 907–913, 2010.
8. Carlstrom M, Wilcox CS, Arendshorst WJ. Renal autoregulation in health and disease. Physiol Rev 95: 405–511, 2015.
9. Chen Y, Pearlman A, Luo Z, Wilcox CS. Hydrogen peroxide mediates a transient vasorelaxation with tempol during oxidative stress. Am J Physiol Heart Circ Physiol 293: H2085–H2092, 2007.
10. Edwards A, Layton AT. Calcium dynamics underlying the myogenic response of the renal afferent arteriole. Am J Physiol Renal Physiol 306: F34–F48, 2014.
11. Epps DE, Wolfe ML, Groppi V. Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3dibutylbarbituric acid)trimethine oxonol [Dibac4(3)] in model systems and cells. Chem Phys Lipids 69: 137–150, 1994.
12. + channels on rat renal arteriolar responses to depolarizing agonists. Am J Physiol Renal Physiol 280: F583–F591, 2001.
13. Fellner RC, Cook AK, O’Connor PM, Zhang S, Pollock DM, Inscho EW. High-salt diet blunts renal autoregulation by a reactive oxygen species-dependent mechanism. Am J Physiol Renal Physiol 307: F33–F40, 2014.
14. 2+-activated BK currents and promoted cell injury in human dermal fibroblasts. Life Sci 90: 424–431, 2012.
15. Fink B, Laude K, McCann L, Doughan A, Harrison DG, Dikalov S. Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an HPLC-based assay. Am J Physiol Cell Physiol 287: C895–C902, 2004.
16. + channels as a mechanism of cytoprotective neuronal silencing. EMBO J 25: 4996–5004, 2006.
17. Griffin KA, Picken MM, Bidani AK. Blood pressure lability and glomerulosclerosis after normotensive 5/6 renal mass reduction in the rat. Kidney Int 65: 209–218, 2004.
18. Harder DR, Narayanan J, Gebremedhin D, Roman RJ. Transduction of physical force by the vascular wall. Role of phospholipase C and cytochrome P450 metabolites of arachidonic acid. Trends Cardiovasc Med 5: 7–14, 1995.
19. Hong NJ, Garvin JL. Endogenous flow-induced superoxide stimulates Na/H exchange activity via PKC in thick ascending limbs. Am J Physiol Renal Physiol 307: F800–F805, 2014.
20. + channels: a functional unit for regulating arterial tone. Acta Physiol Scand 164: 577–587, 1998.
21. Jensen BL, Ellekvist P, Skott O. Chloride is essential for contraction of afferent arterioles after agonists and potassium. Am J Physiol Renal Physiol 272: F389–F396, 1997.
22. Kriz W, Lemley KV. A potential role for mechanical forces in the detachment of podocytes and the progression of CKD. J Am Soc Nephrol 26: 258–269, 2015.
23. Lai EY, Luo Z, Onozato ML, Rudolph EH, Solis G, Jose PA, Wellstein A, Aslam S, Quinn MT, Griendling K, Le T, Li P, Palm F, Welch WJ, Wilcox CS. Effects of the antioxidant drug tempol on renal oxygenation in mice with reduced renal mass. Am J Physiol Renal Physiol 303: F64–F74, 2012.
24. Lai EY, Martinka P, Fahling M, Mrowka R, Steege A, Gericke A, Sendeski M, Persson PB, Persson AE, Patzak A. Adenosine restores angiotensin II-induced contractions by receptor-independent enhancement of calcium sensitivity in renal arterioles. Circ Res 99: 1117–1124, 2006.
25. Lai EY, Onozato ML, Solis G, Aslam S, Welch WJ, Wilcox CS. Myogenic responses of mouse isolated perfused renal afferent arterioles: effects of salt intake and reduced renal mass. Hypertension 55: 983–989, 2010.
26. phox is required for afferent arteriolar contractile responses to angiotensin II and perfusion pressure in mice. Hypertension 59: 415–420, 2012.
27. Lai EY, Wellstein A, Welch WJ, Wilcox CS. Superoxide modulates myogenic contractions of mouse afferent arterioles. Hypertension 58: 650–656, 2011.
28. phox in mice. Am J Physiol Heart Circ Physiol 288: H7–H12, 2005.
29. Li L, Feng D, Luo Z, Welch WJ, Wilcox CS, Lai EY. Remodeling of afferent arterioles from mice with oxidative stress does not account for increased contractility but does limit excessive wall stress. Hypertension 66: 550–556, 2015.
30. 1-adrenoceptor agonist phenylephrine on swelling-activated chloride currents in human atrial myocytes. J Membr Biol 248: 7–18, 2015.
31. 2 is the transferrable factor mediating flow-induced dilation in human coronary arterioles. Circ Res 108: 566–573, 2011.
32. Loutzenhiser R, Griffin K, Williamson G, Bidani A. Renal autoregulation: new perspectives regarding the protective and regulatory roles of the underlying mechanisms. Am J Physiol Regul Integr Comp Physiol 290: R1153–R1167, 2006.
33. Lu H, Zhen J, Wu T, Peng A, Ye T, Wang T, Yu X, Vaziri ND, Mohan C, Zhou XJ. Superoxide dismutase mimetic drug tempol aggravates anti-GBM antibody-induced glomerulonephritis in mice. Am J Physiol Renal Physiol 299: F445–F452, 2010.
34. Narayanan J, Imig M, Roman RJ, Harder DR. Pressurization of isolated renal arteries increases inositol trisphosphate and diacylglycerol. Am J Physiol Heart Circ Physiol 266: H1840–H1845, 1994.
35. Ohanyan V, Yin L, Bardakjian R, Kolz C, Enrick M, Hakobyan T, Kmetz J, Bratz I, Luli J, Nagane M, Khan N, Hou H, Kuppusamy P, Graham J, Fu FK, Janota D, Oyewumi MO, Logan S, Lindner JR, Chilian WM. Requisite role of Kv1.5 channels in coronary metabolic dilation. Circ Res 117: 612–621, 2015.
36. Park SW, Noh HJ, Sung DJ, Kim JG, Kim JM, Ryu SY, Kang K, Kim B, Bae YM, Cho H. Hydrogen peroxide induces vasorelaxation by enhancing 4-aminopyridine-sensitive Kv currents through S-glutathionylation. Pflügers Arch 467: 285–297, 2015.
37. Pelayo JC, Westcott JY. Impaired autoregulation of glomerular capillary hydrostatic pressure in the rat remnant nephron. J Clin Invest 88: 101–105, 1991.
38. + channels in the control of membrane potential in rabbit renal arcuate artery. J Physiol 511: 159–169, 1998.
39. 2: role of modulation of vascular TP receptors and the heme oxygenase system. Antioxid Redox Signal 18: 471–480, 2013.
40. Quiroz Y, Ferrebuz A, Vaziri ND, Rodriguez-Iturbe B. Effect of chronic antioxidant therapy with superoxide dismutase-mimetic drug, tempol, on progression of renal disease in rats with renal mass reduction. Nephron Exp Nephrol 112: e31–e42, 2009.
41. Racasan S, Turkstra E, Joles JA, Koomans HA, Braam B. Hypoxanthine plus xanthine oxidase causes profound natriuresis without affecting renal blood flow autoregulation. Kidney Int 64: 226–231, 2003.
42. 2 and NO. Am J Physiol Renal Physiol 279: F302–F308, 2000.
43. Segal AW. The function of the NADPH oxidase of phagocytes and its relationship to other NOXs in plants, invertebrates, and mammals. Int J Biochem Cell Biol 40: 604–618, 2008.
44. Sharma K, Cook A, Smith M, Valancius C, Inscho EW. TGF-β impairs renal autoregulation via generation of ROS. Am J Physiol Renal Physiol 288: F1069–F1077, 2005.
45. Shen M, Wang L, Wang B, Wang T, Yang G, Shen L, Wang T, Guo X, Liu Y, Xia Y, Jia L, Wang X. Activation of volume-sensitive outwardly rectifying chloride channel by ROS contributes to ER stress and cardiac contractile dysfunction: involvement of CHOP through Wnt. Cell Death Dis 5: e1528, 2014.
46. Su EN, Kelly ME, Cringle SJ, Yu DY. Role of endothelium in abnormal cannabidiol-induced vasoactivity in retinal arterioles. Invest Ophthalmol Vis Sci 56: 4029–4037, 2015.
47. Takenaka T, Kanno Y, Kitamura Y, Hayashi K, Suzuki H, Saruta T. Role of chloride channels in afferent arteriolar constriction. Kidney Int 50: 864–872, 1996.
48. 2 contribute to ACh-induced hyperpolarization of pressurized canine coronary microvessels. Am J Physiol Heart Circ Physiol 285: H1939–H1948, 2003.
49. + channel regulation of afferent arteriolar tone in diabetic rat kidney. Hypertension 59: 657–664, 2012.
50. 2+ entry through L-type channels in the renal afferent arteriole. Hypertension 66: 374–381, 2015.
51. Wang D, Chabrashvili T, Wilcox CS. Enhanced contractility of renal afferent arterioles from angiotensin-infused rabbits: roles of oxidative stress, thromboxane prostanoid receptors, and endothelium. Circ Res 94: 1436–1442, 2004.
52. 1 Receptors protect the renal afferent arteriole of angiotensin-infused rabbits from norepinephrine-induced oxidative stress. J Am Soc Nephrol 17: 3347–3354, 2006.
53. Yang J, Lane PH, Pollock JS, Carmines PK. PKC-dependent superoxide production by the renal medullary thick ascending limb from diabetic rats. Am J Physiol Renal Physiol 297: F1220–F1228, 2009.
54. Yang KC, Kyle JW, Makielski JC, Dudley SC Jr. Mechanisms of sudden cardiac death: oxidants and metabolism. Circ Res 116: 1937–1955, 2015.
55. + channel activation. Circ Res 110: 471–480, 2012.
56. O2 cycling protects diaphragm function during reoxygenation via ROS, Akt, ERK and mitochondrial channels. Am J Physiol Cell Physiol 309: C759–C766, 2015.