Chronic treatment with tempol does not significantly ameliorate renal tissue hypoxia or disease progression in a rodent model of polycystic kidney disease

Clinical and Experimental Pharmacology and Physiology

Volumn 39, Issue 11, 2012, Pages 917-929

  Ding, Alice ^a   Kalaignanasundaram, Priyadharshani ^b   Ricardo, Sharon D ^c   Abdelkader, Amany ^b   Witting, Paul K ^d   Broughton, Brad Rs ^c   Kim, Hyun B ^d   Wyse, Benjamin F ^a   Phillips, Jacqueline K ^a   Evans, Roger G ^b  

^a MACQUARIE UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Heme oxygenase; Hypoxia; Hypoxia inducible factors; Nitrosative stress; Nitrotyrosine; Oxidative stress; Polycystic kidney disease; Superoxide dismutase

Indexed keywords

3 NITROTYROSINE; CREATININE; GLUCOSE TRANSPORTER 1; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PIMONIDAZOLE; SUPEROXIDE DISMUTASE; TEMPOL; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE COURSE; ENZYME ACTIVITY; HEMODYNAMICS; HISTOPATHOLOGY; HYPOXEMIA; HYPOXIA; IMMUNOFLUORESCENCE; KIDNEY CYST; KIDNEY MASS; KIDNEY POLYCYSTIC DISEASE; MALE; MEAN ARTERIAL PRESSURE; MORPHOMETRICS; NITROSATIVE STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; POLYURIA; PROTEIN EXPRESSION; PROTEINURIA; RAT; REAL TIME POLYMERASE CHAIN REACTION; RENOVASCULAR HYPERTENSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; UREMIA;

ANIMALS; ARTERIAL PRESSURE; CELL HYPOXIA; CREATININE; CYCLIC N-OXIDES; DISEASE PROGRESSION; GLUCOSE TRANSPORTER TYPE 1; HEME OXYGENASE (DECYCLIZING); HEMODYNAMICS; HYPERTENSION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; KIDNEY DISEASES; MALE; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; OXIDATIVE STRESS; POLYCYSTIC KIDNEY DISEASES; RATS; RATS, INBRED LEW; SPIN LABELS; SUPEROXIDE DISMUTASE; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84868145753     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12013     Document Type: Article

References (65)

1. Harris PC, Torres VE. Polycystic kidney disease. Annu. Rev. Med. 2009; 60: 321-37.
2. Wilson PD. Polycystic kidney disease. N. Engl. J. Med. 2004; 350: 151-64.
3. Eckardt KU, Bernhardt WM, Weidemann A et al. Role of hypoxia in the pathogenesis of renal disease. Kidney Int. Suppl. 2005; 68: S46-51.
4. Heyman SN, Khamaisi M, Rosen S, Rosenberger C. Renal parenchymal hypoxia, hypoxia response and the progression of chronic kidney disease. Am. J. Nephrol. 2008; 28: 998-1006.
5. Nangaku M. Chronic hypoxia and tubulointerstitial injury: A final common pathway to end-stage renal failure. J. Am. Soc. Nephrol. 2006; 17: 17-25.
6. Nangaku M, Eckardt KU. Hypoxia and the HIF system in kidney disease. J. Mol. Med. 2007; 85: 1325-30.
7. Belibi F, Zafar I, Ravichandran K et al. Hypoxia-inducible factor-1alpha (HIF-1alpha) and autophagy in polycystic kidney disease (PKD). Am. J. Physiol. Renal Physiol. 2011; 300: F1235-43.
8. Bernhardt WM, Wiesener MS, Weidemann A et al. Involvement of hypoxia-inducible transcription factors in polycystic kidney disease. Am. J. Pathol. 2007; 170: 830-42.
9. Yoshida T, Kuwahara M, Maita K, Harada T. Immunohistochemical study on hypoxia in spontaneous polycystic liver and kidney disease in rats. Exp. Toxicol. Pathol. 2001; 53: 123-8.
10. Harrap SB, Davies DL, Macnicol AM et al. Renal, cardiovascular and hormonal characteristics of young adults with autosomal dominant polycystic kidney disease. Kidney Int. 1991; 40: 501-8.
11. King BF, Torres VE, Brummer ME et al. Magnetic resonance measurements of renal blood flow as a marker of disease severity in autosomal-dominant polycystic kidney disease. Kidney Int. 2003; 64: 2214-21.
12. Meijer E, Rook M, Tent H et al. Early renal abnormalities in autosomal dominant polycystic kidney disease. Clin. J. Am. Soc. Nephrol. 2010; 5: 1091-8.
13. Torres VE, King BF, Chapman AB et al. Magnetic resonance measurements of renal blood flow and disease progression in autosomal dominant polycystic kidney disease. Clin. J. Am. Soc. Nephrol. 2007; 2: 112-20.
14. Bello-Reuss E, Holubec K, Rajaraman S. Angiogenesis in autosomal-dominant polycystic kidney disease. Kidney Int. 2001; 60: 37-45.
15. Wei W, Popov V, Walocha JA, Wen J, Bello-Reuss E. Evidence of angiogenesis and microvascular regression in autosomal-dominant polycystic kidney disease kidneys: A corrosion cast study. Kidney Int. 2006; 70: 1261-8.
16. Zeier M, Fehrenbach P, Geberth S, Mohring K, Waldherr R, Ritz E. Renal histology in polycystic kidney disease with incipient and advanced renal failure. Kidney Int. 1992; 42: 1259-65.
17. Haase VH. Oxygen regulates epithelial-to-mesenchymal transition: Insights into molecular mechanisms and relevance to disease. Kidney Int. 2009; 76: 492-9.
18. Higgins DF, Kimura K, Bernhardt WM et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J. Clin. Invest. 2007; 117: 3810-20.
19. Li X, Kimura H, Hirota K et al. Hypoxia reduces the expression and anti-inflammatory effects of peroxisome proliferator-activated receptor-gamma in human proximal renal tubular cells. Nephrol. Dial. Transplant. 2007; 22: 1041-51.
20. Schafer M, Schafer C, Ewald N, Piper HM, Noll T. Role of redox signaling in the autonomous proliferative response of endothelial cells to hypoxia. Circ. Res. 2003; 92: 1010-15.
21. Siddiqi L, Joles JA, Grassi G, Blankestijn PJ. Is kidney ischemia the central mechanism in parallel activation of the renin and sympathetic system? J. Hypertens. 2009; 27: 1341-9.
22. Menon V, Rudym D, Chandra P, Miskulin D, Perrone R, Sarnak M. Inflammation, oxidative stress, and insulin resistance in polycystic kidney disease. Clin. J. Am. Soc. Nephrol. 2011; 6: 7-13.
23. Maser RL, Vassmer D, Magenheimer BS, Calvet JP. Oxidant stress and reduced antioxidant enzyme protection in polycystic kidney disease. J. Am. Soc. Nephrol. 2002; 13: 991-9.
24. Vaziri ND. Roles of oxidative stress and antioxidant therapy in chronic kidney disease and hypertension. Curr. Opin. Nephrol. Hypertens. 2004; 13: 93-9.
25. Palm F, Nordquist L. Renal tubulointerstitial hypoxia: Cause and consequence of kidney dysfunction. Clin. Exp. Pharmacol. Physiol. 2011; 38: 424-30.
26. Palm F, Teerlink T, Hansell P. Nitric oxide and kidney oxygenation. Curr. Opin. Nephrol. Hypertens. 2009; 18: 68-73.
27. Torres VE, Bengal RJ, Litwiller RD, Wilson DM. Aggravation of polycystic kidney disease in Han:SPRD rats by buthionine sulfoximine. J. Am. Soc. Nephrol. 1997; 8: 1283-91.
28. Nagao S, Yamaguchi T, Kasahara M et al. Effect of probucol in a murine model of slowly progressive polycystic kidney disease. Am. J. Kidney Dis. 2000; 35: 221-6.
29. McCooke JC, Appels R, Barrero RA et al. A novel mutation causing nephronophthisis in the Lewis polycystic kidney rat localises to a conserved RCC1 domain in Nek8. BMC Genomics 2012; 13: 393.
30. Phillips JK, Hopwood D, Loxley RA et al. Temporal relationship between renal cyst development, hypertension and cardiac hypertrophy in a new rat model of autosomal recessive polycystic kidney disease. Kidney Blood Press. Res. 2007; 30: 129-44.
31. Harrison JL, Hildreth CM, Callahan SM, Goodchild AK, Phillips JK. Cardiovascular autonomic dysfunction in a novel rodent model of polycystic kidney disease. Auton. Neurosci. 2009; 152: 60-6.
32. Ng K, Hildreth CM, Avolio AP, Phillips JK. Angiotensin converting enzyme inhibitor limits pulse wave velocity and aortic calcification in a rat model of cystic renal disease. Am. J. Physiol. Renal Physiol. 2011; 301: F959-66.
33. Ng K, Hildreth CM, Phillips JK, Avolio AP. Aortic stiffness is associated with vascular calcification and remodeling in a chronic kidney disease rat model. Am. J. Physiol. Renal Physiol. 2011; 301: F1431-6.
34. Nordsmark M, Loncaster J, Aquino-Parsons C et al. Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas. Radiother. Oncol. 2003; 67: 35-44.
35. Rosenberger C, Rosen S, Paliege A, Heyman SN. Pimonidazole adduct immunohistochemistry in the rat kidney: Detection of tissue hypoxia. In: Hewitson TD, Becker GJ (eds). Methods in Molecular Biology: Kidney Research. Humana Press, Totowa. 2009; 161-74.
36. Zou AP, Li N, Cowley AW Jr. Production and actions of superoxide in the renal medulla. Hypertension 2001; 37: 547-53.
37. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1 . Annu. Rev. Pharmacol. Toxicol. 2010; 50: 323-54.
38. Hoppe CC, Evans RG, Moritz KM et al. Combined prenatal and postnatal protein restriction influences adult kidney structure, function, and arterial pressure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007; 292: R462-9.
39. Vlahos R, Stambas J, Bozinovski S, Broughton BR, Drummond GR, Selemidis S. Inhibition of Nox2 oxidase activity ameliorates influenza A virus-induced lung inflammation. PLoS Pathog. 2011; 7: e1001271.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-8.
41. Edwards MA, Loxley RA, Powers-Martin K et al. Unique levels of expression of N-methyl-d-aspartate receptor subunits and neuronal nitric oxide synthase in the rostral ventrolateral medulla of the spontaneously hypertensive rat. Brain Res. Mol. Brain Res. 2004; 129: 33-43.
42. Ahmed MN, Suliman HB, Folz RJ et al. Extracellular superoxide dismutase protects lung development in hyperoxia-exposed newborn mice. Am. J. Respir. Crit. Care Med. 2003; 167: 400-5.
43. Deng YM, Wu BJ, Witting PK, Stocker R. Probucol protects against smooth muscle cell proliferation by upregulating heme oxygenase-1. Circulation 2004; 110: 1855-60.
44. Ryter S, Kvam E, Richman L, Hartmann F, Tyrrell RM. A chromatographic assay for heme oxygenase activity in cultured human cells: Application to artificial heme oxygenase overexpression. Free Radic. Biol. Med. 1998; 24: 959-71.
45. Ludbrook J. Repeated measurements and multiple comparisons in cardiovascular research. Cardiovasc. Res. 1994; 28: 303-11.
46. Ludbrook J. On making multiple comparisons in clinical and experimental pharmacology and physiology. Clin. Exp. Pharmacol. Physiol. 1991; 18: 379-92.
47. Eiserich JP, Hristova M, Cross CE et al. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 1998; 391: 393-7.
48. Wilcox CS, Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol. Rev. 2008; 60: 418-69.
49. Rees MD, Bottle SE, Fairfull-Smith KE, Malle E, Whitelock JM, Davies MJ. Inhibition of myeloperoxidase-mediated hypochlorous acid production by nitroxides. Biochem. J. 2009; 421: 79-86.
50. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-iso prostaglandin F2alpha. Hypertension 1999; 33: 424-8.
51. Kelsen S, He X, Chade AR. Early superoxide scavenging accelerates renal microvascular rarefaction and damage in the stenotic kidney. Am. J. Physiol. Renal Physiol. 2012; 303: F576-83.
52. Haase VH. Hypoxia-inducible factors in the kidney. Am. J. Physiol. Renal Physiol. 2006; 291: F271-81.
53. Chauveau D, Duvic C, Chretien Y et al. Renal involvement in von Hippel-Lindau disease. Kidney Int. 1996; 50: 944-51.
54. Rankin EB, Tomaszewski JE, Haase VH. Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res. 2006; 66: 2576-83.
55. Tao Y, Kim J, Yin Y et al. VEGF receptor inhibition slows the progression of polycystic kidney disease. Kidney Int. 2007; 72: 1358-66.
56. Chabrashvili T, Tojo A, Onozato ML et al. Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension 2002; 39: 269-74.
57. Kinobe R, Ji Y, Nakatsu K. Peroxynitrite-mediated inactivation of heme oxygenases. BMC Pharmacol. 2004; 4: 26.
58. Kawakami T, Puri N, Sodhi K et al. Reciprocal effects of oxidative stress on heme oxygenase expression and activity contributes to reno-vascular abnormalities in EC-SOD knockout mice. Int. J. Hypertens. 2012; 2012: 740203.
59. Fujita H, Fujishima H, Morii T et al. Modulation of renal superoxide dismutase by telmisartan therapy in C57BL/6-Ins2 (Akita) diabetic mice. Hypertens. Res. 2012; 35: 213-20.
60. Jusman SW, Halim A, Wanandi SI, Sadikin M. Expression of hypoxia-inducible factor-1alpha (HIF-1alpha) related to oxidative stress in liver of rat-induced by systemic chronic normobaric hypoxia. Acta Med. Indones. 2010; 42: 17-23.
61. Furukawa Y, Urano T, Minamimura M, Nakajima M, Okuyama S, Furukawa S. 4-Methylcatechol-induced heme oxygenase-1 exerts a protective effect against oxidative stress in cultured neural stem/progenitor cells via PI3 kinase/Akt pathway. Biomed. Res. 2010; 31: 45-52.
62. Bateman RM, Tokunaga C, Kareco T, Dorscheid DR, Walley KR. Myocardial hypoxia-inducible HIF-1alpha, VEGF, and GLUT1 gene expression is associated with microvascular and ICAM-1 heterogeneity during endotoxemia. Am. J. Physiol. Heart Circ. Physiol. 2007; 293: H448-56.
63. Masamune A, Watanabe T, Kikuta K, Satoh K, Shimosegawa T. NADPH oxidase plays a crucial role in the activation of pancreatic stellate cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2008; 294: G99-108.
64. Khanna AK, Pieper GM. NADPH oxidase subunits (NOX-1, p22phox, Rac-1) and tacrolimus-induced nephrotoxicity in a rat renal transplant model. Nephrol. Dial. Transplant. 2007; 22: 376-85.
65. Duong TT, Antao S, Ellis NA, Myers SJ, Witting PK. Supplementation with a synthetic polyphenol limits oxidative stress and enhances neuronal cell viability in response to hypoxia-re-oxygenation injury. Brain Res. 2008; 1219: 8-18.