Detrimental effects of prolonged warm renal ischaemia-reperfusion injury are abrogated by supplemental hydrogen sulphide: An analysis using real-time intravital microscopy and polymerase chain reaction

BJU International

Volumn 110, Issue 11 C, 2012, Pages

  Zhu, Justin X G ^a   Kalbfleisch, Melanie ^b   Yang, Yi Xin ^e   Bihari, Relka ^c   Lobb, Ian ^b   Davison, Michael ^b   Mok, Amy ^c   Cepinskas, Gedaminas ^d   Lawendy, Abdel Rahman ^a,c   Sener, Alp ^a,b,c  

^a WESTERN UNIVERSITY   (Canada)

^b LHSC UH C4 208   (Canada)

^c Departments of Surgery London   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e Matthew Mailing Center for Translational Transplant Studies   (Canada)

Author keywords

Acute tubular necrosis; Hydrogen sulphide; Intravital microscopy; Ischaemia reperfusion injury; Warm ischaemia

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BUFFER; CHEMOKINE RECEPTOR CCR5; CREATININE; GAMMA INTERFERON; HYDROGEN SULFIDE; INTERLEUKIN 2; INTERLEUKIN 8; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER; MESSENGER RNA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD SAMPLING; CELL INFILTRATION; CREATININE BLOOD LEVEL; DIET SUPPLEMENTATION; ENZYME INHIBITION; HISTOLOGY; KIDNEY ISCHEMIA; KIDNEY TUBULE NECROSIS; LEUKOCYTE; LEUKOCYTE MIGRATION; MALE; MICROCIRCULATION; MICROSCOPY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REAL TIME INTRAVITAL MICROSCOPY; REAL TIME POLYMERASE CHAIN REACTION; RENAL PROTECTION; RENAL SYSTEM PARAMETERS; REPERFUSION INJURY; UNINEPHRECTOMY; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; GENETICS; ISCHEMIA; KIDNEY; KIDNEY TRANSPLANTATION; LEWIS RAT; METABOLISM; METHODOLOGY; VASCULARIZATION;

ANIMALS; BIOLOGICAL MARKERS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; HYDROGEN SULFIDE; KIDNEY; KIDNEY TRANSPLANTATION; MALE; RATS; RATS, INBRED LEW; REAL-TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; RNA, MESSENGER; WARM ISCHEMIA;

MLCS; MLOWN;

EID: 84873268960     PISSN: 14644096     EISSN: 1464410X     Source Type: Journal    
DOI: 10.1111/j.1464-410X.2012.11555.x     Document Type: Article

References (59)

1. Ojo AO, Wolfe RA, Held PJ, Port FK, Schmouder RL . Delayed graft function: risk factors and implications for renal allograft survival . T ransplantation 1997; 63: 968-74 (Pubitemid 27173019)
2. Saidi RF, Elias N, Kawai T et al . Outcome of kidney transplantation using expanded criteria donors and donation after cardiac death kidneys: realities and costs . Am J Transplant 2007; 7: 2769-74 (Pubitemid 350045769)
3. Burns AT, Davies DR, McLaren AJ, Cerundolo L, Morris PJ, Fuggle SV . Apoptosis in ischemia/reperfusion injury of human renal allografts . Transplantation 1998; 66: 872-6 (Pubitemid 28487460)
4. Jassem W, Roake J . The molecular and cellular basis of reperfusion injury following organ transplantation . Transplant Rev 1998; 12: 14-33 (Pubitemid 128654152)
5. Hosgood SA, Nicholson ML . Hydrogen sulphide ameliorates ischaemiareperfusion injury in an experimental model of non-heart-beating donor kidney transplantation . Br J Surg 2010; 97: 202-9
6. Burne-Taney MJ, Kofl er J, Yokota N, Weisfeldt M, Traystman RJ, Rabb H . Acute renal failure after whole body ischemia is characterized by infl ammation and T cell-mediated injury . Am J Physiol Renal Physiol 2003; 285: F87-94 (Pubitemid 36818465)
7. De Greef KE, Ysebaert DK, Ghielli M et al . Neutrophils and acute ischemiareperfusion injury . J Nephrol 1998; 11: 110-22
8. Nankivell BJ, Chapman JR . Chronic allograft nephropathy: current concepts and future directions . Transplantation 2006; 81: 643-54
9. Murphy SP, Porrett PM, Turka LA . Innate immunity in transplant tolerance and rejection . Immunol Rev 2011; 241: 39-48
10. Takashima S, Koukoulis G, Inokawa H, Sevala M, Egan TM . Inhaled nitric oxide reduces ischemia-reperfusion injury in rat lungs from non-heart-beating donors . J Thorac Cardiovasc Surg 2006; 132: 132-9
11. Sato K, Balla J, Otterbein L et al . Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants . J Immunol 2001; 166: 4185-94 (Pubitemid 32224952)
12. Caumartin Y, Stephen J, Deng JP et al . Carbon monoxide-releasing molecules protect against ischemia-reperfusion injury during kidney transplantation . Kidney Int 2011; 79: 1080-9
13. Alabbassi A, Tran KC, Bloch M et al . The effects of molecules CORM-3 and H2S on renal protection during pulsatile perfusion . Am J Transplant 2011; S2: A1614
14. Lobb I, Mok A, Lan Z, Wang H, Sener A . Supplemental hydrogen sulphide improves renal transplant function and survival following prolonged cold storage . Am J Transplant 2011; S2: A1123-5
15. Elrod JW, Calvert JW, Morrison J et al . Hydrogen sulfi de attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function . Proc Natl Acad Sci USA 2007; 104: 15560-5 (Pubitemid 47502956)
16. Nicholson CK, Calvert JW . Hydrogen sulfi de and ischemia-reperfusion injury . Pharmacol Res 2010; 62: 289-97
17. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, Zhu YC . The novel proangiogenic effect of hydrogen sulfi de is dependent on Akt phosphorylation . Cardiovasc Res 2007; 76: 29-40 (Pubitemid 47362041)
18. Abe K, Kimura H . The possible role of hydrogen sulfi de as an endogenous neuromodulator . J Neurosci 1996; 16: 1066-71 (Pubitemid 26140863)
19. Johansen D, Ytrehus K, Baxter GF . Exogenous hydrogen sulfi de (H 2 S) protects against regional myocardial ischemia-reperfusion injury-evidence for a role of K ATP channels . Basic Res Cardiol 2006; 101: 53-60 (Pubitemid 43323432)
20. Henderson PW, Singh SP, Belkin D et al . Hydrogen sulfi de protects against ischemia-reperfusion injury in an in vitro model of cutaneous tissue transplantation . J Surg Res 2010; 1 59: 451-5
21. Bos EM, Leuvenink HG, Snijder PM et al . Hydrogen sulfi de-induced hypometabolism prevents renal ischemia/reperfusion injury . J Am Soc Nephrol 2009; 20: 1901-5
22. Tripatara P, Patel NS, Collino M et al . Generation of endogenous hydrogen sulfi de by cystathionine gamma-lyase limits renal ischemia/reperfusion injury and dysfunction . Lab Invest 2008; 88: 1038-48
23. Yamamoto T, Tada T, Brodsky SV et al . Intravital videomicroscopy of peritubular capillaries in renal ischemia . Am J Physiol Renal Physiol 2002; 282: F1150-5 (Pubitemid 34654481)
24. Ott MC, Scott JR, Bihari A et al . Inhalation of carbon monoxide prevents liver injury and infl ammation following hind limb ischemia/reperfusion . FASEB J 2005; 19: 106-8 (Pubitemid 40069933)
25. Wunder C, Scott JR, Lush CW et al . Heme oxygenase modulates hepatic leukocyte sequestration via changes in sinusoidal tone in systemic infl ammation in mice . Microvasc Res 2004; 68: 20-9 (Pubitemid 38813340)
26. Johns DG, Ao Z, Willette RN, Macphee CH, Douglas SA . Role of p38 MAP kinase in postcapillary venule leukocyte adhesion induced by ischemia/reperfusion injury . Pharmacol Res 2005; 51: 463-71 (Pubitemid 40321015)
27. Brock RW, Lawlor DK, Harris KA, Potter RF . Initiation of remote hepatic injury in the rat: interactions between Kupffer cells, tumor necrosis factoralpha, and microvascular perfusion . Hepatology 1999; 30: 137-42 (Pubitemid 29300579)
28. Caradec J, Sirab N, Keumeugni C et al . ' Desperate house genes ': the dramatic example of hypoxia . Br J Cancer 2010; 102: 1037-43
29. Huber AR, Kunkel SL, Todd RF III, Weiss SJ . Regulation of transendothelial neutrophil migration by endogenous interleukin-8 . S cience 1991; 254: 99-102 (Pubitemid 21917325)
30. Eldaif SM, Deneve JA, Wang NP et al . Attenuation of renal ischemiareperfusion injury by postconditioning involves adenosine receptor and protein kinase C activation . Transpl Int 2010; 23: 217-26
31. Tripatara P, Patel NS, Brancaleone V et al . Characterisation of cystathionine gamma-lyase/hydrogen sulphide pathway in ischaemia/reperfusion injury of the mouse kidney: an in vivo study . Eur J Pharmacol 2009; 606: 205-9
32. Cassis P, Azzollini N, Solini S et al . Both darbepoetin alfa and carbamylated erythropoietin prevent kidney graft dysfunction due to ischemia/reperfusion in rats . T ransplantation 2011; 9 2: 271-9
33. Tucci S Jr, Borelli-Bovo TJ, Cologna AJ, Tiraboschi RB, Martins AC, Roselino JE . Calcium channel blocker and renal mitochondrial function in warm renal ischemia . Int Braz J Urol 2005; 31: 384-9 (Pubitemid 41288453)
34. Francis RC, Vaporidi K, Bloch KD, Ichinose F, Zapol WM . Protective and detrimental effects of sodium sulfi de and hydrogen sulfi de in murine ventilator-induced lung injury . Anesthesiology 2011; 115: 1012-21
35. Yates PJ, Hosgood SA, Nicholson ML . A biphasic response to nitric oxide donation in an ex vivo model of donation after cardiac death renal transplantation . J Surg Res 2012; 175: 316-21
36. Patschan D, Patschan S, M ü ller GA . Infl ammation and microvasculopathy in renal ischemia reperfusion injury . J Transplant 2012; 2012: 764154
37. Zhao W, Zhang J, Lu Y, Wang R . The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener . EMBO J 2001; 20: 6008-16 (Pubitemid 33049276)
38. Cao C, Lee-Kwon W, Silldorff EP, Pallone TL . KATP channel conductance of descending vasa recta pericytes . Am J Physiol Renal Physiol 2005; 289: F1235-45 (Pubitemid 41681359)
39. Beltowski J . Hypoxia in the renal medulla: implications for hydrogen sulfi de signaling . J Pharmacol Exp Ther 2010; 334: 358-63
40. Daemen MA, van ' t Veer C, Denecker G et al . Inhibition of apoptosis induced by ischemia-reperfusion prevents infl ammation . J Clin Invest 1999; 104: 541-9
41. Mkaddem SB, Bens M, Vandewalle A . Differential activation of Toll-like receptor-mediated apoptosis induced by hypoxia . Oncotarget 2010; 1: 741-50
42. Wu H, Chen G, Wyburn KR et al . TLR4 activation mediates kidney ischemia/reperfusion injury . J Clin Invest 2007; 117: 2847-59 (Pubitemid 47529615)
43. Donnahoo KK, Shames BD, Harken AH, Meldrum DR . Review article: the role of tumor necrosis factor in renal ischemiareperfusion injury . J Urol 1999; 162: 196-203 (Pubitemid 29420927)
44. Jang HR, Ko GJ, Wasowska BA, Rabb H . The interaction between ischemiareperfusion and immune responses in the kidney . J Mol Med (Berl) 2009; 87: 859-64
45. Donnahoo KK, Meng X, Ayala A, Cain MP, Harken AH, Meldrum DR . Early kidney TNF-alpha expression mediates neutrophil infi ltration and injury after renal ischemia-reperfusion . Am J Physiol 1999; 277: R922-9 (Pubitemid 29458168)
46. Mariggio MA, Pettini F, Fumarulo R . Sulfi de infl uence on polymorphonuclear functions: a possible role for Ca2 + involvement . I mmunopharmacol Immunotoxicol 1997; 19: 393-404 (Pubitemid 27323157)
47. Yusof M, Kamada K, Kalogeris T, Gaskin FS, Korthuis RJ . Hydrogen sulfi de triggers late-phase preconditioning in postischemic small intestine by an NO-and p38 MAPK-dependent mechanism . A m J Physiol Heart Circ Physiol 2009; 296: H868-76
48. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL . Hydrogen sulfi de is an endogenous modulator of leukocyte-mediated infl ammation . FASEB J 2006; 20: 2118-20
49. Linfert D, Chowdhry T, Rabb H . Lymphocytes and ischemia-reperfusion injury . Transplant Rev (Orlando) 2009; 23: 1-10
50. Ko GJ, Linfert D, Jang HR et al . Transcriptional analysis of infi ltrating T cells in kidney ischemia-reperfusion injury reveals a pathophysiological role for CCR5 . Am J Physiol Renal Physiol 2012; 302: F762-73
51. Serrick C, La FS, Giaid A, Shennib H . Cytokine interleukin-2, tumor necrosis factor-alpha, and interferon-gamma release after ischemia/reperfusion injury in a novel lung autograft animal model . Am J Respir Crit Care Med 1995; 152: 277-82
52. Vaghasiya JD, Sheth NR, Bhalodia YS, Jivani NP . Exaggerated liver injury induced by renal ischemia reperfusion in diabetes: effect of exenatide . Saudi J Gastroenterol 2010; 16: 174-80
53. Golab F, Kadkhodaee M, Zahmatkesh M et al . Ischemic and non-ischemic acute kidney injury cause hepatic damage . K idney Int 2009; 7 5: 783-92
54. Hirata K, Ikeda S, Honma T et al . Sepsis and cholestasis: basic fi ndings in the sinusoid and bile canaliculus . J Hepatobiliary Pancreat Surg 2001; 8: 20-6 (Pubitemid 33690510)
55. Sivarajah A, Collino M, Yasin M et al . Anti-apoptotic and anti-infl ammatory effects of hydrogen sulfi de in a rat model of regional myocardial I/R . Shock 2009; 31: 267-74
56. Bhatia M, Wong FL, Fu D, Lau HY, Moochhala SM, Moore PK . Role of hydrogen sulfi de in acute pancreatitis and associated lung injury . FASEB J 2005; 19: 623-5 (Pubitemid 40471265)
57. Li L, Bhatia M, Zhu YZ et al . Hydrogen sulfi de is a novel mediator of lipopolysaccharide-induced infl ammation in the mouse . FASEB J 2005; 19: 1196-8 (Pubitemid 40946463)
58. Dal-Secco D, Cunha TM, Freitas A et al . Hydrogen sulfi de augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels . J Immunol 2008; 181: 4287-98
59. Hegde A, Bhatia M . Hydrogen sulfi de in infl ammation: friend or foe? Infl amm Allergy Drug Targets 2011; 10: 118-22