Supplemental hydrogen sulphide protects transplant kidney function and prolongs recipient survival after prolonged cold ischaemia-reperfusion injury by mitigating renal graft apoptosis and infl ammation

BJU International

Volumn 110, Issue 11 C, 2012, Pages

  Lobb, Ian ^a,b   Mok, Amy ^a,b   Lan, Zhu ^b,c   Liu, Weihua ^c   Garcia, Bertha ^c   Sener, Alp ^a,b,c  

^a Departments of Microbiology and Immunology   (Canada)

^b LONDON HEALTH SCIENCES CENTRE   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Graft function; Hydrogen sulphide; Ischaemia reperfusion injury; Organ preservation; Renal transplantation; Survival

Indexed keywords

HYDROGEN SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; COLD ISCHEMIA; CREATININE BLOOD LEVEL; DIET SUPPLEMENTATION; ENZYME ACTIVITY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KIDNEY FUNCTION; KIDNEY GRAFT; KIDNEY ISCHEMIA; KIDNEY TRANSPLANTATION; KIDNEY TUBULE NECROSIS; MACROPHAGE; MALE; NEPHRECTOMY; NEPHRITIS; NEUTROPHIL; NONHUMAN; OUTCOME ASSESSMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; RENAL PROTECTION; RENAL SYSTEM PARAMETERS; SURVIVAL; URINALYSIS; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; GRAFT SURVIVAL; INFLAMMATION; KIDNEY; LEWIS RAT; METHODOLOGY; ORGAN PRESERVATION; PATHOLOGY; REPERFUSION INJURY;

ANIMALS; APOPTOSIS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; GRAFT SURVIVAL; HYDROGEN SULFIDE; INFLAMMATION; KIDNEY; KIDNEY TRANSPLANTATION; MALE; ORGAN PRESERVATION; RATS; RATS, INBRED LEW; REPERFUSION INJURY;

MLCS; MLOWN;

EID: 84873254472     PISSN: 14644096     EISSN: 1464410X     Source Type: Journal    
DOI: 10.1111/j.1464-410X.2012.11526.x     Document Type: Article

References (42)

1. Tullius SG, Heemann U, Hancock WW, Azuma H, Tilney NL. Long-term kidney isografts develop functional and morphologic changes that mimic those of chronic allograft rejection. Ann Surg 1994; 220: 425-32; discussion 432-5
2. Halloran P, Aprile M. Factors infl uencing early renal function in cadaver kidney transplants. A casecontrol study. Transplantation 1988; 45: 122-7 (Pubitemid 18084623)
3. Hoffmann SC, Kampen RL, Amur S et al. Molecular and immunohistochemical characterization of the onset and resolution of human renal allograft ischemia-reperfusion injury. Transplantation 2002; 74: 916-23 (Pubitemid 35191236)
4. Dragun D, Hoff U, Park JK et al. Prolonged cold preservation augments vascular injury independent of renal transplant immunogenicity and function. Kidney Int 2001; 60: 1173-81 (Pubitemid 34205818)
5. Ojo AO, Wolfe RA, Held PJ, Port FK, Schmouder RL. Delayed graft function: risk factors and implications for renal allograft survival. Transplantation 1997; 63: 968-74 (Pubitemid 27173019)
6. Salahudeen AK, Haider N, May W. Cold ischemia and the reduced long-term survival of cadaveric renal allografts. Kidney Int 2004; 65: 713-8 7 2009 Annual Report of the U.S. Organ Procurement and Transplantation Network and the Scientifi c Registry of Transplant Recipients: Transplant Data 199-2008. Rockville, MD: Department of Health and Human Services, Health Resources and Services Administration, Healthcare Systems Bureau, Division of Transplantation, 2009
7. de Fijter JW, Mallat MJ, Doxiadis II et al. Increased immunogenicity and cause of graft loss of old donor kidneys. J Am Soc Nephrol 2001; 12: 1538-46 (Pubitemid 32666338)
8. Ojo AO, Hanson JA, Meier-Kriesche H et al. Survival in recipients of marginal cadaveric donor kidneys compared with other recipients and wait-listed transplant candidates. J Am Soc Nephrol 2001; 12: 589-97 (Pubitemid 32180029)
9. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 2007; 6: 917-35 (Pubitemid 350042399)
10. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol 2001; 33: 1897-918 (Pubitemid 33097270)
11. Payne D, Kubes P. Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosal permeability. Am J Physiol 1993; 265: G189-95 (Pubitemid 23223106)
12. Villarreal D, Grisham MB, Granger DN. Nitric oxide donors improve gut function after prolonged hypothermic ischemia. Transplantation 1995; 59: 685-9
13. Peralta C, Hotter G, Closa D, Gelpi E, Bulbena O, Rosello-Catafau J. Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: role of nitric oxide and adenosine. Hepatology 1997; 25: 934-7 (Pubitemid 27157137)
14. Nakao A, Toyokawa H, Tsung A et al. Ex vivo application of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemia/reperfusion injury. Am J Transplant 2006; 6: 2243-55 (Pubitemid 44359410)
15. Nakao A, Neto JS, Kanno S et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005; 5: 282-91 (Pubitemid 40179514)
16. 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
17. Neto JS, Nakao A, Kimizuka K et al. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol 2004; 287: F979-89 (Pubitemid 39391095)
18. Blackstone E, Morrison M, Roth MB. H2S induces a suspended animation-like state in mice. Science 2005; 308: 518 (Pubitemid 40570576)
19. Kamoun P. Endogenous production of hydrogen sulfi de in mammals. Amino Acids 2004; 26: 243-54 (Pubitemid 38829787)
20. Wang R. Two ' s company, three ' s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 2002; 16: 1792-8
21. Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfi de (H2S) protects against regional myocardial ischemia-reperfusion injury-Evidence for a role of K ATP channels. Basic Res Cardiol 2006; 101: 53-60 (Pubitemid 43323432)
22. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT. Hydrogen sulfi de is a mediator of cerebral ischemic damage. Stroke 2006; 37: 889-93 (Pubitemid 43731927)
23. Fu Z, Liu X, Geng B, Fang L, Tang C. Hydrogen sulfi de protects rat lung from ischemia-reperfusion injury. Life Sci 2008; 82: 1196-202
24. Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ. Hydrogen sulfi de attenuates hepatic ischemiareperfusion injury: role of antioxidant and antiapoptotic signaling. Am J Physiol Heart Circ Physiol 2008; 295: H801-6
25. 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
26. Lan Z, Ge W, Arp J et al. Induction of kidney allograft tolerance by soluble CD83 associated with prevalence of tolerogenic dendritic cells and indoleamine 2, 3-dioxygenase. Transplantation 2010; 90: 1286-93
27. Biguzas M, Jablonski P, Thomas AC et al. Evaluation of UW solution in a rat kidney preservation model. I. Effect of hydroxyethyl starch and electrolyte composition. T ransplantation 1990; 49: 872-5
28. Garcia-Criado FJ, Eleno N, Santos-Benito F et al. Protective effect of exogenous nitric oxide on the renal function and infl ammatory response in a model of ischemia-reperfusion. Transplantation 1998; 66: 982-90 (Pubitemid 28513374)
29. 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
30. Hosgood SA, Nicholson ML. Hydrogen sulphide ameliorates ischaemiareperfusion injury in an experimental model of non-heart-beating donor kidney transplantation. B r J Surg 2010; 97: 202-9
31. Lee CM, Carter JT, Alfrey EJ, Ascher NL, Roberts JP, Freise CE. Prolonged cold ischemia time obviates the benefi ts of 0 HLA mismatches in renal transplantation. A rch Surg 2000; 1 35: 1016-9; discussion 1019-20
32. Alabbasi AM, Tran K, Bloch M et al. The effects of molecules CORM-3 and H 2 S on renal protection during pulsatile perfusion. [ Abstract ]. Am J Transplant 2011; 11 ( Suppl. S2 ): 213-527
33. Geng B, Chang L, Pan C et al. Endogenous hydrogen sulfi de regulation of myocardial injury induced by isoproterenol. B iochem Biophys Res Commun 2004; 318: 756-63 (Pubitemid 38624219)
34. Sodha NR, Clements RT, Feng J et al. The effects of therapeutic sulfi de on myocardial apoptosis in response to ischemia-reperfusion injury. Eur J Cardiothorac Surg 2008; 33: 906-13
35. 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
36. Friedewald JJ, Rabb H. Infl ammatory cells in ischemic acute renal failure. Kidney Int 2004; 66: 486-91 (Pubitemid 38981983)
37. Hui Y, Du J, Tang C, Bin G, Jiang H. Changes in arterial hydrogen sulfi de (H(2)S) content during septic shock and endotoxin shock in rats. J Infect 2003; 47: 155-60 (Pubitemid 36896399)
38. 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)
39. Zhang J, Sio SW, Moochhala S, Bhatia M. Role of hydrogen sulfi de in severe burn injury-induced infl ammation in mice. Mol Med 2010; 16: 417-24
40. Whiteman M, Armstrong JS, Chu SH et al. The novel neuromodulator hydrogen sulfi de: an endogenous peroxynitrite ' scavenger. J Neurochem 2004; 90: 765-8 (Pubitemid 38989409)
41. 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
42. Rinaldi L, Gobbi G, Pambianco M, Micheloni C, Mirandola P, Vitale M. Hydrogen sulfi de prevents apoptosis of human PMN via inhibition of p38 and caspase 3. Lab Invest 2006; 86: 391-7