An Evaluation of Ischaemic Preconditioning as a Method of Reducing Ischaemia Reperfusion Injury in Liver Surgery and Transplantation

Francis P Robertson, Barry J Fuller, Brian R Davidson, Francis P Robertson, Barry J Fuller, Brian R Davidson

Abstract

Liver Ischaemia Reperfusion (IR) injury is a major cause of post-operative liver dysfunction, morbidity and mortality following liver resection surgery and transplantation. There are no proven therapies for IR injury in clinical practice and new approaches are required. Ischaemic Preconditioning (IPC) can be applied in both a direct and remote fashion and has been shown to ameliorate IR injury in small animal models. Its translation into clinical practice has been difficult, primarily by a lack of knowledge regarding the dominant protective mechanisms that it employs. A review of all current studies would suggest that IPC/RIPC relies on creating a small tissue injury resulting in the release of adenosine and l-arginine which act through the Adenosine receptors and the haem-oxygenase and endothelial nitric oxide synthase systems to reduce hepatocyte necrosis and improve the hepatic microcirculation post reperfusion. The next key step is to determine how long the stimulus requires to precondition humans to allow sufficient injury to occur to release the potential mediators. This would open the door to a new therapeutic chapter in this field.

Keywords: Ischaemic Preconditioning; Ischaemic Reperfusion injury; Remote Ischaemic Preconditioning.

Conflict of interest statement

The authors declare no conflict of interest

Figures

Figure 1
Figure 1
Previously identified mechanism of IPC. Mechanisms identified in the setting of liver IR injury are in black whilst those not implicated/researched are in white.
Figure 2
Figure 2
Protective mechanisms of adenosine release following Ischaemic Preconditioning (IPC).

References

    1. Veteläinen R., van Vliet A., Gouma D.J., van Gulik T.M. Steatosis as a risk factor in liver surgery. Ann. Surg. 2007;245:20–30. doi: 10.1097/.
    1. Selzner M., Clavien P.-A. Fatty liver in liver transplantation and surgery. Semin. Liver Dis. 2001;21:105–113. doi: 10.1055/s-2001-12933.
    1. Callaghan C.J., Charman S.C., Muiesan P., Powell J.J., Gimson A.E., van der Meulen J.H.P. Outcomes of transplantation of livers from donation after circulatory death donors in the UK: A cohort study. BMJ Open. 2013;3:e003287. doi: 10.1136/bmjopen-2013-003287.
    1. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124–1136. doi: 10.1161/01.CIR.74.5.1124.
    1. Przyklenk K., Bauer B., Ovize M., Kloner R.A., Whittaker P. Regional ischemic “preconditioning” protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87:893–899. doi: 10.1161/01.CIR.87.3.893.
    1. Clavien P.A., Yadav S., Sindram D., Bentley R.C. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann. Surg. 2000;232:155–162. doi: 10.1097/00000658-200008000-00001.
    1. Clavien P.-A., Selzner M., Rüdiger H.A., Graf R., Kadry Z., Rousson V., Jochum W. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann. Surg. 2003;238:843–852. doi: 10.1097/01.sla.0000098620.27623.7d.
    1. Kanoria S., Robertson F.P., Mehta N.N., Fusai G., Sharma D., Davidson B.R. Effect of Remote Ischaemic Preconditioning on Liver Injury in Patients Undergoing Major Hepatectomy for Colorectal Liver Metastasis: A Pilot Randomised Controlled Feasibility Trial. World J. Surg. 2016 doi: 10.1007/s00268-016-3823-4.
    1. O’Neill S., Leuschner S., McNally S.J., Garden O.J., Wigmore S.J., Harrison E.M. Meta-analysis of ischaemic preconditioning for liver resections. Br. J. Surg. 2013;100:1689–1700. doi: 10.1002/bjs.9277.
    1. Robertson F.P., Magill L.J., Wright G.P., Fuller B., Davidson B.R. A systematic review and meta-analysis of donor ischaemic preconditioning in liver transplantation. Transpl. Int. 2016 doi: 10.1111/tri.12849.
    1. McCafferty K., Forbes S., Thiemermann C., Yaqoob M.M. The challenge of translating ischemic conditioning from animal models to humans: The role of comorbidities. Dis. Model. Mech. 2014;7:1321–1333. doi: 10.1242/dmm.016741.
    1. Hausenloy D.J., Candilio L., Evans R., Ariti C., Jenkins D.P., Kolvekar S., Knight R., Kunst G., Laing C., Nicholas J., et al. Remote Ischemic Preconditioning and Outcomes of Cardiac Surgery. N. Engl. J. Med. 2015;373:1408–1417. doi: 10.1056/NEJMoa1413534.
    1. Meybohm P., Bein B., Brosteanu O., Cremer J., Gruenewald M., Stoppe C., Coburn M., Schaelte G., Böning A., Niemann B., et al. A Multicenter Trial of Remote Ischemic Preconditioning for Heart Surgery. N. Engl. J. Med. 2015;373:1397–1407. doi: 10.1056/NEJMoa1413579.
    1. Robertson F.P., Goswami R., Wright G.P., Imber C., Sharma D., Malago M., Fuller B.J., Davidson B.R. Remote ischaemic preconditioning in orthotopic liver transplantation (RIPCOLT trial): A pilot randomized controlled feasibility study. HPB. 2017 doi: 10.1016/j.hpb.2017.05.005.
    1. Peralta C., Hotter G., Closa D., Gelpí 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;25:934–937. doi: 10.1002/hep.510250424.
    1. Peralta C., Closa D., Xaus C., Gelpí E., Roselló-catafau J., Hotter G. Hepatic preconditioning in rats is defined by a balance of adenosine and xanthine. Hepatology. 1998;28:768–773. doi: 10.1002/hep.510280325.
    1. Nakayama H., Yamamoto Y., Kume M., Yamagami K., Yamamoto H., Kimoto S., Ishikawa Y., Ozaki N., Shimahara Y., Yamaoka Y. Pharmacologic stimulation of adenosine A2 receptor supplants ischemic preconditioning in providing ischemic tolerance in rat livers. Surgery. 1999;126:945–954. doi: 10.1016/S0039-6060(99)70037-1.
    1. Peralta C., Hotter G., Closa D., Prats N., Xaus C., Gelpí E., Roselló-Catafau J. The protective role of adenosine in inducing nitric oxide synthesis in rat liver ischemia preconditioning is mediated by activation of adenosine A2 receptors. Hepatology. 1999;29:126–132. doi: 10.1002/hep.510290104.
    1. Ajamieh H.H., Candelario-Jalil E., Fernández O.S.L., Gerbes A.L. Ischaemic and pharmacological preconditionings protect liver via adenosine and redox status following hepatic ischaemia/reperfusion in rats. Clin. Sci. 2008;115:69–77. doi: 10.1042/CS20070415.
    1. Schauer R., Gerbes A.L., Vonier D., op den Winkel M., Fraunberger P., Bilzer M. Induction of cellular resistance against Kupffer cell–derived oxidant stress: A novel concept of hepatoprotection by ischemic preconditioning. Hepatology. 2003;37:286–295. doi: 10.1053/jhep.2003.50064.
    1. Chouker A., Ohta A., Martignoni A., Lukashev D., Zacharia L.C., Jackson E.K., Schnermann J., Ward J.M., Kaufmann I., Klaunberg B., et al. In Vivo Hypoxic Preconditioning Protects From Warm Liver Ischemia-Reperfusion Injury Through the Adenosine A2B Receptor. Transplantation. 2012;94:894–902. doi: 10.1097/TP.0b013e31826a9a46.
    1. Koti R.S., Tsui J., Lobos E., Yang W., Seifalian A.M., Davidson B.R. Nitric oxide synthase distribution and expression with ischemic preconditioning of the rat liver. FASEB J. 2005;19:1155–1157. doi: 10.1096/fj.04-3220fje.
    1. Abu-Amara M., Yang S.Y., Quaglia A., Rowley P., Fuller B., Seifalian A., Davidson B. Role of endothelial nitric oxide synthase in remote ischemic preconditioning of the mouse liver. Liver Transpl. 2011;17:610–619. doi: 10.1002/lt.22272.
    1. Carini R., De Cesaris M.G., Splendore R., Bagnati M., Albano E. Ischemic preconditioning reduces Na+ accumulation and cell killing in isolated rat hepatocytes exposed to hypoxia. Hepatology. 2000;31:166–172. doi: 10.1002/hep.510310125.
    1. Carini R., De Cesaris M.G., Splendore R., Vay D., Domenicotti C., Nitti M.P., Paola D., Pronzato M.A., Albano E. Signal pathway involved in the development of hypoxic preconditioning in rat hepatocytes. Hepatology. 2001;33:131–139. doi: 10.1053/jhep.2001.21050.
    1. Ricciardi R., Meyers W.C., Schaffer B.K., Kim R.D., Shah S.A., Wheeler S.M., Donohue S.E., Sheth K.R., Callery M.P., Chari R.S. Protein kinase C inhibition abrogates hepatic ischemic preconditioning responses. J. Surg. Res. 2001;97:144–149. doi: 10.1006/jsre.2001.6139.
    1. Ricciardi R., Shah S.A., Wheeler S.M., Quarfordt S.H., Callery M.P., Meyers W.C., Chari R.S. Regulation of NFκB in hepatic ischemic preconditioning. J. Am. Coll. Surg. 2002;195:319–326. doi: 10.1016/S1072-7515(02)01229-2.
    1. Lai I.-R., Chang K.-J., Chen C.-F., Tsai H.-W. Transient limb ischemia induces remote preconditioning in liver among rats: The protective role of heme oxygenase-1. Transplantation. 2006;81:1311–1317. doi: 10.1097/01.tp.0000203555.14546.63.
    1. Datta G., Luong T.V., Fuller B.J., Davidson B.R. Endothelial nitric oxide synthase and heme oxygenase-1 act independently in liver ischemic preconditioning. J. Surg. Res. 2014;186:417–428. doi: 10.1016/j.jss.2013.08.019.
    1. Wang Y., Shen J., Xiong X., Xu Y., Zhang H., Huang C., Tian Y., Jiao C., Wang X., Li X. Remote ischemic preconditioning protects against liver ischemia-reperfusion injury via heme oxygenase-1-induced autophagy. PLoS ONE. 2014;9:e98834. doi: 10.1371/journal.pone.0098834.
    1. Kinsey G.R., Huang L., Vergis A.L., Li L., Okusa M.D. Regulatory T cells contribute to the protective effect of ischemic preconditioning in the kidney. Kidney Int. 2010;77:771–780. doi: 10.1038/ki.2010.12.
    1. Cho W.Y., Choi H.M., Lee S.Y., Kim M.G., Kim H.-K., Jo S.-K. The role of Tregs and CD11c(+) macrophages/dendritic cells in ischemic preconditioning of the kidney. Kidney Int. 2010;78:981–992. doi: 10.1038/ki.2010.266.
    1. Devey L.R., Richards J.A., O’Connor R.A., Borthwick G., Clay S., Howie A.F., Wigmore S.J., Anderton S.M., Howie S.E.M. Ischemic preconditioning in the liver is independent of regulatory T cell activity. PLoS ONE. 2012;7:e49647. doi: 10.1371/journal.pone.0049647.
    1. Peralta C., Prats N., Xaus C., Gelpí E., Roselló-Catafau J. Protective effect of liver ischemic preconditioning on liver and lung injury induced by hepatic ischemia-reperfusion in the rat. Hepatology. 1999;30:1481–1489. doi: 10.1002/hep.510300622.
    1. Peralta C., Fernández L., Panés J., Prats N., Sans M., Piqué J.M., Gelpí E., Roselló-Catafau J., Roselló-Catafau J. Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockade of tumor necrosis factor–induced P-selectin up-regulation in the rat. Hepatology. 2001;33:100–113. doi: 10.1053/jhep.2001.20529.
    1. Glanemann M., Vollmar B., Nussler A.K., Schaefer T., Neuhaus P., Menger M.D. Ischemic preconditioning protects from hepatic ischemia/reperfusion-injury by preservation of microcirculation and mitochondrial redox-state. J. Hepatol. 2003;38:59–66. doi: 10.1016/S0168-8278(02)00327-6.
    1. Arai M., Ikeda H., Tomiya T., Yanase M., Inoue Y., Nagashima K., Nishikawa T., Watanabe N., Omata M., Fujiwara K., et al. Ischemic preconditioning protects hepatocytes via reactive oxygen species derived from Kupffer cells in rats. Gastroenterology. 2004;127:1488–1496. doi: 10.1053/J.GASTRO.2004.07.023.
    1. Funaki H., Shimizu K., Harada S.-I., Tsuyama H., Fushida S., Tani T., Miwa K. Essential role for nuclear factor kappaB in ischemic preconditioning for ischemia-reperfusion injury of the mouse liver. Transplantation. 2002;74:551–556. doi: 10.1097/00007890-200208270-00021.
    1. Zhang S.-J., Zhu C.-J., Zhao Y.-F., Li J., Guo W.-Z. Different ischemic preconditioning for rat liver graft: Protection and mechanism. Hepatobiliary Pancreat. Dis. Int. 2003;2:509–512.
    1. Yao A., Li X., Pu L., Zhong J., Liu X., Yu Y., Zhang F., Kong L., Sun B., Wang X., et al. Impaired hepatic regeneration by ischemic preconditioning in a rat model of small-for-size liver transplantation. Transpl. Immunol. 2007;18:37–43. doi: 10.1016/j.trim.2007.02.002.
    1. Koneru B., Shareef A., Dikdan G., Desai K., Klein K.M., Peng B., Wachsberg R.H., de la Torre A.N., Debroy M., Fisher A., et al. The ischemic preconditioning paradox in deceased donor liver transplantation—Evidence from a prospective randomized single blind clinical trial. Am. J. Transplant. 2007;7:2788–2796. doi: 10.1111/j.1600-6143.2007.02009.x.
    1. Guimarães Filho M.A.C., Cortez E., Garcia-Souza É.P., Soares V.M., Moura A.S., Carvalho L., Maya M.C.A., Pitombo M.B. Effect of remote ischemic preconditioning in the expression of IL-6 and IL-10 in a rat model of liver ischemia-reperfusion injury. Acta Cir. Bras. 2015;30:452–460. doi: 10.1590/S0102-865020150070000002.
    1. Li D.-Y., Shi X.-J., Li W., Sun X.-D., Wang G.-Y. Ischemic preconditioning and remote ischemic preconditioning provide combined protective effect against ischemia/reperfusion injury. Life Sci. 2016;150:76–80. doi: 10.1016/j.lfs.2016.02.077.
    1. Hausenloy D., Yellon D.M. New directions for protecting the heart against ischaemia–reperfusion injury: Targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc. Res. 2004;61:448–460. doi: 10.1016/j.cardiores.2003.09.024.
    1. Marber M.S., Latchman D.S., Walker J.M., Yellon D.M. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation. 1993;88:1264–1272. doi: 10.1161/01.CIR.88.3.1264.
    1. Kuzuya T., Hoshida S., Yamashita N., Fuji H., Oe H., Hori M., Kamada T., Tada M. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ. Res. 1993;72:1293–1299. doi: 10.1161/01.RES.72.6.1293.
    1. Hausenloy D.J., Yellon D.M. The second window of preconditioning (SWOP) where are we now? Cardiovasc. Drugs Ther. 2010;24:235–254. doi: 10.1007/s10557-010-6237-9.
    1. Lim S.Y., Hausenloy D.J. Remote ischemic conditioning: From bench to bedside. Front. Physiol. 2012;3:27. doi: 10.3389/fphys.2012.00027.
    1. Fredholm B.B. Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ. 2007;14:1315–1323. doi: 10.1038/sj.cdd.4402132.
    1. Fredholm B.B., IJzerman A.P., Jacobson K.A., Klotz K.N., Linden J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 2001;53:527–552.
    1. Laubach V.E., French B.A., Okusa M.D. Targeting of adenosine receptors in ischemia-reperfusion injury. Expert Opin. Ther. Targets. 2011;15:103–118. doi: 10.1517/14728222.2011.541441.
    1. Todo S., Zhu Y., Zhang S., Jin M.B., Ishizaki N., Tanaka H., Subbotin V., Starzl T.E. Attenuation of ischemic liver injury by augmentation of endogenous adenosine. Transplantation. 1997;63:217–223. doi: 10.1097/00007890-199701270-00007.
    1. Li J.M., Fenton R.A., Cutler B.S., Dobson J.G. Adenosine enhances nitric oxide production by vascular endothelial cells. Am. J. Physiol. 1995;269:C519–C523.
    1. Koneru B., Fisher A., He Y., Klein K.M., Skurnick J., Wilson D.J., de la Torre D.N., Merchant A., Arora R., Samanta A.K., et al. Ischemic preconditioning in deceased donor liver transplantation: A prospective randomized clinical trial of safety and efficacy. Liver Transplant. 2005;11:196–202. doi: 10.1002/lt.20315.
    1. Jassem W., Fuggle S.V., Cerundolo L., Heaton N.D., Rela M. Ischemic preconditioning of cadaver donor livers protects allografts following transplantation. Transplantation. 2006;81:169–174. doi: 10.1097/01.tp.0000188640.05459.37.
    1. Kim J., Kim M., Song J.H., Lee H.T. Endogenous A1 adenosine receptors protect against hepatic ischemia reperfusion injury in mice. Liver Transplant. 2008;14:845–854. doi: 10.1002/lt.21432.
    1. Magata S., Taniguchi M., Suzuki T., Shimamura T., Fukai M., Furukawa H., Fujita M., Todo S. The Effect of Antagonism of Adenosine A1 Receptor Against Ischemia and Reperfusion Injury of the Liver. J. Surg. Res. 2007;139:7–14. doi: 10.1016/j.jss.2006.09.021.
    1. Ben-Ari Z., Pappo O., Sulkes J., Cheporko Y., Vidne B.A., Hochhauser E. Effect of adenosine A2A receptor agonist (CGS) on ischemia/reperfusion injury in isolated rat liver. Apoptosis. 2005;10:955–962. doi: 10.1007/s10495-005-0440-3.
    1. Thurman R.G., Lemasters J.J., Arai M., Thurman R.G., Lemasters J.J. Contribution of adenosine A(2) receptors and cyclic adenosine monophosphate to protective ischemic preconditioning of sinusoidal endothelial cells against Storage/Reperfusion injury in rat livers. Hepatology. 2000;32:297–302. doi: 10.1053/jhep.2000.8896.
    1. Day Y.-J., Marshall M.A., Huang L., McDuffie M.J., Okusa M.D., Linden J. Protection from ischemic liver injury by activation of A2A adenosine receptors during reperfusion: inhibition of chemokine induction. AJP Gastrointest. Liver Physiol. 2004;286:G285–G293. doi: 10.1152/ajpgi.00348.2003.
    1. Lappas C.M., Day Y.-J., Marshall M.A., Engelhard V.H., Linden J. Adenosine A2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation. J. Exp. Med. 2006;203:2639–2648. doi: 10.1084/jem.20061097.
    1. Zimmerman M.A., Grenz A., Tak E., Kaplan M., Ridyard D., Brodsky K.S., Mandell M.S., Kam I., Eltzschig H.K. Signaling through hepatocellular A2B adenosine receptors dampens ischemia and reperfusion injury of the liver. Proc. Natl. Acad. Sci. USA. 2013;110:12012–12017. doi: 10.1073/pnas.1221733110.
    1. Abu-Amara M., Yang S.Y., Seifalian A., Davidson B., Fuller B. The nitric oxide pathway—Evidence and mechanisms for protection against liver ischaemia reperfusion injury. Liver Int. 2012;32:531–543. doi: 10.1111/j.1478-3231.2012.02755.x.
    1. Abu-Amara M., Yang S.Y., Quaglia A., Rowley P., Tapuria N., Seifalian A.M., Fuller B.J., Davidson B.R. Effect of remote ischemic preconditioning on liver ischemia/reperfusion injury using a new mouse model. Liver Transpl. 2011;17:70–82. doi: 10.1002/lt.22204.
    1. Peralta C., Rull R., Rimola A., Deulofeu R., Roselló-Catafau J., Gelpí E., Rodés J. Endogenous nitric oxide and exogenous nitric oxide supplementation in hepatic ischemia-reperfusion injury in the rat. Transplantation. 2001;71:529–536. doi: 10.1097/00007890-200102270-00008.
    1. Hines I.N., Kawachi S., Harada H., Pavlick K.P., Hoffman J.M., Bharwani S., Wolf R.E., Grisham M.B. Role of nitric oxide in liver ischemia and reperfusion injury. Mol. Cell. Biochem. 2002;234:229–237. doi: 10.1023/A:1015952926016.
    1. Hines I.N., Harada H., Flores S., Gao B., McCord J.M., Grisham M.B. Endothelial nitric oxide synthase protects the post-ischemic liver: potential interactions with superoxide. Biomed. Pharmacother. 2005;59:183–189. doi: 10.1016/j.biopha.2005.03.011.
    1. Kawachi S., Hines I.N., Laroux F.S., Hoffman J., Bharwani S., Gray L., Leffer D., Grisham M.B. Nitric Oxide Synthase and Postischemic Liver Injury. Biochem. Biophys. Res. Commun. 2000;276:851–854. doi: 10.1006/bbrc.2000.3559.
    1. Lee V.G., Johnson M.L., Baust J., Laubach V.E., Watkins S.C., Billiar T.R. The roles of iNOS in liver ischemia-reperfusion injury. Shock. 2001;16:355–360. doi: 10.1097/00024382-200116050-00006.
    1. Theruvath T.P., Zhong Z., Currin R.T., Ramshesh V.K., Lemasters J.J. Endothelial nitric oxide synthase protects transplanted mouse livers against storage/reperfusion injury: Role of vasodilatory and innate immunity pathways. Transplant. Proc. 2006;38:3351–3357. doi: 10.1016/j.transproceed.2006.10.171.
    1. Duranski M.R., Elrod J.W., Calvert J.W., Bryan N.S., Feelisch M., Lefer D.J. Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. AJP Hear. Circ. Physiol. 2006;291:H2980–H2986. doi: 10.1152/ajpheart.01173.2005.
    1. Serracino-Inglott F., Virlos I.T., Habib N.A., Williamson R.C.N., Mathie R.T. Adenosine preconditioning attenuates hepatic reperfusion injury in the rat by preventing the down-regulation of endothelial nitric oxide synthase. BMC Gastroenterol. 2002;2:22. doi: 10.1186/1471-230X-2-22.
    1. Wang L.-M., Tian X.-F., Song Q.-Y., Gao Z.-M., Luo F.-W., Yang C.-M. Expression and role of inducible nitric oxide synthase in ischemia-reperfusion liver in rats. Hepatobiliary Pancreat. Dis. Int. 2003;2:252–258.
    1. Zwacka R.M., Zhang Y., Halldorson J., Schlossberg H., Dudus L., Engelhardt J.F. CD4(+) T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver. J. Clin. Investig. 1997;100:279–289. doi: 10.1172/JCI119533.
    1. Bradham C.A., Stachlewitz R.F., Gao W., Qian T., Jayadev S., Jenkins G., Hannun Y., Lemasters J.J., Thurman R.G., Brenner D.A. Reperfusion after liver transplantation in rats differentially activates the mitogen-activated protein kinases. Hepatology. 1997;25:1128–1135. doi: 10.1002/hep.510250514.
    1. Nakano A., Cohen M.V., Downey J.M. Ischemic preconditioning: from basic mechanisms to clinical applications. Pharmacol. Ther. 2000;86:263–275. doi: 10.1016/S0163-7258(00)00058-9.
    1. Carini R., Grazia De Cesaris M., Splendore R., Domenicotti C., Nitti M.P., Pronzato M.A., Albano E. Signal pathway responsible for hepatocyte preconditioning by nitric oxide. Free Radic. Biol. Med. 2003;34:1047–1055. doi: 10.1016/S0891-5849(03)00039-X.
    1. Yamaguchi K., Kawahara T., Kumakura S., Hua J., Kugimiya T., Nagaoka I., Inada E. Effect of olprinone, a phosphodiesterase iii inhibitor, on hepatic ischemia-reperfusion injury in rats. Shock. 2010;33:436–441. doi: 10.1097/SHK.0b013e3181be3d7a.
    1. Meng G.-X., Yuan Q., Wei L.-P., Meng H., Wang Y.-J. Protein kinase C-β inhibitor treatment attenuates hepatic ischemia and reperfusion injury in diabetic rats. Exp. Ther. Med. 2016;11:565–570. doi: 10.3892/etm.2015.2927.
    1. Ricciardi R., Schaffer B.K., Kim R.D., Shah S.A., Donohue S.E., Wheeler S.M., Quarfordt S.H., Callery M.P., Meyers W.C., Chari R.S., et al. Protective effects of ischemic preconditioning on the cold-preserved liver are tyrosine kinase dependent. Transplantation. 2001;72:406–412. doi: 10.1097/00007890-200108150-00008.
    1. Hur G.M., Ryu Y.S., Yun H.Y., Jeon B.H., Kim Y.M., Seok J.H., Lee J.H. Hepatic Ischemia/Reperfusion in Rats Induces iNOS Gene Transcription by Activation of NF-κB. Biochem. Biophys. Res. Commun. 1999;261:917–922. doi: 10.1006/bbrc.1999.1143.
    1. Choi A.M.K., Alam J. Heme Oxygenase-1: Function, Regulation, and Implication of a Novel Stress-inducible Protein in Oxidant-induced Lung Injury. Am. J. Respir. Cell Mol. Biol. 1996;15:9–19. doi: 10.1165/ajrcmb.15.1.8679227.
    1. Origassa C.S.T., Câmara N.O.S. Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury. World J. Hepatol. 2013;5:541–549.
    1. Devey L., Ferenbach D., Mohr E., Sangster K., Bellamy C.O., Hughes J., Wigmore S.J. Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol. Ther. 2009;17:65–72. doi: 10.1038/mt.2008.237.
    1. Ha Y.M., Ham S.A., Kim Y.M., Lee Y.S., Kim H.J., Seo H.G., Lee J.H., Park M.K., Chang K.C. β1-Adrenergic receptor-mediated HO-1 induction, via PI3K and p38 MAPK, by isoproterenol in RAW 264.7 cells leads to inhibition of HMGB1 release in LPS-activated RAW 264.7 cells and increases in survival rate of CLP-induced septic mice. Biochem. Pharmacol. 2011;82:769–777. doi: 10.1016/j.bcp.2011.06.041.
    1. Wang J., Hu X., Fu W., Xie J., Zhou X., Jiang H. Isoproterenol-mediated heme oxygenase-1 induction inhibits high mobility group box 1 protein release and protects against rat myocardial ischemia/reperfusion injury in vivo. Mol. Med. Rep. 2014 doi: 10.3892/mmr.2014.2026.
    1. Sun L., Shi T., Qiao H., Jiang X., Jiang H., Krissansen G.W., Sun X. Hepatic Overexpression of Heme Oxygenase-1 Improves Liver Allograft Survival by Expanding T Regulatory Cells. J. Surg. Res. 2011;166:e187–e194. doi: 10.1016/j.jss.2010.11.917.
    1. Burne M.J., Daniels F., El Ghandour A., Mauiyyedi S., Colvin R.B., O’Donnell M.P., Rabb H. Identification of the CD4(+) T cell as a major pathogenic factor in ischemic acute renal failure. J. Clin. Investig. 2001;108:1283–1290. doi: 10.1172/JCI200112080.
    1. Yang Z., Sharma A.K., Linden J., Kron I.L., Laubach V.E. CD4+ T lymphocytes mediate acute pulmonary ischemia-reperfusion injury. J. Thorac. Cardiovasc. Surg. 2009;137:695–702. doi: 10.1016/j.jtcvs.2008.10.044.
    1. Dienz O., Rincon M. The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 2009;130:27–33. doi: 10.1016/j.clim.2008.08.018.
    1. Nish S.A., Schenten D., Wunderlich F.T., Pope S.D., Gao Y., Hoshi N., Yu S., Yan X., Lee H.K., Pasman L., et al. T cell-intrinsic role of IL-6 signaling in primary and memory responses. Elife. 2014;3:e01949. doi: 10.7554/eLife.01949.
    1. Caldwell-Kenkel J.C., Currin R.T., Tanaka Y., Thurman R.G., Lemasters J.J. Kupffer cell activation and endothelial cell damage after storage of rat livers: effects of reperfusion. Hepatology. 1991;13:83–95.
    1. Shiratori Y., Kiriyama H., Fukushi Y., Nagura T., Takada H., Hai K., Kamii K. Modulation of ischemia-reperfusion-induced hepatic injury by Kupffer cells. Dig. Dis. Sci. 1994;39:1265–1272. doi: 10.1007/BF02093792.
    1. Bailey S.M., Reinke L.A. Antioxidants and gadolinium chloride attenuate hepatic parenchymal and endothelial cell injury induced by low flow ischemia and reperfusion in perfused rat livers. Free Radic. Res. 2000;32:497–506. doi: 10.1080/10715760000300501.
    1. Liang J., Yamaguchi Y., Matsumura F., Goto M., Akizuki E., Matsuda T., Okabe K., Ohshiro H., Ishihara K., Yamada S., et al. Calcium-Channel Blocker Attenuates Kupffer Cell Production of Cytokine-Induced Neutrophil Chemoattractant Following Ischemia–Reperfusion in Rat Liver. Dig. Dis. Sci. 2000;45:201–209. doi: 10.1023/A:1005498402659.
    1. Kobayashi T., Hirano K., Yamamoto T., Hasegawa G., Hatakeyama K., Suematsu M., Naito M. The protective role of Kupffer cells in the ischemia-reperfused rat liver. Arch. Histol. Cytol. 2002;65:251–261. doi: 10.1679/aohc.65.251.
    1. Muller W.A. New Mechanisms and Pathways for Monocyte Recruitment. J. Exp. Med. 2001;194:F47–F52. doi: 10.1084/jem.194.9.f47.
    1. Krenkel O., Mossanen J.C., Tacke F. Immune mechanisms in acetaminophen-induced acute liver failure. Hepatobiliary Surg. Nutr. 2014;3:331–343. doi: 10.3978/j.issn.2304-3881.2014.11.01.
    1. Bamboat Z.Z.M., Ocuin L.M., Balachandran V.P., Obaid H., Plitas G., DeMatteo R.R.P., Lotze M., Clavien P., Harvey P., Strasberg S., et al. Conventional DCs reduce liver ischemia/reperfusion injury in mice via IL-10 secretion. J. Clin. Investig. 2010;120:559–569. doi: 10.1172/JCI40008.
    1. Colletti L.M., Remick D.G., Burtch G.D., Kunkel S.L., Strieter R.M., Campbell D.A., Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J. Clin. Investig. 1990;85:1936–1943. doi: 10.1172/JCI114656.
    1. Tsung A., Sahai R., Tanaka H., Nakao A., Fink M.P., Lotze M.T., Yang H., Li J., Tracey K.J., Geller D.A., et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 2005;201:1135–1143. doi: 10.1084/jem.20042614.
    1. Caldwell C.C., Okaya T., Martignoni A., Husted T., Schuster R., Lentsch A.B. Divergent functions of CD4+ T lymphocytes in acute liver inflammation and injury after ischemia-reperfusion. Am. J. Physiol. Gastrointest. Liver Physiol. 2005;289:G969–G976. doi: 10.1152/ajpgi.00223.2005.
    1. Camargo C.A., Madden J.F., Gao W., Selvan R.S., Clavien P. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology. 1997;26:1513–1520. doi: 10.1002/hep.510260619.
    1. Cressman D.E., Greenbaum L.E., DeAngelis R.A., Ciliberto G., Furth E.E., Poli V., Taub R. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science. 1996;274:1379–1383. doi: 10.1126/science.274.5291.1379.
    1. Yamada Y., Kirillova I., Peschon J.J., Fausto N. Initiation of liver growth by tumor necrosis factor: Deficient liver regeneration in mice lacking type I tumor necrosis factor receptor. Proc. Natl. Acad. Sci. USA. 1997;94:1441–1446. doi: 10.1073/pnas.94.4.1441.
    1. Dal-Secco D., Wang J., Zeng Z., Kolaczkowska E., Wong C.H.Y., Petri B., Ransohoff R.M., Charo I.F., Jenne C.N., Kubes P. A dynamic spectrum of monocytes arising from the in situ reprogramming of CCR2+ monocytes at a site of sterile injury. J. Exp. Med. 2015;212:447–456. doi: 10.1084/jem.20141539.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir