Multi‑faceted roles of cathepsins in ischemia reperfusion injury (Review)
- Authors:
- Jaime Huertas
- H. Thomas Lee
-
Affiliations: Department of Anesthesiology, College of Physicians and Surgeons of Columbia University, New York, NY 10032‑3784, USA - Published online on: October 26, 2022 https://doi.org/10.3892/mmr.2022.12885
- Article Number: 368
-
Copyright: © Huertas et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
 |
|
Patel S, Homaei A, El-Seedi HR and Akhtar N: Cathepsins: Proteases that are vital for survival but can also be fatal. Biomed Pharmacother. 105:526–532. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Cocchiaro P, De Pasquale V, Della Morte R, Tafuri S, Avallone L, Pizard A, Moles A and Pavone LM: The multifaceted role of the lysosomal protease cathepsins in kidney disease. Front Cell Dev Biol. 5:1142017. View Article : Google Scholar : PubMed/NCBI | |
|
Brix K, Dunkhorst A, Mayer K and Jordans S: Cysteine cathepsins: Cellular roadmap to different functions. Biochimie. 90:194–207. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Vidak E, Javoršek U, Vizovišek M and Turk B: Cysteine cathepsins and their extracellular roles: Shaping the microenvironment. Cells. 8:2642019. View Article : Google Scholar : PubMed/NCBI | |
|
Xu Y, Wang J, Song X, Wei R, He F, Peng G and Luo B: Protective mechanisms of CA074-me (other than cathepsin-B inhibition) against programmed necrosis induced by global cerebral ischemia/reperfusion injury in rats. Brain Res Bull. 120:97–105. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Stoka V, Turk V and Turk B: Lysosomal cysteine cathepsins: Signaling pathways in apoptosis. Biol Chem. 388:555–560. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Tan GJ, Peng ZK, Lu JP and Tang FQ: Cathepsins mediate tumor metastasis. World J Biol Chem. 4:91–101. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Hook G, Jacobsen JS, Grabstein K, Kindy M and Hook V: Cathepsin B is a new drug target for traumatic brain injury therapeutics: Evidence for E64d as a promising lead drug candidate. Front Neurol. 6:1782015. View Article : Google Scholar : PubMed/NCBI | |
|
Ben-Ari Z, Mor E, Azarov D, Sulkes J, Tor R, Cheporko Y, Hochhauser E and Pappo O: Cathepsin B inactivation attenuates the apoptotic injury induced by ischemia/reperfusion of mouse liver. Apoptosis. 10:1261–1269. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Yadati T, Houben T, Bitorina A and Shiri-Sverdlov R: The Ins and outs of cathepsins: Physiological function and role in disease management. Cells. 9:16792020. View Article : Google Scholar : PubMed/NCBI | |
|
Chevriaux A, Pilot T, Derangère V, Simonin H, Martine P, Chalmin F, Ghiringhelli F and Rébé C: Cathepsin B is required for NLRP3 inflammasome activation in macrophages, through NLRP3 interaction. Front Cell Dev Biol. 8:1672020. View Article : Google Scholar : PubMed/NCBI | |
|
Tang TT, Lv LL, Pan MM, Wen Y, Wang B, Li ZL, Wu M, Wang FM, Crowley SD and Liu BC: Hydroxychloroquine attenuates renal ischemia/reperfusion injury by inhibiting cathepsin mediated NLRP3 inflammasome activation. Cell Death Dis. 9:3512018. View Article : Google Scholar : PubMed/NCBI | |
|
Korkmaz B, Caughey GH, Chapple I, Gauthier F, Hirschfeld J, Jenne DE, Kettritz R, Lalmanach G, Lamort AS, Lauritzen C, et al: Therapeutic targeting of cathepsin C: From pathophysiology to treatment. Pharmacol Ther. 190:202–236. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Rehm SRT, Smirnova NF, Morrone C, Götzfried J, Feuchtinger A, Pedersen J, Korkmaz B, Yildirim AÖ and Jenne DE: Premedication with a cathepsin C inhibitor alleviates early primary graft dysfunction in mouse recipients after lung transplantation. Sci Rep. 9:99252019. View Article : Google Scholar : PubMed/NCBI | |
|
Dennemärker J, Lohmüller T, Müller S, Aguilar SV, Tobin DJ, Peters C and Reinheckel T: Impaired turnover of autophagolysosomes in cathepsin L deficiency. Biol Chem. 391:913–922. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
McComb S, Shutinoski B, Thurston S, Cessford E, Kumar K and Sad S: Cathepsins limit macrophage necroptosis through cleavage of Rip1 kinase. J Immunol. 192:5671–5678. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Figueiredo JL, Aikawa M, Zheng C, Aaron J, Lax L, Libby P, de Lima Filho JL, Gruener S, Fingerle J, Haap W, et al: Selective cathepsin S inhibition attenuates atherosclerosis in apolipoprotein E-deficient mice with chronic renal disease. Am J Pathol. 185:1156–1166. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Nakanishi H: Neuronal and microglial cathepsins in aging and age-related diseases. Ageing Res Rev. 2:367–381. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Kos J, Sekirnik A, Premzl A, Zavasnik Bergant V, Langerholc T, Turk B, Werle B, Golouh R, Repnik U, Jeras M and Turk V: Carboxypeptidases cathepsins X and B display distinct protein profile in human cells and tissues. Exp Cell Res. 306:103–113. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Polcyn R, Capone M, Hossain A, Matzelle D, Banik NL and Haque A: Neuron specific enolase is a potential target for regulating neuronal cell survival and death: Implications in neurodegeneration and regeneration. Neuroimmunol Neuroinflamm. 4:254–257. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Obermajer N, Premzl A, Zavasnik Bergant T, Turk B and Kos J: Carboxypeptidase cathepsin X mediates beta2-integrin-dependent adhesion of differentiated U-937 cells. Exp Cell Res. 312:2515–2527. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ondr JK and Pham CT: Characterization of murine cathepsin W and its role in cell-mediated cytotoxicity. J Biol Chem. 279:27525–27533. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Wex T, Wex H, Hartig R, Wilhelmsen S and Malfertheiner P: Functional involvement of cathepsin W in the cytotoxic activity of NK-92 cells. FEBS Lett. 552:115–119. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Stoeckle C, Gouttefangeas C, Hammer M, Weber E, Melms A and Tolosa E: Cathepsin W expressed exclusively in CD8+ T cells and NK cells, is secreted during target cell killing but is not essential for cytotoxicity in human CTLs. Exp Hematol. 37:266–275. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kakehashi H, Nishioku T, Tsukuba T, Kadowaki T, Nakamura S and Yamamoto K: Differential regulation of the nature and functions of dendritic cells and macrophages by cathepsin E. J Immunol. 179:5728–5737. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Chain BM, Free P, Medd P, Swetman C, Tabor AB and Terrazzini N: The expression and function of cathepsin E in dendritic cells. J Immunol. 174:1791–1800. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Yamamoto K, Kawakubo T, Yasukochi A and Tsukuba T: Emerging roles of cathepsin E in host defense mechanisms. Biochim Biophys Acta. 1824:105–112. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Deussing J, Roth W, Saftig P, Peters C, Ploegh HL and Villadangos JA: Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc Natl Acad Sci USA. 95:4516–4521. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Droga-Mazovec G, Bojic L, Petelin A, Ivanova S, Romih R, Repnik U, Salvesen GS, Stoka V, Turk V and Turk B: Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J Biol Chem. 283:19140–19150. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Conus S, Perozzo R, Reinheckel T, Peters C, Scapozza L, Yousefi S and Simon HU: Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J Exp Med. 205:685–698. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Bidère N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C and Senik A: Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem. 278:31401–31411. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Seyrantepe V, Hinek A, Peng J, Fedjaev M, Ernest S, Kadota Y, Canuel M, Itoh K, Morales CR, Lavoie J, et al: Enzymatic activity of lysosomal carboxypeptidase (cathepsin) A is required for proper elastic fiber formation and inactivation of endothelin-1. Circulation. 117:1973–1981. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Jackman HL, Massad MG, Sekosan M, Tan F, Brovkovych V, Marcic BM and Erdös EG: Angiotensin 1–9 and 1–7 release in human heart: Role of cathepsin A. Hypertension. 39:976–981. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Burster T, Macmillan H, Hou T, Boehm BO and Mellins ED: Cathepsin G: Roles in antigen presentation and beyond. Mol Immunol. 47:658–665. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Meyer-Hoffert U: Neutrophil-derived serine proteases modulate innate immune responses. Front Biosci (Landmark Ed). 14:3409–3418. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Pintucci G, Iacoviello L, Castelli MP, Amore C, Evangelista V, Cerletti C and Donati MB: Cathepsin G-induced release of PAI-1 in the culture medium of endothelial cells: A new thrombogenic role for polymorphonuclear leukocytes? J Lab Clin Med. 122:69–79. 1993.PubMed/NCBI | |
|
Richter R, Bistrian R, Escher S, Forssmann WG, Vakili J, Henschler R, Spodsberg N, Frimpong-Boateng A and Forssmann U: Quantum proteolytic activation of chemokine CCL15 by neutrophil granulocytes modulates mononuclear cell adhesiveness. J Immunol. 175:1599–1608. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Miao Z, Premack BA, Wei Z, Wang Y, Gerard C, Showell H, Howard M, Schall TJ and Berahovich R: Proinflammatory proteases liberate a discrete high-affinity functional FPRL1 (CCR12) ligand from CCL23. J Immunol. 178:7395–7404. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Brignone C, Munoz O, Batoz M, Rouquette-Jazdanian A and Cousin JL: Proteases produced by activated neutrophils are able to release soluble CD23 fragments endowed with proinflammatory effects. FASEB J. 15:2027–2029. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Yang Z, Weian C, Susu H and Hanmin W: Protective effects of mangiferin on cerebral ischemia-reperfusion injury and its mechanisms. Eur J Pharmacol. 771:145–151. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Seyfried DM, Veyna R, Han Y, Li K, Tang N, Betts RL, Weinsheimer S, Chopp M and Anagli J: A selective cysteine protease inhibitor is non-toxic and cerebroprotective in rats undergoing transient middle cerebral artery ischemia. Brain Res. 901:94–101. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Benchoua A, Braudeau J, Reis A, Couriaud C and Onténiente B: Activation of proinflammatory caspases by cathepsin B in focal cerebral ischemia. J Cereb Blood Flow Metab. 24:1272–1279. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH and Gores GJ: Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest. 106:1127–1137. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Tsubokawa T, Solaroglu I, Yatsushige H, Cahill J, Yata K and Zhang JH: Cathepsin and calpain inhibitor E64d attenuates matrix metalloproteinase-9 activity after focal cerebral ischemia in rats. Stroke. 37:1888–1894. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Qin XF, Lu XJ, Ge JB, Xu HZ, Qin HD and Xu F: Ginkgolide B prevents cathepsin-mediated cell death following cerebral ischemia/reperfusion injury. Neuroreport. 25:267–273. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wei R, Wang J, Xu Y, Yin B, He F, Du Y, Peng G and Luo B: Probenecid protects against cerebral ischemia/reperfusion injury by inhibiting lysosomal and inflammatory damage in rats. Neuroscience. 301:168–177. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu YM, Gao X, Ni Y, Li W, Kent TA, Qiao SG, Wang C, Xu XX and Zhang HL: Sevoflurane postconditioning attenuates reactive astrogliosis and glial scar formation after ischemia-reperfusion brain injury. Neuroscience. 356:125–141. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Cui DR, Wang L, Jiang W, Qi AH, Zhou QH and Zhang XL: Propofol prevents cerebral ischemia-triggered autophagy activation and cell death in the rat hippocampus through the NF-κB/p53 signaling pathway. Neuroscience. 246:117–132. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Ahsan A, Zheng Y, Ma S, Liu M, Cao M, Li Y, Zheng W, Zhou X, Xin M, Hu WW, et al: Tomatidine protects against ischemic neuronal injury by improving lysosomal function. Eur J Pharmacol. 882:1732802020. View Article : Google Scholar : PubMed/NCBI | |
|
Kilinc M, Gürsoy-Ozdemir Y, Gürer G, Erdener SE, Erdemli E, Can A and Dalkara T: Lysosomal rupture, necroapoptotic interactions and potential crosstalk between cysteine proteases in neurons shortly after focal ischemia. Neurobiol Dis. 40:293–302. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Wang F, Gómez-Sintes R and Boya P: Lysosomal membrane permeabilization and cell death. Traffic. 19:918–931. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kirkegaard T, Roth AG, Petersen NH, Mahalka AK, Olsen OD, Moilanen I, Zylicz A, Knudsen J, Sandhoff K, Arenz C, et al: Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature. 463:549–553. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Yamashima T: Hsp70.1 and related lysosomal factors for necrotic neuronal death. J Neurochem. 120:477–494. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Heusch G and Gersh BJ: The pathophysiology of acute myocardial infarction and strategies of protection beyond reperfusion: A continual challenge. Eur Heart J. 38:774–784. 2017.PubMed/NCBI | |
|
Vander Heide RS and Steenbergen C: Cardioprotection and myocardial reperfusion: Pitfalls to clinical application. Circ Res. 113:464–477. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Frangogiannis NG: Regulation of the inflammatory response in cardiac repair. Circ Res. 110:159–173. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kain V, Prabhu SD and Halade GV: Inflammation revisited: Inflammation versus resolution of inflammation following myocardial infarction. Basic Res Cardiol. 109:4442014. View Article : Google Scholar : PubMed/NCBI | |
|
Meyer-Hoffert U and Wiedow O: Neutrophil serine proteases: Mediators of innate immune responses. Curr Opin Hematol. 18:19–24. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sabri A, Alcott SG, Elouardighi H, Pak E, Derian C, Andrade-Gordon P, Kinnally K and Steinberg SF: Neutrophil cathepsin G promotes detachment-induced cardiomyocyte apoptosis via a protease-activated receptor-independent mechanism. J Biol Chem. 278:23944–23954. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Iacoviello L, Kolpakov V, Salvatore L, Amore C, Pintucci G, de Gaetano G and Donati MB: Human endothelial cell damage by neutrophil-derived cathepsin G. Role of cytoskeleton rearrangement and matrix-bound plasminogen activator inhibitor-1. Arterioscler Thromb Vasc Biol. 15:2037–2046. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Hooshdaran B, Kolpakov MA, Guo X, Miller SA, Wang T, Tilley DG, Rafiq K and Sabri A: Dual inhibition of cathepsin G and chymase reduces myocyte death and improves cardiac remodeling after myocardial ischemia reperfusion injury. Basic Res Cardiol. 112:622017. View Article : Google Scholar : PubMed/NCBI | |
|
Taleb S, Cancello R, Clément K and Lacasa D: Cathepsin S promotes human preadipocyte differentiation: Possible involvement of fibronectin degradation. Endocrinology. 147:4950–4959. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Chen H, Wang J, Xiang MX, Lin Y, He A, Jin CN, Guan J, Sukhova GK, Libby P, Wang JA and Shi GP: Cathepsin S-mediated fibroblast trans-differentiation contributes to left ventricular remodelling after myocardial infarction. Cardiovasc Res. 100:84–94. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Peng K, Liu H, Yan B, Meng XW, Song SY, Ji FH and Xia Z: Inhibition of cathepsin S attenuates myocardial ischemia/reperfusion injury by suppressing inflammation and apoptosis. J Cell Physiol. 236:1309–1320. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Linz D, Hohl M, Dhein S, Ruf S, Reil JC, Kabiri M, Wohlfart P, Verheule S, Böhm M, Sadowski T and Schotten U: Cathepsin A mediates susceptibility to atrial tachyarrhythmia and impairment of atrial emptying function in Zucker diabetic fatty rats. Cardiovasc Res. 110:371–380. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Hohl M, Erb K, Lang L, Ruf S, Hübschle T, Dhein S, Linz W, Elliott AD, Sanders P, Zamyatkin O, et al: Cathepsin A mediates ventricular remote remodeling and atrial cardiomyopathy in rats with ventricular ischemia/reperfusion. JACC Basic Transl Sci. 4:332–344. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Turski WA and Zasłonka J: Activity of cathepsin D and L in the heart muscle of coronary patients during coronary-aortal bypass graft operation. Med Sci Monit. 6:853–860. 2000.PubMed/NCBI | |
|
Turski WA and Zasłonka J: Effects of Bretschneider cardioplegic fluid on the lysosomal cathepsins D and L of myocardium of coronary patients during coronary-aortal bypass graft operation. Med Sci Monit. 6:861–866. 2000.PubMed/NCBI | |
|
Zhai Y, Petrowsky H, Hong JC, Busuttil RW and Kupiec-Weglinski JW: Ischaemia-reperfusion injury in liver transplantation-from bench to bedside. Nat Rev Gastroenterol Hepatol. 10:79–89. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Baskin-Bey ES, Canbay A, Bronk SF, Werneburg N, Guicciardi ME, Nyberg SL and Gores GJ: Cathepsin B inactivation attenuates hepatocyte apoptosis and liver damage in steatotic livers after cold ischemia-warm reperfusion injury. Am J Physiol Gastrointest Liver Physiol. 288:G396–G402. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Guicciardi ME, Miyoshi H, Bronk SF and Gores GJ: Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: Implications for therapeutic applications. Am J Pathol. 159:2045–2054. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou H, Zhou S, Shi Y, Wang Q, Wei S, Wang P, Cheng F, Auwerx J, Schoonjans K and Lu L: TGR5/Cathepsin E signaling regulates macrophage innate immune activation in liver ischemia and reperfusion injury. Am J Transplant. 21:1453–1464. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Mehta RL, Kellum JA, Shah SV, Molitoris BA, Ronco C, Warnock DG and Levin A; Acute Kidney Injury Network, : Acute Kidney Injury Network: Report of an initiative to improve outcomes in acute kidney injury. Crit Care. 11:R312007. View Article : Google Scholar : PubMed/NCBI | |
|
Eltzschig HK, Bonney SK and Eckle T: Attenuating myocardial ischemia by targeting A2B adenosine receptors. Trends Mol Med. 19:345–354. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Yap SC and Lee HT: Adenosine and protection from acute kidney injury. Curr Opin Nephrol Hypertens. 21:24–32. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Suzuki C, Tanida I, Ohmuraya M, Oliva Trejo JA, Kakuta S, Sunabori T and Uchiyama Y: Lack of Cathepsin D in the renal proximal tubular cells resulted in increased sensitivity against renal ischemia/reperfusion injury. Int J Mol Sci. 20:17112019. View Article : Google Scholar : PubMed/NCBI | |
|
Cocchiaro P, Fox C, Tregidgo NW, Howarth R, Wood KM, Situmorang GR, Pavone LM, Sheerin NS and Moles A: Lysosomal protease cathepsin D; a new driver of apoptosis during acute kidney injury. Sci Rep. 6:271122016. View Article : Google Scholar : PubMed/NCBI | |
|
Fox C, Cocchiaro P, Oakley F, Howarth R, Callaghan K, Leslie J, Luli S, Wood KM, Genovese F, Sheerin NS and Moles A: Inhibition of lysosomal protease cathepsin D reduces renal fibrosis in murine chronic kidney disease. Sci Rep. 6:201012016. View Article : Google Scholar : PubMed/NCBI | |
|
Shimoda N, Fukazawa N, Nonomura K and Fairchild RL: Cathepsin G is required for sustained inflammation and tissue injury after reperfusion of ischemic kidneys. Am J Pathol. 170:930–940. 2007. View Article : Google Scholar : PubMed/NCBI |
