The cathepsin-S/protease-activated receptor-(PAR)-2 axis drives chronic allograft vasculopathy and is a molecular target for therapeutic intervention

Transplant Immunology - Tập 77 - Trang 101782 - 2023
Martin Ryll1, Yutian Lei2, Michael N. Thomas3, Mingming Li1, Bernhard Renz1, Ulrich Wirth1, Florian Kühn1, Alexandr Bazhin1, Jens Werner1, Hans-Joachim Anders2, Joachim Andrassy1
1Hospital of LMU Munich, Division of General, Visceral, Vascular and Transplant Surgery, Munich, Bavaria, Germany
2Hospital of LMU Munich, Division of Nephrology, Department of Medicine IV, Munich, Bavaria, Germany
3University Hospital Cologne, Department for General, Visceral, Cancer and Transplant Surgery, Cologne, North Rhine-Westphalia, Germany

Tài liệu tham khảo

Rana, 2015, Survival benefit of solid-organ transplant in the United States, JAMA Surg., 150, 252, 10.1001/jamasurg.2014.2038 Lee, 2018, Cardiac allograft vasculopathy: a review, Catheter. Cardiovasc. Interv., 92, E527, 10.1002/ccd.27893 Rana, 2019, Outcomes in solid-organ transplantation: success and stagnation, Tex. Heart Inst. J., 46, 75, 10.14503/THIJ-18-6749 Pober, 2014, Interacting mechanisms in the pathogenesis of cardiac allograft vasculopathy, Arterioscler. Thromb. Vasc. Biol., 34, 1609, 10.1161/ATVBAHA.114.302818 Kitchens, 2007, Macrophage depletion suppresses cardiac allograft vasculopathy in mice, Am. J. Transplant., 7, 2675, 10.1111/j.1600-6143.2007.01997.x Uehara, 2005, NK cells can trigger allograft vasculopathy: the role of hybrid resistance in solid organ allografts, J. Immunol., 175, 3424, 10.4049/jimmunol.175.5.3424 Weenink, 1997, Antigen presentation by MHC class II molecules, Immunol. Cell Biol., 75, 69, 10.1038/icb.1997.11 Roche, 1991, Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules, Proc. Natl. Acad. Sci. U. S. A., 88, 3150, 10.1073/pnas.88.8.3150 Saegusa, 2002, Cathepsin S inhibitor prevents autoantigen presentation and autoimmunity, J. Clin. Invest., 110, 361, 10.1172/JCI0214682 Baugh, 2011, Therapeutic dosing of an orally active, selective cathepsin S inhibitor suppresses disease in models of autoimmunity, J. Autoimmun., 36, 201, 10.1016/j.jaut.2011.01.003 Riese, 1998, Cathepsin S activity regulates antigen presentation and immunity, J. Clin. Investig., 101, 2351, 10.1172/JCI1158 Tato, 2017, Cathepsin S inhibition combines control of systemic and peripheral pathomechanisms of autoimmune tissue injury, Sci. Rep., 7, 2775, 10.1038/s41598-017-01894-y Rupanagudi, 2015, Cathepsin S inhibition suppresses systemic lupus erythematosus and lupus nephritis because cathepsin S is essential for MHC class II-mediated CD4 T cell and B cell priming, Ann. Rheum. Dis., 74, 452, 10.1136/annrheumdis-2013-203717 Sukhova, 1998, Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells, J. Clin. Investig., 102, 576, 10.1172/JCI181 Sukhova, 2003, Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice, J. Clin. Investig., 111, 897, 10.1172/JCI200314915 Rodgers, 2006, Destabilizing role of cathepsin S in murine atherosclerotic plaques, Arterioscler. Thromb. Vasc. Biol., 26, 851, 10.1161/01.ATV.0000203526.75772.4b Tennant, 2008, PAR-2 mediates increased inflammatory cell adhesion and neointima formation following vascular injury in the mouse, Atherosclerosis, 198, 57, 10.1016/j.atherosclerosis.2007.09.043 Kumar Vr, 2016, Cathepsin S cleavage of protease-activated receptor-2 on endothelial cells promotes microvascular diabetes complications, J. Am. Soc. Nephrol., 27, 1635, 10.1681/ASN.2015020208 Vergnolle, 1999, Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo, J. Immunol. (Baltimore, Md. 1950), 163, 5064, 10.4049/jimmunol.163.9.5064 Ryll, 2019, Murine cervical aortic transplantation model using a modified non-suture cuff technique, J. Vis. Exp., 153 Theron, 2017, Pharmacodynamic monitoring of RO5459072, a small molecule inhibitor of Cathepsin S, Front. Immunol., 8, 806, 10.3389/fimmu.2017.00806 Oberhuber, 2016, Impaired endothelial nitric oxide synthase homodimer formation triggers development of transplant vasculopathy - insights from a murine aortic transplantation model, Sci. Rep., 6, 37917, 10.1038/srep37917 Bankhead, 2017, QuPath: open source software for digital pathology image analysis, Sci. Rep., 7, 16878, 10.1038/s41598-017-17204-5 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Lemström, 2004, Role of angiogenic growth factors in transplant coronary artery disease, Ann. Med., 36, 184, 10.1080/07853890310025243 Christie, 2011, The registry of the international society for heart and lung transplantation: twenty-eighth adult lung and heart-lung transplant report--2011, J. Heart Lung Transplant., 30, 1104, 10.1016/j.healun.2011.08.004 Mitchell, 2007, Vascular remodeling in transplant vasculopathy, Circ. Res., 100, 967, 10.1161/01.RES.0000261982.76892.09 Shi, 2014, Cathepsin S contributes to macrophage migration via degradation of elastic fibre integrity to facilitate vein graft neointimal hyperplasia, Cardiovasc. Res., 101, 454, 10.1093/cvr/cvt273 Cheng, 2006, Localization of cysteine protease, cathepsin S, to the surface of vascular smooth muscle cells by association with integrin alphanubeta3, Am. J. Pathol., 168, 685, 10.2353/ajpath.2006.050295 Cheng, 2004, Increased expression of elastolytic cysteine proteases, cathepsins S and K, in the neointima of balloon-injured rat carotid arteries, Am. J. Pathol., 164, 243, 10.1016/S0002-9440(10)63114-8 Nagano, 1997, Interferon-gamma deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts, J. Clin. Investig., 100, 550, 10.1172/JCI119564 Klaus, 2018, Cathepsin S is associated with degradation of collagen I in abdominal aortic aneurysm, VASA. Zeitschrift fur Gefasskrankheiten, 47, 285, 10.1024/0301-1526/a000701 Qin, 2012, Deficiency of cathepsin S attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice, Cardiovasc. Res., 96, 401, 10.1093/cvr/cvs263 Samokhin, 2010, Pharmacological inhibition of cathepsin S decreases atherosclerotic lesions in Apoe−/− mice, J. Cardiovasc. Pharmacol., 56, 98, 10.1097/FJC.0b013e3181e23e10 Merola, 2017, Recent advances in allograft vasculopathy, Curr. Opin. Organ Transplant., 22, 1, 10.1097/MOT.0000000000000370 Tellides, 2007, Interferon-gamma axis in graft arteriosclerosis, Circ. Res., 100, 622, 10.1161/01.RES.0000258861.72279.29 Yu, 2011, AIP1 prevents graft arteriosclerosis by inhibiting interferon-γ-dependent smooth muscle cell proliferation and intimal expansion, Circ. Res., 109, 418, 10.1161/CIRCRESAHA.111.248245 Roche, 1990, Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding, Nature, 345, 615, 10.1038/345615a0 Shi, 1999, Cathepsin S required for normal MHC class II peptide loading and germinal center development, Immunity, 10, 197, 10.1016/S1074-7613(00)80020-5 Yang, 2005, Cathepsin S is required for murine autoimmune myasthenia gravis pathogenesis, J. Immunol. (Baltimore, Md. 1950), 174, 1729, 10.4049/jimmunol.174.3.1729 Deschamps, 2011, Genetic and pharmacological evaluation of cathepsin s in a mouse model of asthma, Am. J. Respir. Cell Mol. Biol., 45, 81, 10.1165/rcmb.2009-0392OC Lei, 2020, Cathepsin S and protease-activated receptor-2 drive alloimmunity and immune regulation in kidney allograft rejection, Front. Cell Dev. Biol., 8, 398, 10.3389/fcell.2020.00398 Kubo, 2018, Effective suppression of donor specific antibody production by Cathepsin S inhibitors in a mouse transplantation model, Eur. J. Pharmacol., 838, 145, 10.1016/j.ejphar.2018.09.007 Elmariah, 2014, Cathepsin S signals via PAR2 and generates a novel tethered ligand receptor agonist, PLoS One, 9, 10.1371/journal.pone.0099702 Damiano, 1999, Increased expression of protease activated receptor-2 (PAR-2) in balloon-injured rat carotid artery, Thromb. Haemost., 81, 808, 10.1055/s-0037-1614574 Jones, 2018, PAR2 (protease-activated receptor 2) deficiency attenuates atherosclerosis in mice, Arterioscler. Thromb. Vasc. Biol., 38, 1271, 10.1161/ATVBAHA.117.310082 Zuo, 2017, Protease-activated receptor-2 deficiency attenuates atherosclerotic lesion progression and instability in apolipoprotein E-deficient mice, Front. Pharmacol., 8, 647, 10.3389/fphar.2017.00647 Johansson, 2005, Human peripheral blood monocytes express protease receptor-2 and respond to receptor activation by production of IL-6, IL-8, and IL-1{beta}, J. Leukoc. Biol., 78, 967, 10.1189/jlb.0704422 Dekita, 2017, Cathepsin S is involved in Th17 differentiation through the upregulation of IL-6 by activating PAR-2 after systemic exposure to lipopolysaccharide from porphyromonas gingivalis, Front. Pharmacol., 8, 470, 10.3389/fphar.2017.00470 Csernok, 2006, Wegener autoantigen induces maturation of dendritic cells and licenses them for Th1 priming via the protease-activated receptor-2 pathway, Blood, 107, 4440, 10.1182/blood-2005-05-1875 Ramelli, 2010, Protease-activated receptor 2 signalling promotes dendritic cell antigen transport and T-cell activation in vivo, Immunology, 129, 20, 10.1111/j.1365-2567.2009.03144.x Shi, 1996, Immunologic basis of transplant-associated arteriosclerosis, Proc. Natl. Acad. Sci. U. S. A., 93, 4051, 10.1073/pnas.93.9.4051 Forbes, 1994, Evidence that recipient CD8+ T cell depletion does not alter development of chronic vascular rejection in a rat heart allograft model, Transplantation, 57, 1238, 10.1097/00007890-199404270-00017 Allan, 1997, Cardiac allograft vasculopathy is abrogated by anti-CD8 monoclonal antibody therapy, Ann. Thorac. Surg., 64, 1019, 10.1016/S0003-4975(97)00796-0 Schnickel, 2004, CD8 lymphocytes are sufficient for the development of chronic rejection, Transplantation, 78, 1634, 10.1097/01.TP.0000141362.33931.40 Fischbein, 2002, Role of CD8+ lymphocytes in chronic rejection of transplanted hearts, J. Thorac. Cardiovasc. Surg., 123, 803, 10.1067/mtc.2002.120008 Rothmeier, 2012, Protease-activated receptor 2 signaling in inflammation, Semin. Immunopathol., 34, 133, 10.1007/s00281-011-0289-1