The 20S proteasome core, active within apoptotic exosome-like vesicles, induces autoantibody production and accelerates rejection

Science Translational Medicine

Volumn 7, Issue 318, 2015, Pages

  Dieudé, Mélanie ^a,b   Bell, Christina ^b,c,g   Turgeon, Julie ^a,b   Beillevaire, Deborah ^a,b   Pomerleau, Luc ^a,b   Yang, Bing ^a,b   Hamelin, Katia ^a,b   Qi, Shijie ^a,b   Pallet, Nicolas ^a,h   Béland, Chanel ^a   Dhahri, Wahiba ^a   Cailhier, Jean François ^a,b   Rousseau, Matthieu ^b,d   Duchez, Anne Claire ^b,d   Lévesque, Tania ^b,d   Lau, Arthur ^b,e   Rondeau, Christiane ^f   Gingras, Diane ^f   Muruve, Danie ^b,e   Rivard, Alain ^a   Cardinal, Héloise ^a,b   Perreault, Claude ^b,c   Desjardins, Michel ^f   Boilard, Éric ^b,d   Thibault, Pierre ^b,c   Hébert, Marie Josée ^a,b   more..

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b Canadian National Transplant Research Program   (Canada)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d LAVAL UNIVERSITY   (Canada)

^e UNIVERSITY OF CALGARY   (Canada)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g HARVARD MEDICAL SCHOOL   (United States)

^h INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

20S PROTEASOME; AUTOANTIBODY; CASPASE 3; CELL PROTEIN; PERLECAN ANTIBODY; PROTEASOME; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; PEPTIDE FRAGMENT; PERLECAN; PROTEOHEPARAN SULFATE;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; AORTA GRAFT; APOPTOSIS; ARTICLE; BIOCHEMICAL ANALYSIS; BLOOD VESSEL INJURY; CELL BODY; CELL VACUOLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; EXOSOME; GRAFT REJECTION; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INFLAMMATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN SECRETION; PROTEOMICS; RAT; VALIDATION PROCESS; ACUTE KIDNEY FAILURE; ALLOGRAFT; ANIMAL; AORTA; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; ENZYMOLOGY; IMMUNOLOGY; ISCHEMIA; KIDNEY PROXIMAL TUBULE; MEMBRANE MICROPARTICLE; METABOLISM; PATHOLOGY; PROCEDURES; SMOOTH MUSCLE CELL; TIME FACTOR; TRANSPLANTATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR SMOOTH MUSCLE;

ACUTE KIDNEY INJURY; ALLOGRAFTS; ANIMALS; AORTA; APOPTOSIS; AUTOANTIBODIES; BIOMARKERS; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EXOSOMES; GRAFT REJECTION; HEPARAN SULFATE PROTEOGLYCANS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNITY, HUMORAL; ISCHEMIA; KIDNEY TUBULES, PROXIMAL; MICE, INBRED BALB C; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOMICS; RATS; TIME FACTORS;

EID: 84954285630     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac9816     Document Type: Article

References (78)

1. H. de Kort, M. Willicombe, P. Brookes, K. M. Dominy, E. Santos-Nunez, J. W. Galliford, K. Chan, D. Taube, A. G. McLean, H. T. Cook, C. Roufosse, Microcirculation inflammation associates with outcome in renal transplant patients with de novo donor-specific antibodies. Am. J. Transplant. 13, 485-492 (2013).
2. L. D. Cornell, R. N. Smith, R. B. Colvin, Kidney transplantation: Mechanisms of rejection and acceptance. Annu. Rev. Pathol. 3, 189-220 (2008).
3. B. Sis, G. Einecke, J. Chang, L. G. Hidalgo, M. Mengel, B. Kaplan, P. F. Halloran, Cluster analysis of lesions in nonselected kidney transplant biopsies: Microcirculation changes, tubulointerstitial inflammation and scarring. Am. J. Transplant. 10, 421-430 (2010).
4. B. Sis, G. S. Jhangri, S. Bunnag, K. Allanach, B. Kaplan, P. F. Halloran, Endothelial gene expression in kidney transplants with alloantibody indicates antibody-mediated damage despite lack of C4d staining. Am. J. Transplant. 9, 2312-2323 (2009).
5. G. Einecke, B. Sis, J. Reeve, M. Mengel, P. M. Campbell, L. G. Hidalgo, B. Kaplan, P. F. Halloran, Antibody-mediated microcirculation injury is the major cause of late kidney transplant failure. Am. J. Transplant. 9, 2520-2531 (2009).
6. A. N. Babu, T. Murakawa, J. M. Thurman, E. J. Miller, P. M. Henson, M. R. Zamora, N. F. Voelkel, M. R. Nicolls, Microvascular destruction identifies murine allografts that cannot be rescued from airway fibrosis. J. Clin. Invest. 117, 3774-3785 (2007).
7. Y. Ishii, T. Sawada, K. Kubota, S. Fuchinoue, S. Teraoka, A. Shimizu, Injury and progressive loss of peritubular capillaries in the development of chronic allograft nephropathy. Kidney Int. 67, 321-332 (2005).
8. H. Cardinal, M. Dieudé, N. Brassard, S. Qi, N. Patey, M. Soulez, D. Beillevaire, F. Echeverry, C. Daniel, Y. Durocher, F. Madore, M. J. Hébert, Antiperlecan antibodies are novel accelerators of immunemediated vascular injury. Am. J. Transplant. 13, 861-874 (2013).
9. H. Regele, Non-HLA antibodies in kidney allograft rejection: Convincing concept in need of further evidence. Kidney Int. 79, 583-586 (2011).
10. D. Saini, J. Weber, S. Ramachandran, D. Phelan, V. Tiriveedhi, M. Liu, N. Steward, A. Aloush, R. Hachem, E. Trulock, B. Meyers, G. A. Patterson, T. Mohanakumar, Alloimmunity-induced autoimmunity as a potential mechanism in the pathogenesis of chronic rejection of human lung allografts. J. Heart Lung Transplant. 30, 624-631 (2011).
11. V. Carter, B. K. Shenton, B. Jaques, D. Turner, D. Talbot, A. Gupta, C. E. Chapman, C. J. Matthews, G. Cavanagh, Vimentin antibodies: A non-HLA antibody as a potential risk factor in renal transplantation. Transplant. Proc. 37, 654-657 (2005).
12. S. Jurcevic, M. E. Ainsworth, A. Pomerance, J. D. Smith, D. R. Robinson, M. J. Dunn, M. H. Yacoub, M. L. Rose, Antivimentin antibodies are an independent predictor of transplant-associated coronary artery disease after cardiac transplantation. Transplantation 71, 886-892 (2001).
13. B. Mahesh, H.-S. Leong, A. McCormack, P. Sarathchandra, A. Holder, M. L. Rose, Autoantibodies to vimentin cause accelerated rejection of cardiac allografts. Am. J. Pathol. 170, 1415-1427 (2007).
14. B. Mahesh, H.-S. Leong, K. S. Nair, A. McCormack, P. Sarathchandra, M. L. Rose, Autoimmunity to vimentin potentiates graft vasculopathy in murine cardiac allografts. Transplantation 90, 4-13 (2010).
15. D. Dragun, Humoral responses directed against non-human leukocyte antigens in solidorgan transplantation. Transplantation 86, 1019-1025 (2008).
16. D. Dragun, B. Hegner, Non-HLA antibodies post-transplantation: Clinical relevance and treatment in solid organ transplantation. Contrib. Nephrol. 162, 129-139 (2009).
17. D. Dragun, D. N. Müller, J. H. Bräsen, L. Fritsche, M. Nieminen-Kelhä, R. Dechend, U. Kintscher, B. Rudolph, J. Hoebeke, D. Eckert, I. Mazak, R. Plehm, C. Schönemann, T. Unger, K. Budde, H.-H. Neumayer, F. C. Luft, G. Wallukat, Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N. Engl. J. Med. 352, 558-569 (2005).
18. L. Li, P. Wadia, R. Chen, N. Kambham, M. Naesens, T. K. Sigdel, D. B. Miklos, M. M. Sarwal, A. J. Butte, Identifying compartment-specific non-HLA targets after renal transplantation by integrating transcriptome and "antibodyome" measures. Proc. Natl. Acad. Sci. U.S.A. 106, 4148-4153 (2009).
19. T. K. Sigdel, L. Li, T. Q. Tran, P. Khatri, M. Naesens, P. Sansanwal, H. Dai, S.-. Hsieh, M. M. Sarwal, Non-HLA antibodies to immunogenic epitopes predict the evolution of chronic renal allograft injury. J. Am. Soc. Nephrol. 23, 750-763 (2012).
20. S. Kalache, R. Dinavahi, S. Pinney, A. Mehrotra, M. W. Cunningham, P. S. Heeger, Anticardiac myosin immunity and chronic allograft vasculopathy in heart transplant recipients. J. Immunol. 187, 1023-1030 (2011).
21. S. A. Joosten, Y. W. J. Sijpkens, V. Van Ham, L. A. Trouw, J. Van Der Vlag, B. Van Den Heuvel, C. Van Kooten, L. C. Paul, Antibody response against the glomerular basement membrane protein agrin in patients with transplant glomerulopathy. Am. J. Transplant. 5, 383-393 (2005).
22. M. L. Rose, Role of anti-vimentin antibodies in allograft rejection. Hum. Immunol. 74, 1459-1462 (2013).
23. A. T. Linke, B. Marchant, P. Marsh, G. Frampton, J. Murphy, M. L. Rose, Screening of a HUVEC cDNA library with transplant-associated coronary artery disease sera identifies RPL7 as a candidate autoantigen associated with this disease. Clin. Exp. Immunol. 126, 173-179 (2001).
24. F. Porcheray, J. DeVito, B. Y. Yeap, L. Xue, I. Dargon, R. Paine, T. C. Girouard, S. L. Saidman, R. B. Colvin, W. Wong, E. Zorn, Chronic humoral rejection of human kidney allografts associates with broad autoantibody responses. Transplantation 89, 1239-1246 (2010).
25. R. S. Warraich, A. Pomerance, A. Stanley, N. R. Banner, M. J. Dunn, M. H. Yacoub, Cardiac myosin autoantibodies and acute rejection after heart transplantation in patients with dilated cardiomyopathy. Transplantation 69, 1609-1617 (2000).
26. N. Angaswamy, C. Klein, V. Tiriveedhi, J. Gaut, S. Anwar, A. Rossi, D. Phelan, J. R. Wellen, S. Shenoy, W. C. Chapman, T. Mohanakumar, Immune responses to collagen-IV and fibronectin in renal transplant recipients with transplant glomerulopathy. Am. J. Transplant. 14, 685-693 (2014).
27. A. Bharat, D. Saini, N. Steward, R. Hachem, E. P. Trulock, G. A. Patterson, B. F. Meyers, T. Mohanakumar, Antibodies to self-antigens predispose to primary lung allograft dysfunction and chronic rejection. Ann. Thorac. Surg. 90, 1094-1101 (2010).
28. V. Subramanian, S. Ramachandran, B. Banan, A. Bharat, X. Wang, N. Benshoff, D. Kreisel, A. E. Gelman, T. Mohanakumar, Immune response to tissue-restricted self-antigens induces airway inflammation and fibrosis following murine lung transplantation. Am. J. Transplant. 14, 2359-2366 (2014).
29. G. Hönger, H. Cardinal, M. Dieudé, A. Buser, I. Hösli, D. Dragun, M.-J. Hébert, S. Schaub, Human pregnancy and generation of anti-angiotensin receptor and anti-perlecan antibodies. Transpl. Int. 27, 467-474 (2014).
30. B. Gao, C. Moore, F. Porcheray, C. Rong, C. Abidoglu, J. DeVito, R. Paine, T. C. Girouard, S. L. Saidman, D. Schoenfeld, B. Levin, W. Wong, N. Elias, C. Schuetz, I. Rosales, Y. Fu, E. Zorn, Pretransplant IgG reactivity to apoptotic cells correlates with late kidney allograft loss. Am. J. Transplant. 14, 1581-1591 (2014).
31. F. Porcheray, J. W. Fraser, B. Gao, A. McColl, J. DeVito, I. Dargon, Y. Helou, W. Wong, T. C. Girouard, S. L. Saidman, R. B. Colvin, A. Palmisano, U. Maggiore, A. Vaglio, R. N. Smith, E. Zorn, Polyreactive antibodies developing amidst humoral rejection of human kidney grafts bind apoptotic cells and activate complement. Am. J. Transplant. 13, 2590-2600 (2013).
32. J.-F. Cailhier, I. Sirois, P. Laplante, S. Lepage, M.-A. Raymond, N. Brassard, A. Prat, R. V. Iozzo, A. V. Pshezhetsky, M.-J. Hébert, Caspase-3 activation triggers extracellular cathepsin L release and endorepellin proteolysis. J. Biol. Chem. 283, 27220-27229 (2008).
33. P. Laplante, M.-A. Raymond, A. Labelle, J.-I. Abe, R. V. Iozzo, M.-J. Hébert, Perlecan proteolysis induces an a2b1 integrin- and Src family kinase-dependent anti-apoptotic pathway in fibroblasts in the absence of focal adhesion kinase activation. J. Biol. Chem. 281, 30383-30392 (2006).
34. I. K. H. Poon, C. D. Lucas, A. G. Rossi, K. S. Ravichandran, Apoptotic cell clearance: Basic biology and therapeutic potential. Nat. Rev. Immunol. 14, 166-180 (2014).
35. D. R. Getts, D. P. McCarthy, S. D. Miller, Exploiting apoptosis for therapeutic tolerance induction. J. Immunol. 191, 5341-5346 (2013).
36. K. S. Ravichandran, U. Lorenz, Engulfment of apoptotic cells: Signals for a good meal. Nat. Rev. Immunol. 7, 964-974 (2007).
37. L. A. Casciola-Rosen, G. Anhalt, A. Rosen, Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179, 1317-1330 (1994).
38. P. D. Robbins, A. E. Morelli, Regulation of immune responses by extracellular vesicles. Nat. Rev. Immunol. 14, 195-208 (2014).
39. I. Sirois, J. Groleau, N. Pallet, N. Brassard, K. Hamelin, I. Londono, A. V. Pshezhetsky, M. Bendayan, M.-J. Hébert, Caspase activation regulates the extracellular export of autophagic vacuoles. Autophagy 8, 927-937 (2012).
40. I. Sirois, M.-A. Raymond, N. Brassard, J.-F. Cailhier, M. Fedjaev, K. Hamelin, I. Londono, M. Bendayan, A. V. Pshezhetsky, M.-J. Hébert, Caspase-3-dependent export of TCTP: A novel pathway for antiapoptotic intercellular communication. Cell Death Differ. 18, 549-562 (2011).
41. E. I. Buzas, B. György, G. Nagy, A. Falus, S. Gay, Emerging role of extracellular vesicles in inflammatory diseases. Nat. Rev. Rheumatol. 10, 356-364 (2014).
42. N. Pallet, I. Sirois, C. Bell, L.-A. Hanafi, K. Hamelin, M. Dieudé, C. Rondeau, P. Thibault, M. Desjardins, M.-J. Hebert, A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 13, 1108-1120 (2013).
43. N. Cloutier, S. Tan, L. H. Boudreau, C. Cramb, R. Subbaiah, L. Lahey, A. Albert, R. Shnayder, R. Gobezie, P. A. Nigrovic, R. W. Farndale, W. H. Robinson, A. Brisson, D. M. Lee, E. Boilard, The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: The microparticle-associated immune complexes. EMBO Mol. Med. 5, 235-249 (2013).
44. L. H. Boudreau, A.-C. Duchez, N. Cloutier, D. Soulet, N. Martin, J. Bollinger, A. Paré, M. Rousseau, G. S. Naika, T. Lévesque, C. Laflamme, G. Marcoux, G. Lambeau, R. W. Farndale, M. Pouliot, H. Hamzeh-Cognasse, F. Cognasse, O. Garraud, P. A. Nigrovic, H. Guderley, S. Lacroix, L. Thibault, J. W. Semple, M. H. Gelb, E. Boilard, Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation. Blood 124, 2173-2183 (2014).
45. E. O'Riordan, T. N. Orlova, N. Mendelev, D. Patschan, R. Kemp, P. N. Chander, R. Hu, G. Hao, S. S. Gross, R. V. Iozzo, V. Delaney, M. S. Goligorsky, Urinary proteomic analysis of chronic allograft nephropathy. Proteomics Clin. Appl. 2, 1025-1035 (2008).
46. M. Soulez, E.-A. Pilon, M. Dieudé, H. Cardinal, N. Brassard, S. Qi, S.-J. Wu, Y. Durocher, F. Madore, C. Perreault, M.-J. Hébert, The perlecan fragment LG3 is a novel regulator of obliterative remodeling associated with allograft vascular rejection. Circ. Res. 110, 94-104 (2012).
47. E. A. Pilon, M. Dieudé, S. Qi, K. Hamelin, L. Pomerleau, D. Beillevaire, Y. Durocher, M. Zutter, D. Coutu, C. Perreault, M. J. Hébert, The perlecan fragment LG3 regulates homing of mesenchymal stem cells and neointima formation during vascular rejection. Am. J. Transplant. 15, 1205-1218 (2015).
48. D. P. Basile, The endothelial cell in ischemic acute kidney injury: Implications for acute and chronic function. Kidney Int. 72, 151-156 (2007).
49. D. P. Basile, J. L. Friedrich, J. Spahic, N. Knipe, H. Mang, E. C. Leonard, S. Changizi-Ashtiyani, R. L. Bacallao, B. A. Molitoris, T. A. Sutton, Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am. J. Physiol. Renal Physiol. 300, F721-F733 (2011).
50. D. P. Basile, M. C. Yoder, Renal endothelial dysfunction in acute kidney ischemia reperfusion injury. Cardiovasc. Hematol. Disord. Drug Targets 14, 3-14 (2014).
51. A. A. Sharfuddin, B. A. Molitoris, Pathophysiology of ischemic acute kidney injury. Nat. Rev. Nephrol. 7, 189-200 (2011).
52. B. A. Molitoris, Therapeutic translation in acute kidney injury: The epithelial/endothelial axis. J. Clin. Invest. 124, 2355-2363 (2014).
53. B. György, T. G. Szabó, M. Pásztói, Z. Pál, P. Misják, B. Aradi, V. László, É. Pállinger, E. Pap, Á. Kittel, G. Nagy, A. Falus, E. I. Buzás, Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell. Mol. Life Sci. 68, 2667-2688 (2011).
54. J. Lötvall, A. F. Hill, F. Hochberg, E. I. Buzás, D. Di Vizio, C. Gardiner, Y. S. Gho, I. V. Kurochkin, S. Mathivanan, P. Quesenberry, S. Sahoo, H. Tahara, M. H. Wauben, K. W. Witwer, C. Théry, Minimal experimental requirements for definition of extracellular vesicles and their functions: A position statement from the International Society for Extracellular Vesicles. J. Extracell Vesicles 3, 26913 (2014).
55. M. Majetschak, M. Perez, L. T. Sorell, J. Lam, M. E. Maldonado, R. W. Hoffman, Circulating 20S proteasome levels in patients with mixed connective tissue disease and systemic lupus erythematosus. Clin. Vaccine Immunol. 15, 1489-1493 (2008).
56. L. Henry, T. Lavabre-Bertrand, T. Douche, S. Uttenweiler-Joseph, P. Fabbro-Peray, B. Monsarrat, J. Martinez, L. Meunier, P.-E. Stoebner, Diagnostic value and prognostic significance of plasmatic proteasome level in patients with melanoma. Exp. Dermatol. 19, 1054-1059 (2010).
57. C. Jakob, K. Egerer, P. Liebisch, S. Türkmen, I. Zavrski, U. Kuckelkorn, U. Heider, M. Kaiser, C. Fleissner, J. Sterz, L. Kleeberg, E. Feist, G.-R. Burmester, P.-M. Kloetzel, O. Sezer, Circulating proteasome levels are an independent prognostic factor for survival in multiple myeloma. Blood 109, 2100-2105 (2007).
58. L. Henry, T. Lavabre-Bertrand, L. Vercambre, J. Ramos, S. Carillo, I. Guiraud, P. Pouderoux, M. Bismuth, J.-C. Valats, C. Demattei, Y. Duny, I. Chaze, N. Funakoshi, J. P. Bureau, J.-P. Daurès, P. Blanc, Plasma proteasome level is a reliable early marker of malignant transformation of liver cirrhosis. Gut 58, 833-838 (2009).
59. M. Wada, M. Kosaka, S. Saito, T. Sano, K. Tanaka, A. Ichihara, Serum concentration and localization in tumor cells of proteasomes in patients with hematologic malignancy and their pathophysiologic significance. J. Lab. Clin. Med. 121, 215-223 (1993).
60. M. Heubner, P. Wimberger, B. Dahlmann, S. Kasimir-Bauer, R. Kimmig, J. Peters, J. Wohlschlaeger, S. U. Sixt, The prognostic impact of circulating proteasome concentrations in patients with epithelial ovarian cancer. Gynecol. Oncol. 120, 233-238 (2011).
61. S. U. Sixt, B. Dahlmann, Extracellular, circulating proteasomes and ubiquitin-incidence and relevance. Biochim. Biophys. Acta 1782, 817-823 (2008).
62. I. Bochmann, F. Ebstein, A. Lehmann, J. Wohlschlaeger, S. U. Sixt, P.-M. Kloetzel, B. Dahlmann, T lymphocytes export proteasomes by way of microparticles: A possible mechanism for generation of extracellular proteasomes. J. Cell. Mol. Med. 18, 59-68 (2014).
63. R. C. Lai, S. S. Tan, B. J. Teh, S. K. Sze, F. Arslan, D. P. de Kleijn, A. Choo, S. K. Lim, Proteolytic potential of the MSC exosome proteome: Implications for an exosome-mediated delivery of therapeutic proteasome. Int. J. Proteomics 2012, 971907 (2012).
64. R. C. Walsh, R. R. Alloway, A. L. Girnita, E. S. Woodle, Proteasome inhibitor-based therapy for antibody-mediated rejection. Kidney Int. 81, 1067-1074 (2012).
65. A. Mulder, S. Heidt, M. Vergunst, D. L. Roelen, F. H. J. Claas, Proteasome inhibition profoundly affects activated human B cells. Transplantation 95, 1331-1337 (2013).
66. L. Schaefer, Complexity of danger: The diverse nature of damage-associated molecular patterns. J. Biol. Chem. 289, 35237-35245 (2014).
67. S. A. Joosten, M. G. A. van Dixhoorn, M. C. Borrias, H. Benediktsson, P. A. van Veelen, C. van Kooten, L. C. Paul, Antibody response against perlecan and collagen types IV and VI in chronic renal allograft rejection in the rat. Am. J. Pathol. 160, 1301-1310 (2002).
68. S. A. Joosten, C. van Kooten, Non-HLA humoral immunity and chronic kidney-graft loss. Lancet 365, 1522-1523 (2005).
69. A. Vilaysane, J. Chun, M. E. Seamone, W. Wang, R. Chin, S. Hirota, Y. Li, S. A. Clark, J. Tschopp, K. Trpkov, B. R. Hemmelgarn, P. L. Beck, D. A. Muruve, The NLRP3 inflammasome promotes renal inflammation and contributes to CKD. J. Am. Soc. Nephrol. 21, 1732-1744 (2010).
70. M. Rousseau, C. Belleannee, A.-C. Duchez, N. Cloutier, T. Levesque, F. Jacques, J. Perron, P. A. Nigrovic, M. Dieude, M.-J. Hebert, M. H. Gelb, E. Boilard, Detection and quantification of microparticles from different cellular lineages using flow cytometry. Evaluation of the impact of secreted phospholipase A2 on microparticle assessment. PLOS One 10, e0116812 (2015).
71. L. English, M. Chemali, J. Duron, C. Rondeau, A. Laplante, D. Gingras, D. Alexander, D. Leib, C. Norbury, R. Lippé, M. Desjardins, Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat. Immunol. 10, 480-487 (2009).
72. D. W. Huang, B. T. Sherman, R. A. Lempicki, Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
73. D. W. Huang, B. T. Sherman, R. A. Lempicki, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2008).
74. J. Koulack, V. C. McAlister, C. A. Giacomantonio, H. Bitter-Suermann, A. S. MacDonald, T. D. G. Lee, Development of a mouse aortic transplant model of chronic rejection. Microsurgery 16, 110-113 (1995).
75. K. Shimizu, S. Sugiyama, M. Aikawa, Y. Fukumoto, E. Rabkin, P. Libby, R. N. Mitchell, Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Nat. Med. 7, 738-741 (2001).
76. S. H. Lee, J. H. Lee, Y.-S. Han, J. M. Ryu, Y. M. Yoon, H. J. Han, Hypoxia accelerates vascular repair of endothelial colony-forming cells on ischemic injury via STAT3-BCL3 axis. Stem Cell Res. Ther. 6, 139 (2015).
77. J. Turgeon, S. Dussault, F. Maingrette, J. Groleau, P. Haddad, G. Perez, A. Rivard, Fish oilenriched diet protects against ischemia by improving angiogenesis, endothelial progenitor cell function and postnatal neovascularization. Atherosclerosis 229, 295-303 (2013).
78. M. Soulez, I. Sirois, N. Brassard, M.-A. Raymond, F. Nicodème, N. Noiseux, Y. Durocher, A. V. Pshezhetsky, M.-J. Hébert, Epidermal growth factor and perlecan fragments produced by apoptotic endothelial cells co-ordinately activate ERK1/2-dependent antiapoptotic pathways in mesenchymal stem cells. Stem Cells 28, 810-820 (2010).