Targeting pathogenic postischemic self-recognition by natural IgM to protect against posttransplantation cardiac reperfusion injury

Circulation

Volumn 131, Issue 13, 2015, Pages 1171-1180

  Atkinson, Carl ^a   Qiao, Fei ^a   Yang, Xiaofeng ^a   Zhu, Peng ^a   Reaves, Nicholas ^a   Kulik, Liudmila ^b   Goddard, Martin ^c   Holers, V Michael ^b   Tomlinson, Stephen ^a,d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c PAPWORTH HOSPITAL   (United Kingdom)

^d RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Antibodies; Complement system proteins; Inflammation; Ischemia; Transplantation

Indexed keywords

COMPLEMENT COMPONENT C3D; COMPLEMENT INHIBITOR; CRRY COMPLEMENT COMPONENT C3 INHIBITOR; EPITOPE; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 6; IODINE 125; KERATINOCYTE DERIVED CHEMOKINE; LIPOCORTIN 4; MONOCLONAL ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN 1; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TROPONIN I; UNCLASSIFIED DRUG; BISPECIFIC ANTIBODY; COMPLEMENT RECEPTOR; CRRY PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN M; PHOSPHOLIPID; RAG-1 PROTEIN; SYNTHETIC DNA;

ALLOTRANSPLANTATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; COLD ISCHEMIA; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG HALF LIFE; ENDOTHELIUM CELL; GRAFT RECIPIENT; HEART TRANSPLANTATION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; ISCHEMIA; MALE; MOUSE; NONHUMAN; ORGAN DONOR; POLYACRYLAMIDE GEL ELECTROPHORESIS; POSTTRANSPLANTATION CARDIAC REPERFUSION INJURY; PRIORITY JOURNAL; REPERFUSION INJURY; TISSUE DISTRIBUTION; WILD TYPE; ADVERSE EFFECTS; ANIMAL; ANTIBODY SPECIFICITY; BAGG ALBINO MOUSE; C57BL MOUSE; CARDIAC MUSCLE; DEFICIENCY; GENETICS; HEART MUSCLE REPERFUSION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; MYOCARDIAL REPERFUSION INJURY; TRANSPLANTATION TOLERANCE;

ANIMALS; ANNEXIN A4; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; COMPLEMENT ACTIVATION; EPITOPES; GENES, SYNTHETIC; HEART TRANSPLANTATION; HOMEODOMAIN PROTEINS; IMMUNOGLOBULIN M; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL REPERFUSION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; ORGAN SPECIFICITY; PHOSPHOLIPIDS; RECEPTORS, COMPLEMENT; RECOMBINANT FUSION PROTEINS; SELF TOLERANCE; SINGLE-CHAIN ANTIBODIES; TRANSPLANTATION TOLERANCE;

EID: 84929353534     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.010482     Document Type: Article

References (33)

1. Weiser MR, Williams JP, Moore FD Jr, Kobzik L, Ma M, Hechtman HB, Carroll MC. Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J Exp Med. 1996;183:2343-2348.
2. Zhang M, Alicot EM, Chiu I, Li J, Verna N, Vorup-Jensen T, Kessler B, Shimaoka M, Chan R, Friend D, Mahmood U, Weissleder R, Moore FD, Carroll MC. Identification of the target self-antigens in reperfusion injury. J Exp Med. 2006;203:141-152. doi: 10.1084/jem.20050390.
3. Zhang M, Austen WG Jr, Chiu I, Alicot EM, Hung R, Ma M, Verna N, Xu M, Hechtman HB, Moore FD Jr, Carroll MC. Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. Proc Natl Acad Sci U S A. 2004;101:3886-3891. doi: 10.1073/pnas.0400347101.
4. Elvington A, Atkinson C, Kulik L, Zhu H, Yu J, Kindy MS, Holers VM, Tomlinson S. Pathogenic natural antibodies propagate cerebral injury following ischemic stroke in mice. J Immunol. 2012;188:1460-1468. doi: 10.4049/jimmunol.1102132.
5. Kulik L, Fleming SD, Moratz C, Reuter JW, Novikov A, Chen K, Andrews KA, Markaryan A, Quigg RJ, Silverman GJ, Tsokos GC, Holers VM. Pathogenic natural antibodies recognizing annexin IV are required to develop intestinal ischemia-reperfusion injury. J Immunol. 2009;182:5363-5373. doi: 10.4049/jimmunol.0803980.
6. Gorsuch WB, Chrysanthou E, Schwaeble WJ, Stahl GL. The complement system in ischemia-reperfusion injuries. Immunobiology. 2012;217:1026-1033. doi: 10.1016/j.imbio.2012.07.024.
7. Atkinson C, Song H, Lu B, Qiao F, Burns TA, Holers VM, Tsokos GC, Tomlinson S. Targeted complement inhibition by C3d recognition ameliorates tissue injury without apparent increase in susceptibility to infection. J Clin Invest. 2005;115:2444-2453. doi: 10.1172/JCI25208.
8. Rescher U, Gerke V. Annexins: unique membrane binding proteins with diverse functions. J Cell Sci. 2004;117(pt 13):2631-2639. doi: 10.1242/jcs.01245.
9. Walsh MC, Bourcier T, Takahashi K, Shi L, Busche MN, Rother RP, Solomon SD, Ezekowitz RA, Stahl GL. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J Immunol. 2005;175:541-546.
10. Atkinson C, He S, Morris K, Qiao F, Casey S, Goddard M, Tomlinson S. Targeted complement inhibitors protect against posttransplant cardiac ischemia and reperfusion injury and reveal an important role for the alternative pathway of complement activation. J Immunol. 2010;185:7007-7013. doi: 10.4049/jimmunol.1001504.
11. Quigg RJ, Kozono Y, Berthiaume D, Lim A, Salant DJ, Weinfeld A, Griffin P, Kremmer E, Holers VM. Blockade of antibody-induced glomerulonephritis with Crry-Ig, a soluble murine complement inhibitor. J Immunol. 1998;160:4553-4560.
12. Leinhase I, Schmidt OI, Thurman JM, Hossini AM, Rozanski M, Taha ME, Scheffler A, John T, Smith WR, Holers VM, Stahel PF. Pharmacological complement inhibition at the C3 convertase level promotes neuronal survival, neuroprotective intracerebral gene expression, and neurological outcome after traumatic brain injury. Exp Neurol. 2006;199:454-464. doi: 10.1016/j.expneurol.2006.01.033.
13. Bao L, Haas M, Kraus DM, Hack BK, Rakstang JK, Holers VM, Quigg RJ. Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice. J Am Soc Nephrol. 2003;14:670-679.
14. Banda NK, Kraus D, Vondracek A, Huynh LH, Bendele A, Holers VM, Arend WP. Mechanisms of effects of complement inhibition in murine collagen-induced arthritis. Arthritis Rheum. 2002;46:3065-3075. doi: 10.1002/art.10591.
15. Baumgarth N, Herman OC, Jager GC, Brown L, Herzenberg LA, Herzenberg LA. Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc Natl Acad Sci U S A. 1999;96:2250-2255.
16. Silverman GJ, Grönwall C, Vas J, Chen Y. Natural autoantibodies to apoptotic cell membranes regulate fundamental innate immune functions and suppress inflammation. Discov Med. 2009;8:151-156.
17. Zhang M, Michael LH, Grosjean SA, Kelly RA, Carroll MC, Entman ML. The role of natural IgM in myocardial ischemia-reperfusion injury. J Mol Cell Cardiol. 2006;41:62-67. doi: 10.1016/j.yjmcc.2006.02.006.
18. Haas MS, Alicot EM, Schuerpf F, Chiu I, Li J, Moore FD, Carroll MC. Blockade of self-reactive IgM significantly reduces injury in a murine model of acute myocardial infarction. Cardiovasc Res. 2010;87:618-627. doi: 10.1093/cvr/cvq141.
19. Fleming SD, Egan RP, Chai C, Girardi G, Holers VM, Salmon J, Monestier M, Tsokos GC. Anti-phospholipid antibodies restore mesenteric ischemia/reperfusion-induced injury in complement receptor 2/complement receptor 1-deficient mice. J Immunol. 2004;173:7055-7061.
20. Molina H, Wong W, Kinoshita T, Brenner C, Foley S, Holers VM. Distinct receptor and regulatory properties of recombinant mouse complement receptor 1 (CR1) and Crry, the two genetic homologues of human CR1. J Exp Med. 1992;175:121-129.
21. Testa L, Van Gaal WJ, Bhindi R, Biondi-Zoccai GG, Abbate A, Agostoni P, Porto I, Andreotti F, Crea F, Banning AP. Pexelizumab in ischemic heart disease: a systematic review and meta-analysis on 15,196 patients. J Thorac Cardiovasc Surg. 2008;136:884-893. doi: 10.1016/j.jtcvs.2007.12.062.
22. Raedler H, Vieyra MB, Leisman S, Lakhani P, Kwan W, Yang M, Johnson K, Faas SJ, Tamburini P, Heeger PS. Anti-complement component C5 mAb synergizes with CTLA4Ig to inhibit alloreactive T cells and prolong cardiac allograft survival in mice. Am J Transplant. 2011;11:1397-1406. doi: 10.1111/j.1600-6143.2011.03561.x.
23. Ferraresso M, Macor P, Valente M, Della Barbera M, D'Amelio F, Borghi O, Raschi E, Durigutto P, Meroni P, Tedesco F. Posttransplant ischemia-reperfusion injury in transplanted heart is prevented by a minibody to the fifth component of complement. Transplantation. 2008;86:1445-1451. doi: 10.1097/TP.0b013e31818a68e2.
24. Raedler H, Yang M, Lalli PN, Medof ME, Heeger PS. Primed CD8(+) T-cell responses to allogeneic endothelial cells are controlled by local complement activation. Am J Transplant. 2009;9:1784-1795. doi: 10.1111/j.1600-6143.2009.02723.x.
25. Kwan WH, Hashimoto D, Paz-Artal E, Ostrow K, Greter M, Raedler H, Medof ME, Merad M, Heeger PS. Antigen-presenting cell-derived complement modulates graft-versus-host disease. J Clin Invest. 2012;122:2234-2238. doi: 10.1172/JCI61019.
26. Patel H, Smith RA, Sacks SH, Zhou W. Therapeutic strategy with a membrane-localizing complement regulator to increase the number of usable donor organs after prolonged cold storage. J Am Soc Nephrol. 2006;17:1102-1111. doi: 10.1681/ASN.2005101116.
27. Atkinson C, Floerchinger B, Qiao F, Casey S, Williamson T, Moseley E, Stoica S, Goddard M, Ge X, Tullius SG, Tomlinson S. Donor brain death exacerbates complement-dependent ischemia reperfusion injury in transplanted hearts. Circulation. 2013;127:1290-1299.
28. Holers VM, Rohrer B, Tomlinson S. CR2-mediated targeting of complement inhibitors: bench-to-bedside using a novel strategy for site-specific complement modulation. Adv Exp Med Biol. 2013;735:137-154.
29. Oroszlán M, Daha MR, Cervenak L, Prohászka Z, Füst G, Roos A. MBL and C1q compete for interaction with human endothelial cells. Mol Immunol. 2007;44:1150-1158. doi: 10.1016/j.molimm.2006.06.015.
30. Delcayre AX, Salas F, Mathur S, Kovats K, Lotz M, Lernhardt W. Epstein Barr virus/complement C3d receptor is an interferon alpha receptor. EMBO J. 1991;10:919-926.
31. Aubry JP, Pochon S, Graber P, Jansen KU, Bonnefoy JY. CD21 is a ligand for CD23 and regulates IgE production. Nature. 1992;358:505-507. doi: 10.1038/358505a0.
32. Holers VM, Kulik L. Complement receptor 2, natural antibodies and innate immunity: inter-relationships in B cell selection and activation. Mol Immunol. 2007;44:64-72. doi: 10.1016/j.molimm.2006.07.003.
33. Lowell CA, Klickstein LB, Carter RH, Mitchell JA, Fearon DT, Ahearn JM. Mapping of the Epstein-Barr virus and C3dg binding sites to a common domain on complement receptor type 2. J Exp Med. 1989;170:1931-1946.