Identification of the target self-antigens in reperfusion injury

Journal of Experimental Medicine

Volumn 203, Issue 1, 2006, Pages 141-152

  Zhang, Ming ^a,b,e   Alicot, Elisabeth M ^e   Chiu, Isaac ^a   Li, Jinan ^a   Verna, Nicola ^b   Vorup Jensen, Thomas ^a   Kessler, Benedikt ^b   Shimaoka, Motomu ^a   Chan, Rodney ^b   Friend, Daniel ^b   Mahmood, Umar ^d   Weissleder, Ralph ^d   Moore, Francis D ^b,c   Carroll, Michael C ^a,b  

^a CENTER FOR BLOOD RESEARCH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e DecImmune Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN M; MYOSIN IIA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ARTICLE; CONTROLLED STUDY; HYPOXIA; IMMUNE RESPONSE; IMMUNOPRECIPITATION; INNATE IMMUNITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; CAPILLARY PERMEABILITY; HINDLIMB; HOMEODOMAIN PROTEINS; IMMUNITY, NATURAL; IMMUNOGLOBULIN M; ISCHEMIA; JEJUNUM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; NONMUSCLE MYOSIN TYPE IIA; REPERFUSION INJURY;

EID: 31344460778     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20050390     Document Type: Article

References (58)

1. Wu, B., A. Ootani, R. Iwakiri, T. Fujise, S. Tsunada, S. Toda, and K. Fujimoto. 2004. Ischemic preconditioning attenuates ischemia-reperfusion-induced mucosal apoptosis by inhibiting the mitochondria-dependent pathway in rat small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 286:G580-G587.
2. Thiemermann, C., J. Bowes, F.P. Myint, and J.R. Vane. 1997. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc. Natl. Acad. Sci. USA. 94:679-683.
3. Szabo, G., L. Liaudet, S. Hagl, and C. Szabo. 2004. Poly(ADP-ribose) polymerase activation in the reperfused myocardium. Cardiovasc. Res. 61:471-480.
4. Becker, L.B. 2004. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc. Res. 61:461-470.
5. Becker, L.B., T.L. Vanden Hoek, Z.H. Shao, C.Q. Li, and P.T. Schumacker. 1999. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am. J. Physiol. 277:H2240-H2246.
6. Li, C., and R. Jackson. 2002. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am. J. Physiol. Cell Physiol. 282:C227-C241.
7. Briaud, S.A., Z.M. Ding, L.H. Michael, M.L. Entman, S. Daniel, and C.M. Ballantyne. 2001. Leukocyte trafficking and myocardial reperfusion injury in ICAM-1/P-selectin-knockout mice. Am. J. Physiol. Heart Circ. Physiol. 280:H60-H67.
8. Bowden, R.A., Z.M. Ding, E.M. Donnachie, T.K. Petersen, L.H. Michael, C.M. Ballantyne, and A.R. Burns. 2002. Role of alpha4 integrin and VCAM-1 in CD18-independent neutrophil migration across mouse cardiac endothelium. Circ. Res. 90:562-569.
9. Hill, J.H., and P.A. Ward. 1971. The phlogistic role of C3 leukotactic fragments in myocardial infarcts of rats. J. Exp. Med. 133:885-900.
10. Weisman, H.F., T. Bartow, M.K. Leppo, H.C. Marsh, G.R. Carson, M.F. Concino, M.P. Boyle, K.H. Roux, M.L. Weisfeldt, and D.T. Fearon. 1990. Soluble human complement receptor type I: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science. 249:146-151.
11. Chai, P.J., R. Nassar, A.E. Oakeley, D.M. Craig, G. Quick Jr., J. Jaggers, S.P. Sanders, R.M. Ungerleider, and P.A. Anderson. 2000. Soluble complement receptor-1 protects heart, lung, and cardiac myofilament function from cardiopulmonary bypass damage. Circulation. 101:541-546.
12. Huang, J., L. Kim, R. Mealey, H. Marsh, Y. Zhang, A. Tenner, E. Connolly, and D. Pinsky. 1999. Neuronal protection in stroke by an sLex-glycosylated complement inhibitory protein. Science. 285:595-599.
13. Hill, J., T.F. Lindsay, F. Ortiz, C.G. Yeh, H.B. Hechtman, and F.D. Moore. 1992. Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat. J. Immunol. 149:1723-1730.
14. Schafer, H., D. Mathey, F. Hugo, and S. Bhakdi. 1986. Deposition of terminal C5b-9 complement complex in infarcted areas of human myocardium. J. Immunol. 137:1945-1949.
15. Robert-Offerman, S.R., M.P. Leers, R.J. van Suylen, M. Nap, M.J. Daemen, and P.H. Theunissen. 2000. Evaluation of the membrane attack complex of complement for the detection of a recent myocardial infarction in man. J. Pathol. 191:48-53.
16. Fleming, S.D., D. Mastellos, G. Karpel-Massler, T. Shea-Donohue, J.D. Lambris, and G.C. Tsokos. 2003. C5a causes limited, polymorphonuclear cell-independent, mesenteric ischemia/reperfusion-induced injury. Clin. Immunol. 108:263-273.
17. Homeister, J.W., P. Satoh, and B.R. Lucchesi. 1992. Effects of complement activation in the isolated heart. Role of the terminal complement components. Circ. Res. 71:303-319.
18. Zhao, H., M.C. Montalto, K.J. Pfeiffer, L. Hao, and G.L. Stahl. 2002. Murine model of gastrointestinal ischemia associated with complement-dependent injury. J. Appl. Physiol. 93:338-345.
19. Austen, W.G., Jr., C. Kyriakides, J. Favuzza, Y. Wang, L. Kobzik, F.D. Moore Jr., and H.B. Hechtman. 1999. Intestinal ischemia-reperfusion injury is mediated by the membrane attack complex. Surgery. 126:343-348.
20. Kilgore, K.S., J.L. Park, E.J. Tanhehco, E.A. Booth, R.M. Marks, and B.R. Lucchesi. 1998. Attenuation of interleukin-8 expression in C6-deficient rabbits after myocardial ischemia/reperfusion. J. Mol. Cell. Cardiol. 30:75-85.
21. Ito, W., H.J. Schafer, S. Bhakdi, R. Klask, S. Hansen, S. Schaarschmidt, J. Schofer, F. Hugo, T. Hamdoch, and D. Mathey. 1996. Influence of the terminal complement-complex on reperfusion injury, no-reflow and arrhythmias: a comparison between C6-competent and C6-deficient rabbits. Cardiovasc. Res. 32:294-305.
22. Abonia, J.P., D.S. Friend, W.G. Austen Jr., F.D. Moore Jr., M.C. Carroll, R. Chan, J. Afnan, A. Humbles, C. Gerard, P. Knight, et al. 2005. Mast cell protease 5 mediates ischemia-reperfusion injury of mouse skeletal muscle. J. Immunol. 174:7285-7291.
23. Weiser, M., J. Williams, F. Moore, L. Kobzik, M. Ma, H. Hechtman, and M. Carroll. 1996. Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J. Exp. Med. 183:2343-2348.
24. Williams, J.P., F.D. Moore, L. Kobzik, M.C. Carroll, and H.B. Hechtman. 1999. Intestinal reperfusion injury is mediated by IgM and complement. J. Appl. Physiol. 86:938-942.
25. Fleming, S.D., T. Shea-Donohue, J.M. Guthridge, L. Kulik, T.J. Waldschmidt, M.G. Gipson, G.C. Tsokos, and V.M. Holers. 2002. Mice deficient in complement receptors 1 and 2 lack a tissue injury-inducing subset of the natural antibody repertoire. J. Immunol. 169:2126-2133.
26. Reid, R.R., S. Woodcock, A. Shimabukuro-Vornhagen, W.G. Austen Jr., L. Kobzik, M. Zhang, H.B. Hechtman, F.D. Moore Jr., and M.C. Carroll. 2002. Functional activity of natural antibody is altered in Cr2-deficient mice. J. Immunol. 169:5433-5440.
27. Zhang, M., W.G. Austen Jr., I. Chiu, E.M. Alicot, R. Hung, M. Ma, N. Verna, M. Xu, H.B. Hechtman, F.D. Moore Jr., and M.C. Carroll. 2004. Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. Proc. Natl. Acad. Sci. USA. 101:3886-3891.
28. Austen, W.G., Jr., M. Zhang, R. Chan, D. Friend, H.B. Hechtman, M.C. Carroll, and F.D. Moore Jr. 2004. Murine hindlimb reperfusion injury can be initiated by a self-reactive monoclonal IgM. Surgery. 136:401-406.
29. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature. 430:257-263.
30. Carroll, M.C., and V.M. Holers. 2005. Innate autoimmunity. Adv. Immunol. 86:137-157.
31. Kocks, C., R. Maehr, H.S. Overkleeft, E.W. Wang, L.K. Iyer, A.M. Lennon-Dumenil, H.L. Ploegh, and B.M. Kessler. 2003. Functional proteomics of the active cysteine protease content in drosophila S2 cells. Mol. Cell. Proteomics. 2:1188-1197.
32. Golomb, E., X. Ma, S.S. Jana, Y.A. Preston, S. Kawamoto, N.G. Shoham, E. Goldin, M.A. Conti, J.R. Sellers, and R.S. Adelstein. 2004. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J. Biol. Chem. 279:2800-2808.
33. Kelley, C.A., J.R. Sellers, D.L. Gard, D. Bui, R.S. Adelstein, and I.C. Baines. 1996. Xenopus nonmuscle myosin heavy chain isoforms have different subcellular localizations and enzymatic activities. J. Cell Biol. 134:675-687.
34. Hart, M.L., K.A. Ceonzo, L.A. Shaffer, K. Takahashi, R.P. Rother, W.R. Reenstra, J.A. Buras, and G.L. Stahl. 2005. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J. Immunol. 174:6373-6380.
35. Hardy, R.R., C.E. Carmack, Y.S. Li, and K. Hayakawa. 1994. Distinctive developmental origins and specificities of murine CD5+ B cells. Immunol. Rev. 137:91-118.
36. Herzenberg, L.A., and A.B. Kantor. 1993. B cell lineages exist in the mouse. Immunol. Today. 14:79-83.
37. Arnold, L., C. Pennell, S. McCray, and S. Clarke. 1994. Development of B-1 cells: segregation of phosphatidyl choline-specific B cells to the B-1 population occurs after immunoglobulin gene expression. J. Exp. Med. 179:1585-1595.
38. Bendelac, A., M. Bonneville, and J.F. Kearney. 2001. Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 1:177-186.
39. Martin, F., and J. Kearney. 2001. B1 cells: similarities and differences with other B cell subsets. Curr. Opin. Immunol. 13:195-201.
40. Bresnick, A.R. 1999. Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11:26-33.
41. Zorov, D.B., C.R. Filburn, L.O. Klotz, J.L. Zweier, and S.J. Sollott. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med. 192:1001-1014.
42. Kolega, J. 1998. Cytoplasmic dynamics of myosin IIA and IIB: spatial "sorting" of isoforms in locomoting cells. J. Cell Sci. 111:2085-2095.
43. Gasser, S., S. Orsulic, E.J. Brown, and D.H. Raulet. 2005. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature. 436:1186-1190.
44. Fleming, S.D., R.P. Egan, C. Chai, G. Girardi, V.M. Holers, J. Salmon, M. Monestier, and G.C. Tsokos. 2004. Anti-phospholipid antibodies restore mesenteric ischemia/reperfusion-induced injury in complement receptor 2/complement receptor 1-deficient mice. J. Immunol. 173:7055-7061.
45. Fleming, S.D., M. Monestier, and G.C. Tsokos. 2004. Accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice. J. Immunol. 173:4230-4235.
46. Eisenberg, R.A., S.Y. Craven, C.L. Fisher, S.C. Morris, R. Rapoport, D.S. Pisetsky, and P.L. Cohen. 1989. The genetics of autoantibody production in MRL/lpr lupus mice. Clin. Exp. Rheumatol. 7:S35-S40.
47. Paimela, H., P.J. Goddard, and W. Silen. 1995. Present views on restitution of gastrointestinal epithelium. Dig. Dis. Sci. 40:2495-2496.
48. Fujita, T., M. Matsushita, and Y. Endo. 2004. The lectin-complement pathway - its role in innate immunity and evolution. Immunol. Rev. 198:185-202.
49. Vandivier, R.W., C.A. Ogden, V.A. Fadok, P.R. Hoffmann, K.K. Brown, M. Botto, M.J. Walport, J.H. Fisher, P.M. Henson, and K.E. Greene. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169:3978-3986.
50. Gardai, S.J., Y.Q. Xiao, M. Dickinson, J.A. Nick, D.R. Voelker, K.E. Greene, and P.M. Henson. 2003. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell. 115:13-23.
51. Taylor, P.R., A. Carugati, V.A. Fadok, H.T. Cook, M. Andrews, M.C. Carroll, J.S. Savill, P.M. Henson, M. Botto, and M.J. Walport. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192:359-366.
52. Cotran, R.S., V. Kumar, and S.L. Robbins. 1994. Pathologic Basis of Disease. Fifth edition. W.B. Saunders, Philadelphia. 1425 pp.
53. Brandt, L.J. 2003. Messenteric vascular diease. In Current Diagnosis and Treatment in Gastroenterology. Second edition. S.L. Friedman, editor. McGraw-Hill Inc., New York. Chapter 9.
54. Chiu, C.J., A.H. McArdle, R. Brown, H.J. Scott, and F.N. Gurd. 1970. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch. Surg. 101:478-483.
55. Vorup-Jensen, T., C. Ostermeier, M. Shimaoka, U. Hommel, and T.A. Springer. 2003. Structure and allosteric regulation of the alpha X beta 2 integrin I domain. Proc. Natl. Acad. Sci. USA. 100:1873-1878.
56. Borodovsky, A., H. Ovaa, N. Kolli, T. Gan-Erdene, K.D. Wilkinson, H.L. Ploegh, and B.M. Kessler. 2002. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9:1149-1159.
57. Wang, Q., C.H. Fang, and P.O. Hasselgren. 2001. Intestinal permeability is reduced and IL-10 levels are increased in septic IL-6 knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R1013-R1023.
58. Alencar, H., U. Mahmood, Y. Kawano, T. Hirata, and R. Weissleder. 2005. Novel multiwavelength microscopic scanner for mouse imaging. Neoplasia. 7:977-983.