Mannan-binding lectin-associated serine protease 2 is critical for the development of renal ischemia reperfusion injury and mediates tissue injury in the absence of complement C4

FASEB Journal

Volumn 28, Issue 9, 2014, Pages 3996-4003

  Asgari, Elham ^a   Farrar, Conrad A ^a   Lynch, Nicholas ^b   Ali, Youssif M ^b   Roscher, Silke ^b   Stover, Cordula ^b   Zhou, Wuding ^a   Schwaeble, Wilhelm J ^b   Sacks, Steven H ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Inflammation; Kidney transplantation

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 2; UNCLASSIFIED DRUG; C4 PROTEIN, MOUSE; COMPLEMENT COMPONENT C3D; MASP-2 PROTEIN, MOUSE;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DONOR; EXPERIMENTAL TRANSPLANTATION; GRAFT RECIPIENT; KIDNEY FUNCTION; KIDNEY GRAFT; KIDNEY ISCHEMIA; KIDNEY TRANSPLANTATION; MOUSE; NEPHRECTOMY; NONHUMAN; REPERFUSION INJURY; TISSUE INJURY; WILD TYPE; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; ENZYME IMMUNOASSAY; FEMALE; KIDNEY DISEASES; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY; POSTOPERATIVE COMPLICATION; UREA NITROGEN BLOOD LEVEL;

ANIMALS; BLOOD UREA NITROGEN; COMPLEMENT C3D; COMPLEMENT C4; FEMALE; IMMUNOENZYME TECHNIQUES; KIDNEY DISEASES; KIDNEY TRANSPLANTATION; MALE; MANNOSE-BINDING PROTEIN-ASSOCIATED SERINE PROTEASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEPHRECTOMY; POSTOPERATIVE COMPLICATIONS; REPERFUSION INJURY;

EID: 84907200730     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-246306     Document Type: Article

References (44)

1. Damman, J., Schuurs, T. A., Ploeg, R. J., and Seelen, M. A. (2008) Complement and renal transplantation: from donor to recipient. Transplantation 85, 923-927
2. Shoskes, D. A., and Cecka, J. M. (1998) Deleterious effects of delayed graft function in cadaveric renal transplant recipients independent of acute rejection. Transplantation 66, 1697-1701
3. Boros, P., and Bromberg, J. S. (2006) New cellular and molecular immune pathways in ischemia/reperfusion injury. Am. J. Transplant. 6, 652-658
4. Mastellos, D., Morikis, D., Isaacs, S. N., Holland, M. C., Strey, C. W., and Lambris, J. D. (2003) Complement: structure, functions, evolution, and viral molecular mimicry. Immunol. Res. 27, 367-386
5. Collard, C. D., Vakeva, A., Morrissey, M. A., Agah, A., Rollins, S. A., Reenstra, W. R., Buras, J. A., Meri, S., and Stahl, G. L. (2000) Complement activation after oxidative stress: role of the lectin complement pathway. Am. J. Pathol. 156, 1549-1556
6. Fujita, T. (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat. Rev. Immunol. 2, 346-353
7. Ali, Y. M., Lynch, N. J., Haleem, K. S., Fujita, T., Endo, Y., Hansen, S., Holmskov, U., Takahashi, K., Stahl, G. L., Dudler, T., Girija, U. V., Wallis, R., Kadioglu, A., Stover, C. M., Andrew, P. W., and Schwaeble, W. J. (2012) The lectin pathway of complement activation is a critical component of the innate immune response to pneumococcal infection. PLoS Pathog. 8, e1002793
8. Lachmann, P. J., and Halbwachs, L. (1975) The influence of C3b inactivator (KAF) concentration on the ability of serum to support complement activation. Clin. Exp. Immunol. 21, 109-114
9. Diepenhorst, G. M., van Gulik, T. M., and Hack, C. E. (2009) Complement-mediated ischemia-reperfusion injury: lessons learned from animal and clinical studies. Ann. Surg. 249, 889-899
10. Zhou, W., Farrar, C. A., Abe, K., Pratt, J. R., Marsh, J. E., Wang, Y., Stahl, G. L., and Sacks, S. H. (2000) Predominant role for C5b-9 in renal ischemia/reperfusion injury. J. Clin. Invest. 105, 1363-1371
11. Hart, M. L., Ceonzo, K. A., Shaffer, L. A., Takahashi, K., Rother, R. P., Reenstra, W. R., Buras, J. A., and Stahl, G. L. (2005) Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J. Immunol. 174, 6373-6380
12. Walsh, M. C., Bourcier, T., Takahashi, K., Shi, L., Busche, M. N., Rother, R. P., Solomon, S. D., Ezekowitz, R. A., and Stahl, G. L. (2005) Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J. Immunol. 175, 541-546
13. Thurman, J. M., Lucia, M. S., Ljubanovic, D., and Holers, V. M. (2005) Acute tubular necrosis is characterized by activation of the alternative pathway of complement. Kidney Int. 67, 524-530
14. Thurman, J. M., Royer, P. A., Ljubanovic, D., Dursun, B., Lenderink, A. M., Edelstein, C. L., and Holers, V. M. (2006) Treatment with an inhibitory monoclonal antibody to mouse factor B protects mice from induction of apoptosis and renal ischemia/reperfusion injury. J. Am. Soc. Nephrol. 17, 707-715
15. Thurman, J. M., Ljubanovic, D., Edelstein, C. L., Gilkeson, G. S., and Holers, V. M. (2003) Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. J. Immunol. 170, 1517-1523
16. Moller-Kristensen, M., Wang, W., Ruseva, M., Thiel, S., Nielsen, S., Takahashi, K., Shi, L., Ezekowitz, A., Jensenius, J. C., and Gadjeva, M. (2005) Mannan-binding lectin recognizes structures on ischaemic reperfused mouse kidneys and is implicated in tissue injury. Scand. J. Immunol. 61, 426-434
17. de Vries, B., Walter, S. J., Peutz-Kootstra, C. J., Wolfs, T. G., van Heurn, L. W., and Buurman, W. A. (2004) The mannose-binding lectin-pathway is involved in complement activation in the course of renal ischemia-reperfusion injury. Am. J. Pathol. 165, 1677-1688
18. Osthoff, M., Katan, M., Fluri, F., Schuetz, P., Bingisser, R., Kappos, L., Steck, A. J., Engelter, S. T., Mueller, B., Christ-Crain, M., and Trendelenburg, M. (2011) Mannose-binding lectin deficiency is associated with smaller infarction size and favorable outcome in ischemic stroke patients. PLoS ONE 6, e21338
19. Cervera, A., Planas, A. M., Justicia, C., Urra, X., Jensenius, J. C., Torres, F., Lozano, F., and Chamorro, A. (2010) Genetically-defined deficiency of mannose-binding lectin is associated with protection after experimental stroke in mice and outcome in human stroke. PLoS ONE 5, e8433
20. Chan, R. K., Ibrahim, S. I., Takahashi, K., Kwon, E., McCormack, M., Ezekowitz, A., Carroll, M. C., Moore, F. D., Jr., and Austen, W. G., Jr. (2006) The differing roles of the classical and mannose-binding lectin complement pathways in the events following skeletal muscle ischemia-reperfusion. J. Immunol. 177, 8080-8085
21. Jordan, J. E., Montalto, M. C., and Stahl, G. L. (2001) Inhibition of mannose-binding lectin reduces postischemic myocardial reperfusion injury. Circulation 104, 1413-1418
22. Weiser, M. R., Williams, J. P., Moore, F. D., Jr., Kobzik, L., Ma, M., Hechtman, H. B., and Carroll, M. C. (1996) Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J. Exp. Med. 183, 2343-2348
23. Williams, J. P., Pechet, T. T., Weiser, M. R., Reid, R., Kobzik, L., Moore, F. D., Jr., Carroll, M. C., and Hechtman, H. B. (1999) Intestinal reperfusion injury is mediated by IgM and complement. J. Appl. Physiol. 86, 938-942
24. Zhang, M., Alicot, E. M., Chiu, I., Li, J., Verna, N., Vorup-Jensen, T., Kessler, B., Shimaoka, M., Chan, R., Friend, D., Mahmood, U., Weissleder, R., Moore, F. D., and Carroll, M. C. (2006) Identification of the target self-antigens in reperfusion injury. J. Exp. Med. 203, 141-152
25. McMullen, M. E., Hart, M. L., Walsh, M. C., Buras, J., Takahashi, K., and Stahl, G. L. (2006) Mannose-binding lectin binds IgM to activate the lectin complement pathway in vitro and in vivo. Immunobiology 211, 759-766
26. Busche, M. N., Pavlov, V., Takahashi, K., and Stahl, G. L. (2009) Myocardial ischemia and reperfusion injury is dependent on both IgM and mannose-binding lectin. Am. J. Physiol. Heart Circ. Physiol. 297, H1853-H1859
27. Zhang, M., Takahashi, K., Alicot, E. M., Vorup-Jensen, T., Kessler, B., Thiel, S., Jensenius, J. C., Ezekowitz, R. A., Moore, F. D., and Carroll, M. C. (2006) Activation of the lectin pathway by natural IgM in a model of ischemia/reperfusion injury. J. Immunol. 177, 4727-4734
28. Hirano, M., Ma, B. Y., Kawasaki, N., Oka, S., and Kawasaki, T. (2012) Role of interaction of mannan-binding protein with meprins at the initial step of complement activation in ischemia/reperfusion injury to mouse kidney. Glycobiology 22, 84-95
29. Schwaeble, W. J., Lynch, N. J., Clark, J. E., Marber, M., Samani, N. J., Ali, Y. M., Dudler, T., Parent, B., Lhotta, K., Wallis, R., Farrar, C. A., Sacks, S., Lee, H., Zhang, M., Iwaki, D., Takahashi, M., Fujita, T., Tedford, C. E., and Stover, C. M. (2011) Targeting of mannan-binding lectin-associated serine protease-2 confers protection from myocardial and gastrointestinal ischemia/reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 108, 7523-7528
30. Wessels, M. R., Butko, P., Ma, M., Warren, H. B., Lage, A. L., and Carroll, M. C. (1995) Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. U. S. A. 92, 11490-11494
31. Kalina, S. L., and Mottram, P. L. (1993) A microsurgical technique for renal transplantation in mice. Aust. N. Z. J. Surg. 63, 213-216
32. Wyss-Coray, T., Yan, F., Lin, A. H., Lambris, J. D., Alexander, J. J., Quigg, R. J., and Masliah, E. (2002) Prominent neurodegeneration and increased plaque formation in complementinhibited Alzheimer's mice. Proc. Natl. Acad. Sci. U. S. A. 99, 10837-10842
33. Stover, C. M., Thiel, S., Lynch, N. J., and Schwaeble, W. J. (1999) The rat and mouse homologues of MASP-2 and MAp19, components of the lectin activation pathway of complement. J. Immunol. 163, 6848-6859
34. Gal, P., Harmat, V., Kocsis, A., Bian, T., Barna, L., Ambrus, G., Vegh, B., Balczer, J., Sim, R. B., Naray-Szabo, G., and Zavodszky, P. (2005) A true autoactivating enzyme. Structural insight into mannose-binding lectin-associated serine protease-2 activations. J. Biol. Chem. 280, 33435-33444
35. Farrar, C. A., Wang, Y., Sacks, S. H., and Zhou, W. (2004) Independent pathways of P-selectin and complement-mediated renal ischemia/reperfusion injury. Am. J. Pathol. 164, 133-141
36. Selander, B. (2006) Mannan-binding lectin activates C3 and the alternative complement pathway without involvement of C2. J. Clin. Invest. 116, 1425-1434
37. Peng, Q., Li, K., Smyth, L. A., Xing, G., Wang, N., Meader, L., Lu, B., Sacks, S. H., and Zhou, W. (2012) C3a and C5a promote renal ischemia-reperfusion injury. J. Am. Soc. Nephrol. 23, 1474-1485
38. Lewis, A. G., Kohl, G., Ma, Q., Devarajan, P., and Kohl, J. (2008) Pharmacological targeting of C5a receptors during organ preservation improves kidney graft survival. Clin. Exp. Immunol. 153, 117-126
39. Zheng, X., Zhang, X., Feng, B., Sun, H., Suzuki, M., Ichim, T., Kubo, N., Wong, A., Min, L. R., Budohn, M. E., Garcia, B., Jevnikar, A. M., and Min, W. P. (2008) Gene silencing of complement C5a receptor using siRNA for preventing ischemia/reperfusion injury. Am. J. Pathol. 173, 973-980
40. Patel, H., Smith, R. A., Sacks, S. H., and Zhou, W. (2006) Therapeutic strategy with a membrane-localizing complement regulator to increase the number of usable donor organs after prolonged cold storage. J. Am. Soc. Nephrol. 17, 1102-1111
41. Van der Pol, P., Schlagwein, N., van Gijlswijk, D. J., Berger, S. P., Roos, A., Bajema, I. M., de Boer, H. C., de Fijter, J. W., Stahl, G. L., Daha, M. R., and van Kooten, C. (2012) Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am. J. Transplant. 12, 877-887
42. Park, P., Haas, M., Cunningham, P. N., Alexander, J. J., Bao, L., Guthridge, J. M., Kraus, D. M., Holers, V. M., and Quigg, R. J. (2001) Inhibiting the complement system does not reduce injury in renal ischemia reperfusion. J. Am. Soc. Nephrol. 12, 1383-1390
43. Zhang, M., Alicot, E. M., and Carroll, M. C. (2008) Human natural IgM can induce ischemia/reperfusion injury in a murine intestinal model. Mol. Immunol. 45, 4036-4039
44. Zhang, M., and Carroll, M. C. (2007) Natural antibody mediated innate autoimmune response. Mol. Immunol. 44, 103-110