Critical role and therapeutic control of the lectin pathway of complement activation in an abortion-prone mouse mating

Journal of Immunology

Volumn 195, Issue 12, 2015, Pages 5602-5607

  Petitbarat, Marie ^a   Durigutto, Paolo ^b   Macor, Paolo ^b   Bulla, Roberta ^b   Palmioli, Alessandro ^c   Bernardi, Anna ^c   De Simoni, Maria Grazia ^d   Ledee, Nathalie ^a   Chaouat, Gerard ^e   Tedesco, Francesco ^f  

^a SAINT LOUIS HOSPITAL   (France)

^b UNIVERSITY OF TRIESTE   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^e INSERM   (France)

^f ISTITUTO AUXOLOGICO ITALIANO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1R; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C9; MANNOSE BINDING LECTIN; MANNOSE BINDING LECTIN A; MANNOSE BINDING LECTIN C; MANNOSIDE; POLYMAN2; UNCLASSIFIED DRUG; BLOCKING ANTIBODY; COMPLEMENT COMPONENT C5; MANNOSE BINDING PROTEIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CBA MOUSE; CHEMOPROPHYLAXIS; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; COMPLEMENT LECTIN PATHWAY; CONTROLLED STUDY; DBA 2 MOUSE; FEMALE; MALE; MATING; MOUSE; NIDATION; NONHUMAN; PREGNANCY TERMINATION; PRIORITY JOURNAL; SPONTANEOUS ABORTION; ANIMAL; DBA MOUSE; DISEASE MODEL; DRUG EFFECTS; HUMAN; IMMUNOLOGY; METABOLISM; PRE-ECLAMPSIA; PREGNANCY;

ANIMALS; ANTIBODIES, BLOCKING; COMPLEMENT C5; COMPLEMENT PATHWAY, MANNOSE-BINDING LECTIN; DISEASE MODELS, ANIMAL; EMBRYO IMPLANTATION; FEMALE; HUMANS; MALE; MANNOSE-BINDING LECTIN; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; MICE, INBRED DBA; PRE-ECLAMPSIA; PREGNANCY;

EID: 84958279890     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501361     Document Type: Article

References (40)

1. Hsu, P., and R. K. Nanan. 2014. Innate and adaptive immune interactions at the fetal-maternal interface in healthy human pregnancy and pre-eclampsia. Front. Immunol. 5: 125.
2. Denny, K. J., T. M. Woodruff, S. M. Taylor, and L. K. Callaway. 2013. Complement in pregnancy: a delicate balance. Am. J. Reprod. Immunol. 69: 3-11.
3. Girardi, G., Z. Prohászka, R. Bulla, F. Tedesco, and S. Scherjon. 2011. Complement activation in animal and human pregnancies as a model for immuno-logical recognition. Mol. Immunol. 48: 1621-1630.
4. Bulla, R., F. Bossi, and F. Tedesco. 2012. The complement system at the embryo implantation site: friend or foe? Front. Immunol. 3: 55.
5. Redman, C. W. 2011. Preeclampsia: a multi-stress disorder. Rev. Med. Interne 32 (Suppl. 1): S41-S44.
6. Chaiworapongsa, T., P. Chaemsaithong, L. Yeo, and R. Romero. 2014. Pre-eclampsia part 1: current understanding of its pathophysiology. Nat. Rev. Nephrol. 10: 466-480.
7. Chaouat, G., N. Kiger, and T. G. Wegmann. 1983. Vaccination against spontaneous abortion in mice. J. Reprod. Immunol. 5: 389-392.
8. Clark, D. A., M. R. McDermott, and M. R. Szewczuk. 1980. Impairment of host-versus-graft reaction in pregnant mice. II. Selective suppression of cytotoxic T-cell generation correlates with soluble suppressor activity and with successful allogeneic pregnancy. Cell. Immunol. 52: 106-118.
9. Girardi, G., D. Yarilin, J. M. Thurman, V. M. Holers, and J. E. Salmon. 2006. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J. Exp. Med. 203: 2165-2175.
10. Ahmed, A., J. Singh, Y. Khan, S. V. Seshan, and G. Girardi. 2010. A new mouse model to explore therapies for preeclampsia. PLoS One 5: e13663.
11. Qing, X., P. B. Redecha, M. A. Burmeister, S. Tomlinson, V. D. D'Agati, R. L. Davisson, and J. E. Salmon. 2011. Targeted inhibition of complement activation prevents features of preeclampsia in mice. Kidney Int. 79: 331-339.
12. Singh, J., A. Ahmed, and G. Girardi. 2011. Role of complement component C1q in the onset of preeclampsia in mice. Hypertension 58: 716-724.
13. Sattin, S., A. Daghetti, M. Thépaut, A. Berzi, M. Sánchez-Navarro, G. Tabarani, J. Rojo, F. Fieschi, M. Clerici, and A. Bernardi. 2010. Inhibition of DC-SIGN-mediated HIV infection by a linear trimannoside mimic in a tetravalent presentation. ACS Chem. Biol. 5: 301-312.
14. Orsini, F., P. Villa, S. Parrella, R. Zangari, E. R. Zanier, R. Gesuete, M. Stravalaci, S. Fumagalli, R. Ottria, J. J. Reina, et al. 2012. Targeting mannose-binding lectin confers long-lasting protection with a surprisingly wide therapeutic window in cerebral ischemia. Circulation 126: 1484-1494.
15. Marzari, R., D. Sblattero, P. Macor, F. Fischetti, R. Gennaro, J. D. Marks, A. Bradbury, and F. Tedesco. 2002. The cleavage site of C5 from man and animals as a common target for neutralizing human monoclonal antibodies: in vitro and in vivo studies. Eur. J. Immunol. 32: 2773-2782.
16. Fischetti, F., P. Durigutto, V. Pellis, A. Debeus, P. Macor, R. Bulla, F. Bossi, F. Ziller, D. Sblattero, P. Meroni, and F. Tedesco. 2005. Thrombus formation induced by antibodies to beta2-glycoprotein I is complement dependent and requires a priming factor. Blood 106: 2340-2346.
17. Agostinis, C., S. Biffi, C. Garrovo, P. Durigutto, A. Lorenzon, A. Bek, R. Bulla, C. Grossi, M. O. Borghi, P. Meroni, and F. Tedesco. 2011. In vivo distribution of b2 glycoprotein I under various pathophysiologic conditions. Blood 118: 4231-4238.
18. Macor, P., P. Durigutto, L. De Maso, C. Garrovo, S. Biffi, A. Cortini, F. Fischetti, D. Sblattero, C. Pitzalis, R. Marzari, and F. Tedesco. 2012. Treatment of experimental arthritis by targeting synovial endothelium with a neutralizing recombinant antibody to C5. Arthritis Rheum. 64: 2559-2567.
19. Durigutto, P., P. Macor, F. Ziller, L. De Maso, F. Fischetti, R. Marzari, D. Sblattero, and F. Tedesco. 2013. Prevention of arthritis by locally synthesized recombinant antibody neutralizing complement component C5. PLoS One 8: e58696.
20. Ferraresso, M., P. Macor, M. Valente, M. Della Barbera, F. D'Amelio, O. Borghi, E. Raschi, P. Durigutto, P. Meroni, and F. Tedesco. 2008. Posttransplant ischemia-reperfusion injury in transplanted heart is prevented by a minibody to the fifth component of complement. Transplantation 86: 1445-1451.
21. Fischetti, F., P. Durigutto, P. Macor, R. Marzari, R. Carretta, and F. Tedesco. 2007. Selective therapeutic control of C5a and the terminal complement complex by anti-C5 single-chain Fv in an experimental model of antigen-induced arthritis in rats. Arthritis Rheum. 56: 1187-1197.
22. Macor, P., E. Secco, N. Mezzaroba, S. Zorzet, P. Durigutto, T. Gaiotto, L. De Maso, S. Biffi, C. Garrovo, S. Capolla, et al. 2015. Bispecific antibodies targeting tumor-associated antigens and neutralizing complement regulators increase the efficacy of antibody-based immunotherapy in mice. Leukemia 29: 406-414.
23. Shi, L., K. Takahashi, J. Dundee, S. Shahroor-Karni, S. Thiel, J. C. Jensenius, F. Gad, M. R. Hamblin, K. N. Sastry, and R. A. Ezekowitz. 2004. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J. Exp. Med. 199: 1379-1390.
24. Chaouat, G., M. Petitbarat, R. Bulla, S. Dubanchet, K. Valdivia, N. Ledée, T. Steffen, J. C. Jensenius, and F. Tedesco. 2009. Early regulators in abortion and implications for a preeclampsia model. J. Reprod. Immunol. 82: 131-140.
25. Chaouat, G., A. Assal Meliani, J. Martal, R. Raghupathy, J. F. Elliott, T. Mosmann, and T. G. Wegmann. 1995. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-tau. J. Immunol. 154: 4261-4268.
26. Agostinis, C., P. Durigutto, D. Sblattero, M. O. Borghi, C. Grossi, F. Guida, R. Bulla, P. Macor, F. Pregnolato, P. L. Meroni, and F. Tedesco. 2014. A non-complement-fixing antibody to b2 glycoprotein I as a novel therapy for anti-phospholipid syndrome. Blood 123: 3478-3487.
27. Gorsuch, W. B., E. Chrysanthou, W. J. Schwaeble, and G. L. Stahl. 2012. The complement system in ischemia-reperfusion injuries. Immunobiology 217: 1026-1033.
28. Orsini, F., D. De Blasio, R. Zangari, E. R. Zanier, and M. G. De Simoni. 2014. Versatility of the complement system in neuroinflammation, neurodegeneration and brain homeostasis. Front. Cell. Neurosci. 8: 380.
29. Bonney, E. A., and S. A. Brown. 2014. To drive or be driven: the path of a mouse model of recurrent pregnancy loss. Reproduction 147: R153-R167.
30. Chaouat, G., N. Rodde, M. Petitbarat, R. Bulla, M. Rahmati, S. Dubanchet, S. Zourbas, I. Bataillon, N. Coqué, B. Hennuy, et al. 2011. An insight into normal and pathological pregnancies using large-scale microarrays: lessons from microarrays. J. Reprod. Immunol. 89: 163-172.
31. Berman, J., G. Girardi, and J. E. Salmon. 2005. TNF-alpha is a critical effector and a target for therapy in antiphospholipid antibody-induced pregnancy loss. J. Immunol. 174: 485-490.
32. Bulla, R., C. Agostinis, F. Bossi, L. Rizzi, A. Debeus, C. Tripodo, O. Radillo, F. De Seta, B. Ghebrehiwet, and F. Tedesco. 2008. Decidual endothelial cells express surface-bound C1q as a molecular bridge between endovascular tro-phoblast and decidual endothelium. Mol. Immunol. 45: 2629-2640.
33. Agostinis, C., R. Bulla, C. Tripodo, A. Gismondi, H. Stabile, F. Bossi, C. Guarnotta, C. Garlanda, F. De Seta, P. Spessotto, et al. 2010. An alternative role of C1q in cell migration and tissue remodeling: contribution to trophoblast invasion and placental development. J. Immunol. 185: 4420-4429.
34. Hansen, S., S. Thiel, A. Willis, U. Holmskov, and J. C. Jensenius. 2000. Purification and characterization of two mannan-binding lectins from mouse serum. J. Immunol. 164: 2610-2618.
35. Ihara, S., A. Takahashi, H. Hatsuse, K. Sumitomo, K. Doi, and M. Kawakami. 1991. Major component of Ra-reactive factor, a complement-activating bactericidal protein, in mouse serum. J. Immunol. 146: 1874-1879.
36. Liu, H., L. Jensen, S. Hansen, S. V. Petersen, K. Takahashi, A. B. Ezekowitz, F. D. Hansen, J. C. Jensenius, and S. Thiel. 2001. Characterization and quantification of mouse mannan-binding lectins (MBL-A and MBL-C) and study of acute phase responses. Scand. J. Immunol. 53: 489-497.
37. de Vries, B., S. J. Walter, C. J. Peutz-Kootstra, T. G. Wolfs, L. W. van Heurn, and W. A. Buurman. 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.
38. Nakamura, A., M. Okigaki, N. Miura, C. Suzuki, N. Ohno, F. Kametani, and K. Hamaoka. 2014. Involvement of mannose-binding lectin in the pathogenesis of Kawasaki disease-like murine vasculitis. Clin. Immunol. 153: 64-72.
39. Wagner, S., N. J. Lynch, W. Walter, W. J. Schwaeble, and M. Loos. 2003. Differential expression of the murine mannose-binding lectins A and C in lymphoid and nonlymphoid organs and tissues. J. Immunol. 170: 1462-1465.
40. van der Pol, P., N. Schlagwein, D. J. van Gijlswijk, S. P. Berger, A. Roos, I. M. Bajema, H. C. de Boer, J. W. de Fijter, G. L. Stahl, M. R. Daha, and C. van Kooten. 2012. Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am. J. Transplant. 12: 877-887.