Increased complement C4d deposition at the maternal-fetal interface in unexplained recurrent miscarriage

Journal of Reproductive Immunology

Volumn 113, Issue , 2016, Pages 54-60

  Meuleman, Tess ^a   Cohen, Danielle ^a   Swings, Godelieve M J S ^a   Veraar, Kimberly ^a   Claas, Frans H J ^a   Bloemenkamp, Kitty W M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

C4d; Classical complement system; Recurrent miscarriage

Indexed keywords

ACETYLSALICYLIC ACID; COMPLEMENT COMPONENT C4D; LOW MOLECULAR WEIGHT HEPARIN; COMPLEMENT COMPONENT C4;

ADULT; ANTICOAGULANT THERAPY; ARTICLE; CASE CONTROL STUDY; CLINICAL ARTICLE; COMPLEMENT DEPOSITION; CONCEPTION; CONTROLLED STUDY; ELECTIVE SURGERY; FEMALE; FETUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INDUCED ABORTION; MOTHER FETUS RELATIONSHIP; PREGNANCY; PRIORITY JOURNAL; PROPHYLAXIS; RECURRENT ABORTION; SPONTANEOUS ABORTION; TROPHOBLAST; IMMUNOLOGY; METABOLISM; PATHOLOGY; PLACENTA; RANDOMIZED CONTROLLED TRIAL;

ABORTION, HABITUAL; CASE-CONTROL STUDIES; COMPLEMENT C4; FEMALE; HUMANS; PLACENTA; PREGNANCY;

EID: 84960407612     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2015.12.001     Document Type: Article

References (41)

1. Branch D.W., Gibson M., Silver R.M. Clinical practice. Recurrent miscarriage. N. Engl. J. Med. 2010, 363:1740-1747.
2. Bulla R., et al. Complement production by trophoblast cells at the feto-maternal interface. J. Reprod. Immunol. 2009, 82:119-125.
3. Buurma A., et al. Preeclampsia is characterized by placental complement dysregulation. Hypertension 2012, 60:1332-1337.
4. Chan Y.Y., Jayaprakasan K., Tan A., Thornton J.G., Coomarasamy A., Raine-Fenning N.J. Reproductive outcomes in women with congenital uterine anomalies: a systematic review. Ultrasound Obstet. Gynecol. 2011, 38:371-382.
5. Chan Y.Y., Jayaprakasan K., Zamora J., Thornton J.G., Raine-Fenning N., Coomarasamy A. The prevalence of congenital uterine anomalies in unselected and high-risk populations: a systematic review. Hum. Reprod. Update 2011, 17:761-771.
6. Cohen D., et al. Classical complement activation as a footprint for murine and human antiphospholipid antibody-induced fetal loss. J. Pathol. 2011, 225:502-511.
7. Cohen D., et al. Pros and cons for C4d as a biomarker. Kidney Int. 2012, 81:628-639.
8. Collins A.B., et al. Complement activation in acute humoral renal allograft rejection: diagnostic significance of C4d deposits in peritubular capillaries. J. Am. Soc. Nephrol. 1999, 10:2208-2214.
9. Colvin R.B. Dimensions of antibody-mediated rejection. Am. J. Transplant. 2010, 10:1509-1510.
10. Conway E.M. Thrombomodulin and its role in inflammation. Semin. Immunopathol. 2012, 34:107-125.
11. Coulam C.B. Epidemiology of recurrent spontaneous abortion. Am. J. Reprod. Immunol. 1991, 26:23-27.
12. Federation of Medical Scientific Societies, 2014.
13. Gelber S.E., et al. Prevention of defective placentation and pregnancy loss by blocking innate immune pathways in a syngeneic model of placental insufficiency. J. Immunol. 2015, 195:1129-1138.
14. Giannakopoulos B., Passam F., Ioannou Y., Krilis S.A. How we diagnose the antiphospholipid syndrome. Blood 2009, 113:985-994.
15. Girardi G., Redecha P., Salmon J.E. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat. Med. 2004, 10:1222-1226.
16. Grennan D.M., McCormick J.N., Wojtacha D., Carty M., Behan W. Immunological studies of the placenta in systemic lupus erythematosus. Ann. Rheum. Dis. 1978, 37:129-134.
17. Guleria I., Sayegh M.H. Maternal acceptance of the fetus: true human tolerance. J. Immunol. 2007, 178:3345-3351.
18. Heuser C.C., Eller A.G., Warren J., Branch D.W., Salmon J., Silver R.M. A case-control study of membrane cofactor protein mutations in two populations of patients with early pregnancy loss. J. Reprod. Immunol. 2011, 91:71-75.
19. Hodes-Wertz B., et al. Idiopathic recurrent miscarriage is caused mostly by aneuploid embryos. Fertil. Steril. 2012, 98:675-680.
20. Johnson P.M., Natvig J.B., Ystehede U.A., Faulk W.P. Immunological studies of human placentae: the distribution and character of immunoglobulins in chorionic villi. Clin. Exp. Immunol. 1977, 30:145-153.
21. Kloosterman G.J. Intrauterine growth and intrauterine growth curves. Maandschr Kindergeneeskd 1969, 37:209-225.
22. Larsen E.C., Christiansen O.B., Kolte A.M., Macklon N. New insights into mechanisms behind miscarriage. BMC. Med. 2013, 11:154.
23. Lashley E.E., Meuleman T., Claas F.H. Beneficial or harmful effect of antipaternal human leukocyte antibodies on pregnancy outcome? A systematic review and meta-analysis. Am. J. Reprod. Immunol. 2013, 70:87-103.
24. Lee J., et al. A signature of maternal anti-fetal rejection in spontaneous preterm birth: chronic chorioamnionitis, anti-human leukocyte antigen antibodies, and c4d. PLoS One 2011, 6:e16806.
25. Lee J.Y., et al. Placental C4d as a common feature of chromosomally normal and abnormal miscarriages. Virchows Arch. 2014, 464:613.
26. Loupy A., et al. Complement-binding anti-HLA antibodies and kidney-allograft survival. N. Engl. J. Med. 2013, 369:1215-1226.
27. Macklon N.S., Brosens J.J. The human endometrium as a sensor of embryo quality. Biol. Reprod. 2014, 91:98.
28. McNamee K., Dawood F., Farquharson R. Recurrent miscarriage and thrombophilia: an update. Curr. Opin. Obstet. Gynecol. 2012, 24:229-234.
29. Medawar P. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 1953, 44:320-338.
30. Mosnier L.O., Zlokovic B.V., Griffin J.H. The cytoprotective protein C pathway. Blood 2007, 109:3161-3172.
31. Nauta A.J., et al. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur. J. Immunol. 2002, 32:1726-1736.
32. Rai R., Regan L. Recurrent miscarriage. Lancet 2006, 368:601-611.
33. Redecha P., van R.N., Torry D., Girardi G. Pravastatin prevents miscarriages in mice: role of tissue factor in placental and fetal injury. Blood 2009, 113:4101-4109.
34. Regan L., Braude P.R., Hill D.P. A prospective study of the incidence: time of appearance and significance of anti-paternal lymphocytotoxic antibodies in human pregnancy. Hum. Reprod. 1991, 6:294-298.
35. Salmon J.E., et al. Mutations in complement regulatory proteins predispose to preeclampsia: a genetic analysis of the PROMISSE cohort. PLoS Med. 2011, 8:e1001013.
36. Serrano F., Lima M.L. Recurrent miscarriage: psychological and relational consequences for couples. Psychol. Psychother. 2006, 79:585-594.
37. Shamonki J.M., Salmon J.E., Hyjek E., Baergen R.N. Excessive complement activation is associated with placental injury in patients with antiphospholipid antibodies. Am. J. Obstet. Gynecol. 2007, 196:167-175.
38. Solez K., et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am. J. Transplant. 2008, 8:753-760.
39. Tranquilli A.L., Brown M.A., Zeeman G.G., Dekker G., Sibai B.M. The definition of severe and early-onset preeclampsia. Statements from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Pregancy Hypertens. 2012, 3:44-47.
40. van Kampen C.A., Versteeg-van der Voort Maarschalk M.F., Langerak-Langerak J., van Beelen E., Roelen D.L., Claas F.H. Pregnancy can induce long-persisting primed CTLs specific for inherited paternal HLA antigens. Hum. Immunol. 2001, 62:201-207.
41. Visser J., et al. Thromboprophylaxis for recurrent miscarriage in women with or without thrombophilia. HABENOX: a randomised multicentre trial. Thromb. Haemost. 2011, 105:295-301.