Popular myths in reproductive immunology

Journal of Reproductive Immunology

Volumn 104-105, Issue C, 2014, Pages 54-62

  Clark, David A ^a,b,c  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Angiogenesis; Complement; Evidence based medicine; Maternofetal tolerance; Regulatory T cells; Uterine NK cells

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ANGIOGENESIS; ANTIGEN PRESENTING CELL; CD8+ T LYMPHOCYTE; COMPLEMENT ACTIVATION; DRUG IMPURITY; HUMAN; IMMUNOLOGY; INTRAUTERINE GROWTH RETARDATION; NATURAL KILLER CELL; NONHUMAN; PRACTICE GUIDELINE; PREGNANCY DISORDER; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REPRODUCTION; REVIEW; SUPPRESSOR CELL; TROPHOBLAST; ANIMAL; FEMALE; MALE; PATHOLOGY; PREECLAMPSIA; PREGNANCY; RECURRENT ABORTION;

ABORTION, HABITUAL; ANIMALS; FEMALE; FETAL GROWTH RETARDATION; HUMANS; MALE; PRE-ECLAMPSIA; PREGNANCY; REPRODUCTION;

EID: 84929994236     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2014.06.002     Document Type: Review

References (72)

1. Abe Y., Urakami H., Ostanin D., Zibari G., Hayashode T., Kitagawa Y. Induction of Foxp3-expressing regulatory T-cells by donor blood transfusion is required for tolerance to rat liver allografts. PLoS ONE 2009, 4:e7840.
2. Barber E.M., Pollard J.W. Uterine NK population requires IL-15 but these cells are not required for pregnancy or the resolution of Listeria monocytogenes infection. J. Immunol. 2003, 171:37-46.
3. Bazrgar M., Gourabi H., Valojerdi M.R., Yazdi P.E., Baharvand H. Self-correction of chromosomal abnormalities in human preimplantation embryos and embryonic stem cells. Stem Cells Dev. 2013, 22:2449-2456.
4. Burton G.J., Jauniaux E., Watson A.L. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: The Boyd Collection revisited. Am. J. Obstet. Gynecol. 1999, 181:718-724.
5. Chen T., Darrasse-Jeze G., Bergot A.-S., Courau T., Churland G., Valdivia K., et al. Self-specific memory regulatory T cells protect embryos at implantation in mice. J. Immunol. 2013, 191:2273-2281.
6. Clark D.A. Controversies in reproductive immunology. Crit. Rev. Immunol. 1991, 11:215-247.
7. Clark D.A. Does immunological intercourse prevent pre-eclampsia?. Lancet 1994, 344:969-970.
8. Clark D.A. Is there any evidence for immunologically-mediated or immunologically-modifiable early pregnancy failure?. J. Assist. Reprod. Genet. 2003, 20:63-72.
9. Clark D.A. Immunological factors in pregnancy wastage: fact or fiction. Am. J. Reprod. Immunol. 2008, 59:277-300.
10. Clark D.A. Cell-surface CD200 may predict efficacy of paternal mononuclear leukocyte immunotherapy in treatment of human recurrent pregnancy loss. Am. J. Reprod. Immunol. 2009, 61:75-84.
11. Clark D.A. Anti-TNF-α therapy in immune-mediated subfertility: state of the art. J. Reprod. Immunol. 2010, 85:15-24.
12. Clark D.A. The power of observation. Am. J. Reprod. Immunol. 2011, 66:71-75. 66:182.
13. Clark D.A. The end of evidence-based medicine. Inflammopharmacology 2012, 20:187-193.
14. Clark D.A. The use and misuse of animal models of human pregnancy disorders. J. Reprod. Immunol. 2014, 103:1-8.
15. Clark D.A., Chaouat G. Regulatory T cells and reproduction: how do they do it?. J. Reprod. Immunol. 2012, 96:1-7.
16. Clark D.A., Lea R.G., Podor T., Daya S., Banwatt D., Harley C. Cytokines determining the success or failure of pregnancy. Ann. NY Acad. Sci. 1991, 626:524-536.
17. Clark D.A., Gunby J., Daya S. The use of allogeneic leukocytes or IV IgG for the treatment of patients with recurrent spontaneous abortions. Transfus. Med. Rev. 1997, 11:85-94.
18. Clark D.A., Ding J.W., Yu G., Levy G.A., Gorczynski R.M. Fgl2 prothrombinase expression in mouse trophoblast and deciduas triggers abortion but may be countered by OX-2. Mol. Human Reprod. 2001, 7:185-194.
19. Clark D.A., Coulam C.B., Daya S., Chaouat G. Unexplained sporadic and recurrent miscarriage in the new millennium: a critical analysis of immune mechanisms and treatments. Human Reprod. Update 2001, 7:501-511.
20. Clark D.A., Manuel J., Lee L., Chaouat G., Gorczynski R.M., Levy G.A. Ecology of danger-dependent cytokine-boosted spontaneous in the CBA x DBA/2 mouse model. I. Synergistic effect of LPS and (TNF-α + IFN-γ) on pregnancy loss. Am. J. Reprod. Immunol. 2004, 52:370-387.
21. Clark D.A., Blois S., Kandil J., Handjiski B., Manuel J., Arck P.C. Reduced uterine indoleamine 2,3-dioygenase versus increased Th1/Th2 cytokine ratio as a basis for occult and clinical pregnancy failure in mice and humans. Am. J. Reprod. Immunol. 2005, 54:203-216.
22. Clark D.A., Chaouat G., Banwatt D., Friebe A., Arck P.C. Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA x DBA/2 mouse model. II. Fecal LPS levels in colonies with different basal abortion rates. Am. J. Reprod. Immunol. 2008, 60:529-533.
23. Clark D.A., Rahmati M., Bensussan A., Markert U.R., Chaouat G. Seminal plasma peptides may determine maternal immune response that alters success or failure of pregnancy in the abortion-prone CBAxDBA/2 model. J. Reprod. Immunol. 2013, 99:46-53.
24. Craven C.M., Ward K. Transfusion of fetal cord blood cells: an improved method of hematopoietic stem cell transplantation?. J. Reprod. Immunol. 1999, 42:59-77.
25. Croy B.A., Chen Z., Hofmann A.P., Lord E.M., Sedlacek A.L., Gerber S.A. Imaging of vascular development in early mouse decidua and its association with leukocytes and trophoblasts. Biol. Reprod. 2012, 87:1-11.
26. bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J. Immunol. 2004, 173:6418-6426.
27. Demir R., Yabs A., Huppert B. Vasculogenesis and angiogenesis in the endometrium during the menstrual cycle and implantation. Acta Histochem. 2010, 112:203-214.
28. Erlebacher A., Vencato D., Price K.A., Zhang D., Glimcher L.H. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 2007, 117:1399-1411.
29. Ferry B.L., Sargent I.L., Starkey P.M., Redman C.W.G. Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from human early pregnancy deciduas. Cell. Immunol. 1991, 132:140-149.
30. Fragouli E., Escalona A., Gutierrez-Mateo C., Tormasi S., Alfarawati S., Sepulveda S., et al. Comparative genomic hybridization of oocytes and first polar bodies from young donors. Reprod. Biomed. 2009, 19:228-237. (online).
31. Girardi G., Yarilin D., Thurman J.M., Holers V.M., Salmon J.E. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J. Exp. Med. 2006, 203. 2165-217-282.
32. + cell pool and CCL19-mediated recruitment. Biol. Reprod. 2011, 85:397-408.
33. Guimond M.J., Wang B., Croy B.A. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits of natural killer cell-deficient epsilon 26 mice. J. Exp. Med. 1998, 187:217-223.
34. Hernandez-Diaz S., Toh S., Cnattingius S. Risk of pre-eclampsia in first and subsequent pregnancies: prospective cohort study. BMJ 2009, 338:b2255.
35. Hunkapiller N.M., Gasperowicz M., Kapidzic M., Plaks V., Maltepe E., Kitajewski J., et al. A role for Notch signaling in trophoblast endovascular invasion and the pathogenesis of pre-eclampsia. Development 2011, 138:2987-2998.
36. Kahn D.A., Baltimore D. Pregnancy induces a fetal antigen-specific maternal T regulatory cell response that contributes to tolerance. Proc. Natl. Acad. Sci. 2010, 107:9299-9304.
37. Krishnan L., Guilbert L.J., Wegmann T.G., Belosevic M., Mosmann T.R. T helper 1 response against Leishmania major in pregnant C56BL/6 mice increases implantation failure and fetal resorption. Correlation with increased IFN-γ and reduced IL-10 production by placental cells. J. Immunol. 1996, 156:652-662.
38. Krishnan L., Guilbert L.J., Russell A.S., Wegmann T.G., Mosmann T.R., Belosevic M. Pregnancy impairs resistance of C57BL/6 mice to Leishmania major and causes decreased antigen-specific IFN-γ response and increased production of T helper 2 cytokines. J. Immunol. 1996, 156:644-652.
39. Klauber N., Rohan R.M., Flynn E., D'Amato R.J. Critical components of the female reproductive pathway are suppressed by the angiogenesis inhibitor AGM-1470. Nat. Med. 1997, 3:433-436.
40. Le Bouteiller P. Decidual NK cell effector function in normal and virus-infected pregnancy. J. Reprod. Immunol. 2014, 101-102:7.
41. + Cytotoxic T cell responses during normal pregnancy exhibit broad functional capacity. J. Immunol. 2012, 189:1072-1080.
42. Liu J., Wang W., Sun X., Liu L., Li M., Witz C., et al. DNA microarray reveals that a high proportion of human blastocysts from women of advanced maternal age are aneuploid and mosaic. Biol. Reprod. 2012, 87:148.
43. Martin G.H., Gregoire S., Landau D.A., Pilon C., Grinberg-Bleyer Y., Mege C.F., et al. In vitro activation of transferred regulatory T cells specific for third-party exogenous antigen controls GVH disease in mice. Eur. J. Immunol. 2013, 43:2263-2272.
44. Mold J.E., Michaelsson J., Burt T.D., Muench M.O., Beckerman K.P., Busch M.P., et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 1988, 322:1562-1565.
45. Mowbray J.F., Underwood J.L. Effect of paternal lymphocyte immunization on birthweight and pregnancy outcome. Cellular and Molecular Biology of the Materno-Fetal Relationship. INSERM Colloques 1991, vol. 212:295-302. John Libby Eurotext.
46. Munne S., Ary J., Zouves C., Escudero T., Barnes F., Cinioglu C., et al. Wide range of chromosome abnormalities in the embryos of young egg donors. Reprod. Biomed. 2006, 12:340-346. (online).
47. Nardo L.G. Vascular endothelial growth factor expression in the endometrium during the menstrual cycle, implantation window and early pregnancy. Curr. Opin. Obstet. Gynecol. 2005, 17:419-423.
48. Plaks V., Birnberg T., Sola S., Ben Yashar A., Kalchenko V., Mor G., et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008, 118:3954-3965.
49. Pollard J.W. Uterine DCs are essential for pregnancy. J. Clin. Invest. 2008, 116:3832-3835.
50. Rajalingam R., Krausa P., Shilling H.G., Stein J.B., Balamurugan A., McGinnis M.D., et al. Distinctive KIR and HLA diversity in a panel of north Indian Hindus. Immunogenetics 2002, 53:1009-1019.
51. Redecha P., van Rooijen N., Torry D., Girardi G. Pravastatin prevents miscarriages in mice: role of tissue factor in placental and fetal injury. Blood 2009, 113:4101-4109.
52. Red-Horse K., Zhou Y., Genbacev O., Prakobphol A., Foulk R., McMaster M., et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Invest. 2004, 114:744-754.
53. Regan L. A prospective study of spontaneous abortion. Early Pregnancy Loss; Mechanisms and Treatment. Royal College of Obstetricians and Gynaecologists 1988, 23-37. Peacock Press, Ashton-under-Lyne, UK. R.W. Beard, F. Sharp (Eds.).
54. Regan L., Braude P., Trembath P.L. Influence of past reproductive performance on risk of spontaneous abortion. BMJ 1989, 299:541-545. (correction 399, 1082).
55. RMITG (Recurrent Miscarriage Immunotherapy Trialists Group) Worldwide collaborative observational study and meta-analysis on allogenic leukocyte immunotherapy for recurrent spontaneous abortion. Am. J. Reprod. Immunol. 1994, 32:55-72.
56. + T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol. Reprod. 2009, 80:1036-1045.
57. Romo A., Carceller R., Tobajas J. Intrauterine growth retardation (IUGR): epidemiology and etiology. Pediatr. Endocrinol. Rev. 2009, (Suppl. 3):332-336.
58. Rowe J.H., Ertelt J.M., Xin L., Way S.S. Pregnancy imprints regulatory memory that sustains anergy to fetal antigens. Nature 2012, 490:102-106.
59. Rutland C.S., Mukhopadhyay M., Underwood S., Clyde N., Mayhew T.M., Mitchell C.A. Induction of intrauterine growth restriction by reducing placental vascular growth. Biol. Reprod. 2005, 73:1164-1175.
60. Saito S., Takeda Y., Sakai M., Nakabayahi M., Hayakawa S. The incidence of pre-eclampsia among couples consisting of Japanese women and Caucasian med. J. Reprod. Immunol. 2006, 70:93-98.
61. Samstein R.M., Josefowicz S.Z., Avery A., Treuting P.M., Rudensky A.Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012, 159:29-38.
62. Santos M.A., Teklenburg G., Macklon N.S., Van Opstal D., Schuring-Blom G.H., Krijtenburg P.J., et al. The fate of the mosaic embryo chromosomal constitution and development of day 4, 5 and 8 human embryos. Human Reprod. 2010, 25:1816-1926.
63. Stern M., Ruggert L., Mancusi A., Bernardo M.E., de Angelis C., Bucher C., et al. Survival after T cell-depleted haploidentical stem cell transplantation is improved using the mother as donor. Blood 2008, 112:2990-2995.
64. Tafuri A., Alferink J., Moller P., Hammerling G.J., Arnold B. T cell awareness of paternal alloantigens during pregnancy. Science 1995, 270:630-633.
65. Tilburgs T., Strominger J.L. CD8+ effector T cells at the fetal-maternal interface, balancing fetal tolerance and antiviral immunity. Am. J. Reprod. Immunol. 2013, 69:395-407.
66. Verlinsky Y., Kuliev A. Clinical application of polar body biopsy. Textbook of Assisted Reproductive Technologies 2004, 371-379. Informa Healthcare, London, UK. D.K. Gardner, A. Weissman, C.M. Howles, Z. Shoham (Eds.).
67. Wegmann T.G., Waters C.A., Drell D.W., Carlson G.A. Pregnant mice are not primed but can be primed to fetal alloantigens. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:2410-2414.
68. Wick M., Dubey P., Koeppen H., Siegel C.T., Fields P.E., Chen L., et al. Antigenic cancer cells grow progressively in immune hosts without evidence for T cell exhaustion or systemic anergy. J. Exp. Med. 1997, 186:229-238.
69. Woodruff M.F.A. Transplantation immunity and the immunological problem of pregnancy. Proc. Royal Soc. London Ser. B 1958, 148:68-75.
70. Xiong S., Sharkey A.M., Kennedy P.R., Gardner L., Farrell L.E., Chazara O., et al. Maternal NK cell-activating receptor K1R2DS1 enhances placentation. J. Clin. Invest. 2013, 123:4264-4272.
71. Xu C., Mao D., Holers V.M., Palanca B., Cheng A.M., Molina H. A critical role for murine complement regulator crry in fetomaternal tolerance. Science 2000, 287:498-501.
72. Yu G., Sun Y., Foerster K., Manuel J., Molina H., Levy G.A., Gorczynski R.M., Clark D.A. LPS-induced murine abortions require C5 but not C3, and are prevented by upregulating expression of the CD200 tolerance signaling molecule. Am. J. Reprod. Immunol. 2008, 60:135-140.