Pregnancy and multiple sclerosis: Feto-maternal immune cross talk and its implications for disease activity

Journal of Reproductive Immunology

Volumn 97, Issue 1, 2013, Pages 140-146

  Patas, Konstantinos ^a   Engler, Jan Broder ^a   Friese, Manuel A ^a   Gold, Stefan M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Autoimmunity; Immune tolerance; Multiple sclerosis; Pregnancy; Regulatory T cells

Indexed keywords

AUTOANTIGEN; FETAL ANTIGEN;

ARTICLE; DISEASE ACTIVITY; FETOPLACENTAL UNIT; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; MULTIPLE SCLEROSIS; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

AUTOIMMUNITY; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNITY, MATERNALLY-ACQUIRED; IMMUNOMODULATION; MULTIPLE SCLEROSIS; PLACENTAL CIRCULATION; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 84874509735     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.10.005     Document Type: Article

References (70)

1. Airas L., et al. Immunoregulatory factors in multiple sclerosis patients during and after pregnancy: relevance of natural killer cells. Clin. Exp. Immunol. 2008, 151:235-243.
2. Al-Shammri S., et al. Th1/Th2 cytokine patterns and clinical profiles during and after pregnancy in women with multiple sclerosis. J. Neurol. Sci. 2004, 222:21-27.
3. Aluvihare V.R., et al. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5:266-271.
4. Bielekova B., et al. Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5941-5946.
5. Bilate A.M., Lafaille J.J. Induced CD4+Foxp3+ regulatory T cells in immune tolerance. Annu. Rev. Immunol. 2012, 30:733-758.
6. Blois S.M., et al. Dendritic cells: key to fetal tolerance?. Biol. Reprod. 2007, 77:590-598.
7. Burton G.J., et al. Regulation of vascular growth and function in the human placenta. Reproduction 2009, 138:895-902.
8. Chan J., et al. Glucocorticoid-induced apoptosis in human decidua: a novel role for 11beta-hydroxysteroid dehydrogenase in late gestation. J. Endocrinol. 2007, 195:7-15.
9. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy?. Semin. Immunopathol. 2007, 29:95-113.
10. Compston A., Coles A. Multiple sclerosis. Lancet 2008, 372:1502-1517.
11. Confavreux C., et al. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in multiple sclerosis group. N. Engl. J. Med. 1998, 339:285-291. (see comments).
12. Daniel C., Von Boehmer H. Extra-thymically induced regulatory T cells: do they have potential in disease prevention?. Semin. Immunol. 2011, 23:410-417.
13. low cells. Brain 2008, 131:1701-1711.
14. Erlebacher A., et al. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 2007, 117:1399-1411.
15. Ernerudh J., et al. Regulatory T helper cells in pregnancy and their roles in systemic versus local immune tolerance. Am. J. Reprod. Immunol. 2011, 66(Suppl. 1):31-43.
16. Fallon P.G., et al. IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 2002, 17:7-17.
17. Finkelsztejn A., et al. What can we really tell women with multiple sclerosis regarding pregnancy? A systematic review and meta-analysis of the literature. BJOG 2011, 118:790-797.
18. Franssen R.A., et al. Reproductive experience facilitates recovery from kainic acid-induced neural insult in female long-Evans rats. Brain Res. 2012, 1454:80-89.
19. Gatson N.N., et al. Induction of pregnancy during established EAE halts progression of CNS autoimmune injury via pregnancy-specific serum factors. J. Neuroimmunol. 2011, 230:105-113.
20. Gilli F., et al. Learning from nature: pregnancy changes the expression of inflammation-related genes in patients with multiple sclerosis. PLoS ONE 2010, 5:e8962.
21. Gilmore W., et al. Preliminary studies of cytokine secretion patterns associated with pregnancy in MS patients. J. Neurol. Sci. 2004, 224:69-76.
22. Gold S.M., Voskuhl R.R. Estrogen treatment in multiple sclerosis. J. Neurol. Sci. 2009, 286(1-2):99-103.
23. Gold S.M., et al. Dynamic development of glucocorticoid resistance during autoimmune neuroinflammation. J. Clin. Endocrinol. Metab. 2012, 97:E1402-E1410.
24. Gregg C., et al. White matter plasticity and enhanced remyelination in the maternal CNS. J. Neurosci. 2007, 27:1812-1823.
25. Haribhai D., et al. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 2011, 35:109-122.
26. Iorio R., et al. T-bet, pSTAT1 and pSTAT3 expression in peripheral blood mononuclear cells during pregnancy correlates with post-partum activation of multiple sclerosis. Clin. Immunol. 2009, 131:70-83.
27. Kahn D.A., Baltimore D. Pregnancy induces a fetal antigen-specific maternal T regulatory cell response that contributes to tolerance. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9299-9304.
28. Karimi K., Arck P.C. Natural killer cells: keepers of pregnancy in the turnstile of the environment. Brain Behav. Immun. 2010, 24:339-347.
29. Khosrotehrani K., Bianchi D.W. Multi-lineage potential of fetal cells in maternal tissue: a legacy in reverse. J. Cell Sci. 2005, 118:1559-1563.
30. Kinsley C.H., Amory-Meyer E. Why the maternal brain?. J. Neuroendocrinol. 2011, 23:974-983.
31. Kipp M., Beyer C. Impact of sex steroids on neuroinflammatory processes and experimental multiple sclerosis. Front. Neuroendocrinol. 2009, 30:188-200.
32. Kretschmer K., et al. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 2005, 6:1219-1227.
33. Langer-Gould A., et al. Late pregnancy suppresses relapses in experimental autoimmune encephalomyelitis: evidence for a suppressive pregnancy-related serum factor. J. Immunol. 2002, 169:1084-1091.
34. Leber A., et al. Regulatory T cells and their role in pregnancy. Am. J. Reprod. Immunol. 2010, 63:445-459.
35. Lopez C., et al. Variations in chemokine receptor and cytokine expression during pregnancy in multiple sclerosis patients. Mult. Scler. 2006, 12:421-427.
36. McClain M.A., et al. Pregnancy suppresses experimental autoimmune encephalomyelitis through immunoregulatory cytokine production. J. Immunol. 2007, 179:8146-8152.
37. Mjosberg J., et al. CD4+CD25+ regulatory T cells in human pregnancy: development of a Treg-MLC-ELISPOT suppression assay and indications of paternal specific Tregs. Immunology 2007, 120:456-466.
38. highFoxp3+Tregs in human second trimester pregnancy is induced by progesterone and 17beta-estradiol. J. Immunol. 2009, 183:759-769.
39. Mjosberg J., et al. Foxp3+ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol. Reprod. 2010, 82:698-705.
40. Moldenhauer L.M., et al. Cross-presentation of male seminal fluid antigens elicits T cell activation to initiate the female immune response to pregnancy. J. Immunol. 2009, 182:8080-8093.
41. Mor G., et al. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann. N.Y. Acad. Sci. 2011, 1221:80-87.
42. Munoz-Suano A., et al. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 2011, 241:20-38.
43. Munoz-Suano A., et al. Regulatory T cells protect from autoimmune arthritis during pregnancy. J. Autoimmun. 2012, 38:J103-J108.
44. Neuteboom R.F., et al. Pregnancy-induced fluctuations in functional T-cell subsets in multiple sclerosis patients. Mult. Scler. 2010, 16:1073-1078.
45. Petroff M.G. Review: Fetal antigens - identity, origins, and influences on the maternal immune system. Placenta 2011, 32(Suppl. 2):S176-S181.
46. bright natural killer (NK) cells: an important NK cell subset. Immunology 2009, 126:458-465.
47. Ponsonby A.L., et al. Offspring number, pregnancy, and risk of a first clinical demyelinating event: the AusImmune Study. Neurology 2012, 78:867-874.
48. Redman C.W., et al. Review: Does size matter? Placental debris and the pathophysiology of pre-eclampsia. Placenta 2012, 33(Suppl.):S48-S54.
49. Robinson D.P., Klein S.L. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm. Behav. 2012, 62:263-271.
50. Rowe J.H., et al. Foxp3(+) regulatory T cell expansion required for sustaining pregnancy compromises host defense against prenatal bacterial pathogens. Cell Host Microbe 2011, 10:54-64.
51. Rowe J.H., et al. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 2012, 490:102-106.
52. Samstein R.M., et al. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012, 150:29-38.
53. Sanchez-Ramon S., et al. Pregnancy-induced expansion of regulatory T-lymphocytes may mediate protection to multiple sclerosis activity. Immunol. Lett. 2005, 96:195-201.
54. bright natural killer cells in the peripheral blood of multiple sclerosis patients treated with interferon-beta. Neurol. Sci. 2007, 28:121-126.
55. Sargent I.L., et al. NK cells and human pregnancy - an inflammatory view. Trends Immunol. 2006, 27:399-404.
56. Sasaki Y., et al. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 2004, 10:347-353.
57. Shima T., et al. Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J. Reprod. Immunol. 2010, 85:121-129.
58. Sicotte N.L., et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann. Neurol. 2002, 52:421-428.
59. Somerset D.A., et al. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+CD4+ regulatory T-cell subset. Immunology 2004, 112:38-43.
60. Taglauer E.S., et al. The hidden maternal-fetal interface: events involving the lymphoid organs in maternal-fetal tolerance. Int. J. Dev. Biol. 2010, 54:421-430.
61. Thuere C., et al. Kinetics of regulatory T cells during murine pregnancy. Am. J. Reprod. Immunol. 2007, 58:514-523.
62. bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J. Immunol. 2008, 180:5737-5745.
63. Trowsdale J., Betz A.G. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat. Immunol. 2006, 7:241-246.
64. Voskuhl R.R., Gold S.M. Sex-related factors in multiple sclerosis susceptibility and progression. Nat. Rev. Neurol. 2012, 8:255-263.
65. Waites G.T., Whyte A. Effect of pregnancy on collagen-induced arthritis in mice. Clin. Exp. Immunol. 1987, 67:467-476.
66. Wing K., Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 2010, 11:7-13.
67. Zenclussen M.L., et al. The persistence of paternal antigens in the maternal body is involved in regulatory T-cell expansion and fetal-maternal tolerance in murine pregnancy. Am. J. Reprod. Immunol. 2010, 63:200-208.
68. Zeng X.X., et al. Pregnancy-associated progenitor cells differentiate and mature into neurons in the maternal brain. Stem Cells Dev. 2010, 19:1819-1830.
69. Zhao J.X., et al. Fetal alloantigen is responsible for the expansion of the CD4(+)CD25(+) regulatory T cell pool during pregnancy. J. Reprod. Immunol. 2007, 75:71-81.
70. Zheng Y., et al. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010, 463:808-812.