Th17 and Regulatory T cells in Women with Recurrent Pregnancy Loss

American Journal of Reproductive Immunology

Volumn 67, Issue 4, 2012, Pages 311-318

  Lee, Sung Ki ^a   Kim, Jee Yun ^a   Lee, Millina ^a   Gilman Sachs, Alice ^a   Kwak Kim, Joanne ^b  

^a Konyang University   (South Korea)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Foxp3; IL 17; Infertility; Recurrent pregnancy loss; Regulatory T cells; Th17

Indexed keywords

CHEMOKINE RECEPTOR CCR5; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 23; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANTIGEN EXPRESSION; CD3+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DOWN REGULATION; EFFECTOR CELL; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFERTILITY; LYMPHOCYTE DIFFERENTIATION; MENSTRUAL CYCLE; PREGNANCY; PREGNANCY RATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENT ABORTION; REGULATORY T LYMPHOCYTE; REVIEW; TH17 CELL; THYMUS;

ABORTION, HABITUAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFERTILITY, FEMALE; PREGNANCY; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84862828630     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2012.01116.x     Document Type: Review

References (73)

1. Witkin SS, Linhares IM, Bongiovanni AM, Herway C, Skupski D: Unique alterations in infection-induced immune activation during pregnancy. BJOG 2011; 118:145-153.
2. Hogge WA, Byrnes AL, Lanasa MC, Surti U: The clinical use of karyotyping spontaneous abortions. Am J Obstet Gynecol 2003; 189:397-400; discussion 400-392.
3. Wilcox AJ, Weinberg CR, O'Connor JF, Baird DD, Schlatterer JP, Canfield RE, Armstrong EG, Nisula BC: Incidence of early loss of pregnancy. N Engl J Med 1988; 319:189-194.
4. Christiansen OB, Nielsen HS, Kolte AM: Future directions of failed implantation and recurrent miscarriage research. Reprod Biomed Online 2006; 13:71-83.
5. Kwak JY, Beaman KD, Gilman-Sachs A, Ruiz JE, Schewitz D, Beer AE: Up-regulated expression of CD56+, CD56+/CD16+, and CD19+ cells in peripheral blood lymphocytes in pregnant women with recurrent pregnancy losses. Am J Reprod Immunol 1995; 34:93-99.
6. Aoki K, Kajiura S, Matsumoto Y, Ogasawara M, Okada S, Yagami Y, Gleicher N: Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet 1995; 345:1340-1342.
7. Dosiou C, Giudice LC: Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 2005; 26:44-62.
8. Kwak-Kim JY, Chung-Bang HS, Ng SC, Ntrivalas EI, Mangubat CP, Beaman KD, Beer AE, Gilman-Sachs A: Increased T helper 1 cytokine responses by circulating T cells are present in women with recurrent pregnancy losses and in infertile women with multiple implantation failures after IVF. Hum Reprod 2003; 18:767-773.
9. Lee SK, Kim JY, Hur SE, Kim CJ, Na BJ, Lee M, Gilman-Sachs A, Kwak-Kim J: An imbalance in interleukin-17-producing T and Foxp3+ regulatory T cells in women with idiopathic recurrent pregnancy loss. Hum Reprod 2011; 26:2964-2971.
10. Hill JA, Polgar K, Anderson DJ: T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. JAMA 1995; 273:1933-1936.
11. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M: Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155:1151-1164.
12. Wing K, Sakaguchi S: Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010; 11:7-13.
13. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT: Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-1132.
14. Laurence A, O'Shea JJ: T(H)-17 differentiation: of mice and men. Nat Immunol 2007; 8:903-905.
15. Gershon RK, Kondo K: Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970; 18:723-737.
16. Gershon RK, Cohen P, Hencin R, Liebhaber SA: Suppressor T cells. J Immunol 1972; 108:586-590.
17. Hori S, Nomura T, Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061.
18. Roncador G, Brown PJ, Maestre L, Hue S, Martinez-Torrecuadrada JL, Ling KL, Pratap S, Toms C, Fox BC, Cerundolo V, Powrie F, Banham AH: Analysis of FOXP3 protein expression in human CD4+CD25+ regulatory T cells at the single-cell level. Eur J Immunol 2005; 35:1681-1691.
19. Sakaguchi S, Miyara M, Costantino CM, Hafler DA: FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10:490-500.
20. Powell BR, Buist NR, Stenzel P: An X-linked syndrome of diarrhea, polyendocrinopathy, and fatal infection in infancy. J Pediatr 1982; 100:731-737.
21. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD: The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27:20-21.
22. Fontenot JD, Rudensky AY: A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005; 6:331-337.
23. Lee SK, Kim JY, Jang BW, Hur SE, Na BJ, Lee M, Fukui A, Gilman-Sachs A, Kwak-Kim J: Foxp3(high) and Foxp3(low) regulatory T cells differentially correlate with T helper 1 and natural killer cells in peripheral blood. Hum Immunol 2011; 72:621-626.
24. Vignali DA, Collison LW, Workman CJ: How regulatory T cells work. Nat Rev Immunol 2008; 8:523-532.
25. Guerin LR, Prins JR, Robertson SA: Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum Reprod Update 2009; 15:517-535.
26. Zhao JX, Zeng YY, Liu Y: Fetal alloantigen is responsible for the expansion of the CD4(+)CD25(+) regulatory T cell pool during pregnancy. J Reprod Immunol 2007; 75:71-81.
27. Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, Robertson SA: Seminal fluid regulates accumulation of FOXP3+ regulatory T Cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod 2011; 85:397-408.
28. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk HD: Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol 2005; 166:811-822.
29. Mjosberg J, Berg G, Ernerudh J, Ekerfelt C: CD4+ CD25+ regulatory T cells in human pregnancy: development of a regulatory T-MLC-ELISPOT suppression assay and indications of paternal specific regulatory Ts. Immunology 2007; 120:456-466.
30. Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, Scherjon SA, Claas FH: Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol 2008; 180:5737-5745.
31. Wan YY, Flavell RA: Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007; 445:766-770.
32. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE: Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007; 37:129-138.
33. Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, Niwa A, Parizot C, Taflin C, Heike T, Valeyre D, Mathian A, Nakahata T, Yamaguchi T, Nomura T, Ono M, Amoura Z, Gorochov G, Sakaguchi S: Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 2009; 30:899-911.
34. O'Connor W Jr, Zenewicz LA, Flavell RA: The dual nature of T(H)17 cells: shifting the focus to function. Nat Immunol 2010; 11:471-476.
35. Zhou L, Chong MM, Littman DR: Plasticity of CD4+ T cell lineage differentiation. Immunity 2009; 30:646-655.
36. Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, Mellor AL: IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009; 183:2475-2483.
37. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL: Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986; 136:2348-2357.
38. Coffman RL, Carty J: A T cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. J Immunol 1986; 136:949-954.
39. Steinman L: A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med 2007; 13:139-145.
40. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ: IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201:233-240.
41. Manel N, Unutmaz D, Littman DR: The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008; 9:641-649.
42. O'Garra A, Stockinger B, Veldhoen M: Differentiation of human T(H)-17 cells does require TGF-beta! Nat Immunol 2008; 9:588-590.
43. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, Oukka M, Kuchroo VK, Hafler DA: IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008; 454:350-352.
44. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C: A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6:1133-1141.
45. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Bamba T, Fujiyama Y: Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003; 52:65-70.
46. Kolls JK, Linden A: Interleukin-17 family members and inflammation. Immunity 2004; 21:467-476.
47. Ouyang W, Kolls JK, Zheng Y: The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008; 28:454-467.
48. Nakashima A, Ito M, Shima T, Bac ND, Hidaka T, Saito S: Accumulation of IL-17-Positive Cells in Decidua of Inevitable Abortion Cases. Am J Reprod Immunol 2010; 64:4-11.
49. van den Berg WB, Miossec P: IL-17 as a future therapeutic target for rheumatoid arthritis. Nat Rev Rheumatol 2009; 5:549-553.
50. Yen HR, Harris TJ, Wada S, Grosso JF, Getnet D, Goldberg MV, Liang KL, Bruno TC, Pyle KJ, Chan SL, Anders RA, Trimble CL, Adler AJ, Lin TY, Pardoll DM, Huang CT, Drake CG: Tc17 CD8 T cells: functional plasticity and subset diversity. J Immunol 2009; 183:7161-7168.
51. Nakashima A, Ito M, Yoneda S, Shiozaki A, Hidaka T, Saito S: Circulating and decidual Th17 cell levels in healthy pregnancy. Am J Reprod Immunol 2010; 63:104-109.
52. Arruvito L, Sanz M, Banham AH, Fainboim L: Expansion of CD4+CD25+and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol 2007; 178:2572-2578.
53. Prieto GA, Rosenstein Y: Oestradiol potentiates the suppressive function of human CD4 CD25 regulatory T cells by promoting their proliferation. Immunology 2006; 118:58-65.
54. Berbic M, Hey-Cunningham AJ, Ng C, Tokushige N, Ganewatta S, Markham R, Russell P, Fraser IS: The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum Reprod 2010; 25:900-907.
55. Kallikourdis M, Andersen KG, Welch KA, Betz AG: Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc Natl Acad Sci USA 2007; 104:594-599.
56. Kallikourdis M, Betz AG: Periodic accumulation of regulatory T cells in the uterus: preparation for the implantation of a semi-allogeneic fetus? PLoS ONE 2007; 2:e382.
57. Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, Alexander T, Taran A, Malfertheiner SF, Costa SD, Zimmermann G, Nitschke C, Volk HD, Alexander H, Gunzer M, Zenclussen AC: Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol 2009; 182:5488-5497.
58. Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT: Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 2004; 112:38-43.
59. Xiong H, Zhou C, Qi G: Proportional changes of CD4+CD25+Foxp3+ regulatory T cells in maternal peripheral blood during pregnancy and labor at term and preterm. Clin Invest Med 2010; 33:E422.
60. Steinborn A, Haensch GM, Mahnke K, Schmitt E, Toermer A, Meuer S, Sohn C: Distinct subsets of regulatory T cells during pregnancy: is the imbalance of these subsets involved in the pathogenesis of preeclampsia? Clinical Immunol 2008; 129:401-412.
61. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S: Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 2004; 10:347-353.
62. Tai P, Wang J, Jin H, Song X, Yan J, Kang Y, Zhao L, An X, Du X, Chen X, Wang S, Xia G, Wang B: Induction of regulatory T cells by physiological level estrogen. J Cell Physiol 2008; 214:456-464.
63. Santner-Nanan B, Peek MJ, Khanam R, Richarts L, Zhu E, Fazekas de St Groth B, Nanan R: Systemic increase in the ratio between Foxp3+ and IL-17-producing CD4+ T cells in healthy pregnancy but not in preeclampsia. J Immunol 2009; 183:7023-7030.
64. Liu YS, Wu L, Tong XH, Wu LM, He GP, Zhou GX, Luo LH, Luan HB: Study on the relationship between Th17 cells and unexplained recurrent spontaneous abortion. Am J Reprod Immunol 2011; 65:503-511.
65. Toldi G, Molvarec A, Stenczer B, Muller V, Eszes N, Bohacs A, Bikov A, Rigo J Jr, Vasarhelyi B, Losonczy G, Tamasi L: Peripheral Th1/Th2/Th17/regulatory T-cell balance in asthmatic pregnancy. Int Immunol 2011; 23:669-677.
66. Toldi G, Rigo J Jr, Stenczer B, Vasarhelyi B, Molvarec A: Increased prevalence of IL-17-producing peripheral blood lymphocytes in pre-eclampsia. Am J Reprod Immunol 2011; 66:223-229.
67. Ginsburg ES, Xiao L, Gargiulo AR, Kung FT, Politch JA, Schust DJ, Hill JA: T-helper 2 and 3 type immunity to trophoblast in successful in vitro fertilization-embryo transfer. Fertil Steril 2005; 83:1659-1664.
68. Jasper MJ, Tremellen KP, Robertson SA: Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod 2006; 12:301-308.
69. Boomsma CM, Kavelaars A, Eijkemans MJ, Amarouchi K, Teklenburg G, Gutknecht D, Fauser BJ, Heijnen CJ, Macklon NS: Cytokine profiling in endometrial secretions: a non-invasive window on endometrial receptivity. Reprod Biomed Online 2009; 18:85-94.
70. Wang WJ, Hao CF, Yi L, Yin GJ, Bao SH, Qiu LH, Lin QD: Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol 2010; 84:164-170.
71. Yang H, Qiu L, Di W, Zhao A, Chen G, Hu K, Lin Q: Proportional change of CD4+CD25+ regulatory T cells after lymphocyte therapy in unexplained recurrent spontaneous abortion patients. Fertil Steril 2009; 92:301-305.
72. Kessel A, Ammuri H, Peri R, Pavlotzky ER, Blank M, Shoenfeld Y, Toubi E: Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J Immunol 2007; 179:5571-5575.
73. Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD: The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod 2010; 25:2591-2596.