Modulation of T-cell Reactivity During Equine Pregnancy is Antigen Independent

American Journal of Reproductive Immunology

Volumn 68, Issue 2, 2012, Pages 107-115

  Noronha, Leela E ^a   Antczak, Douglas F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Cytotoxic T lymphocytes; Histocompatibility; Horse; Maternal tolerance; Paternal alloantigen

Indexed keywords

ALLOANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BREEDING; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENOME; HAPLOTYPE; HOMOZYGOSITY; IMMUNOMODULATION; MARE; MATING; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; STALLION;

ANIMALS; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HORSES; IMMUNE TOLERANCE; ISOANTIGENS; MALE; PREGNANCY; PREGNANCY, ANIMAL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84863859856     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2012.01154.x     Document Type: Article

References (70)

1. Roe R, Bell SC : Humoral immune responses in murine pregnancy. II. Kinetics and nature of the response in females preimmunized against paternal alloantigens. Immunology 1982; 46:23-30.
2. Smith RN, Amsden A, Sudilovsky O, Coleman N, Margolies R : The alloantibody response in the allogeneically pregnant rat. IV. Analysis of the alloantibody specificities with monoclonal antibodies. J Immunol 1986; 136:4063-4069.
3. Antczak DF, Bright SM, Remick LH, Bauman BE : Lymphocyte alloantigens of the horse. I. Serologic and genetic studies. Tissue Antigens 1982; 20:172-187.
4. Antczak DF, Miller JM, Remick LH : Lymphocyte alloantigens of the horse. II. Antibodies to ELA antigens produced during equine pregnancy. J Reprod Immunol 1984; 6:283-297.
5. Van Rood JJ, Eernisse JG, Van Leeuwen A : Leucocyte antibodies in sera from pregnant women. Nature 1958; 181:1735-1736.
6. Robertson SA, Guerin LR, Moldenhauer LM, Hayball JD : Activating T regulatory cells for tolerance in early pregnancy - the contribution of seminal fluid. J Reprod Immunol 2009; 83:109-116.
7. Tilburgs T, Scherjon SA, van der Mast BJ, Haasnoot GW, Versteeg VDV-MM, Roelen DL, van Rood JJ, Claas FH : Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J Reprod Immunol 2009; 82:148-157.
8. Zenclussen ML, Thuere C, Ahmad N, Wafula PO, Fest S, Teles A, Leber A, Casalis PA, Bechmann I, Priller J, Volk HD, Zenclussen AC : 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.
9. Seavey MM, Mosmann TR : Paternal antigen-bearing cells transferred during insemination do not stimulate anti-paternal CD8+ T cells: role of estradiol in locally inhibiting CD8+ T cell responses. J Immunol 2006; 177:7567-7578.
10. Smith JL : Foodborne infections during pregnancy. J Food Prot 1999; 62:818-829.
11. van der Klooster JM, Roelofs HJ : Management of Salmonella infections during pregnancy and puerperium. Neth J Med 1997; 51:83-86.
12. Avelino MM, Campos D Jr, do Carmo Barbosa de Parada J, de Castro AM : Pregnancy as a risk factor for acute toxoplasmosis seroconversion. Eur J Obstet Gynecol Reprod Biol 2003; 108:19-24.
13. Krishnan L, Guilbert LJ, Russell AS, Wegmann TG, Mosmann TR, Belosevic M : Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. J Immunol 1996; 156:644-652.
14. Luft BJ, Remington JS : Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice. Infect Immun 1982; 38:1164-1171.
15. Rowe JH, Ertelt JM, Aguilera MN, Farrar MA, Way SS : Foxp3(+) regulatory T cell expansion required for sustaining pregnancy compromises host defense against prenatal bacterial pathogens. Cell Host Microbe 2011; 10:54-64.
16. Ostensen M, Husby G : A prospective clinical study of the effect of pregnancy on rheumatoid arthritis and ankylosing spondylitis. Arthritis Rheum 1983; 26:1155-1159.
17. Waites GT, Whyte A : Effect of pregnancy on collagen-induced arthritis in mice. Clin Exp Immunol 1987; 67:467-476.
18. Petroff MG : Review: fetal antigens-identity, origins, and influences on the maternal immune system. Placenta 2011; 32(Suppl 2):S176-S181.
19. Yamada K : [Analysis on the CTL-p frequency before and after immunotherapy for patients with unexplained habitual abortion]. Nippon Sanka Fujinka Gakkai Zasshi 1993; 45:527-532.
20. Kotlan B, Fulop V, Padanyi A, Szigetvari I, Reti M, Gyodi E, Feher E, Petranyi G : High anti-paternal cytotoxic T-lymphocyte precursor frequencies in women with unexplained recurrent spontaneous abortions. Hum Reprod 2001; 16:1278-1285.
21. Manyonda IT, Pereira RS, Pearce JM, Sharrock CE : Limiting dilution analysis of the allo-MHC anti-paternal cytotoxic T cell response. II: recurrent spontaneous abortion and the effect of immunotherapy. Clin Exp Immunol 1993; 93:132-137.
22. Jiang SP, Vacchio MS : Multiple mechanisms of peripheral T cell tolerance to the fetal "allograft". J Immunol 1998; 160:3086-3090.
23. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B : T cell awareness of paternal alloantigens during pregnancy. Science 1995; 270:630-633.
24. Erlebacher A, Vencato D, Price KA, Zhang D, Glimcher LH : Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J Clin Invest 2007; 117:1399-1411.
25. Parvin M, Isobe K, Goto S, Nakashima I, Tomoda Y : Further evaluation of the pregnancy-linked down-regulation of the paternal antigen-specific splenic cytotoxic T lymphocyte activity in allogeneically pregnant mice. Microbiol Immunol 1992; 36:757-765.
26. Baker JM, Bamford AI, Antczak DF : Modulation of allospecific CTL responses during pregnancy in equids: an immunological barrier to interspecies matings? J Immunol 1999; 162:4496-4501.
27. Clark DA, McDermott MR : Impairment of host vs graft reaction in pregnant mice. I. Suppression of cytotoxic T cell generation in lymph nodes draining the uterus. J Immunol 1978; 121:1389-1393.
28. van Halteren AG, Jankowska-Gan E, Joosten A, Blokland E, Pool J, Brand A, Burlingham WJ, Goulmy E : Naturally acquired tolerance and sensitization to minor histocompatibility antigens in healthy family members. Blood 2009; 114:2263-2272.
29. Zhou M, Mellor AL : Expanded cohorts of maternal CD8+ T-cells specific for paternal MHC class I accumulate during pregnancy. J Reprod Immunol 1998; 40:47-62.
30. Nakamura N, Miyazaki K, Kitano Y, Fujisaki S, Okamura H : Suppression of cytotoxic T-lymphocyte activity during human pregnancy. J Reprod Immunol 1993; 23:119-130.
31. Thomas IK, Erickson KL : Gestational immunosuppression is mediated by specific Lyt 2+ T cells. Immunology 1986; 57:201-206.
32. Slapsys RM, Clark DA : Active suppression of host-vs-graft reaction in pregnant mice. IV. Local suppressor cells in decidua and uterine blood. J Reprod Immunol 1982; 4:355-364.
33. Chaouat G, Monnot P, Hoffmann M, Voisin GA : Regulatory T cells in pregnancy. VI. Evidence for T-cell-mediated suppression of CTL generation toward paternal alloantigens. Cell Immunol 1982; 68:322-331.
34. Hamilton MS, Hellstrom I : Altered immune responses in pregnant mice. Transplantation 1977; 23:423-430.
35. Clark DA, McDermott MR, Szewczuk MR : 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 1980; 52:106-118.
36. Noronha LE, Antczak DF : Maternal immune responses to trophoblast: the contribution of the horse to pregnancy immunology. Am J Reprod Immunol 2010; 64:231-244.
37. Antczak DF : Lymphocyte alloantigens of the horse. III. ELY-2.1: a lymphocyte alloantigen not coded for by the MHC. Anim Blood Groups Biochem Genet 1984; 15:103-115.
38. Adams AP, Oriol JG, Campbell RE, Oppenheim YC, Allen WR, Antczak DF : The effect of skin allografting on the equine endometrial cup reaction. Theriogenology 2007; 68:237-247.
39. Ellis SA, Bontrop RE, Antczak DF, Ballingall K, Davies CJ, Kaufman J, Kennedy LJ, Robinson J, Smith DM, Stear MJ, Stet RJ, Waller MJ, Walter L, Marsh SG : ISAG/IUIS-VIC Comparative MHC Nomenclature Committee report, 2005. Immunogenetics 2006; 57:953-958.
40. Lazary S, Antczak DF, Bailey E, Bell TK, Bernoco D, Byrns G, McClure JJ : Joint Report of the Fifth International Workshop on Lymphocyte Alloantigens of the Horse, Baton Rouge, Louisiana, 31 October-1 November 1987. Anim Genet 1988; 19:447-456.
41. Tseng CT, Miller D, Cassano J, Bailey E, Antczak DF : Identification of equine major histocompatibility complex haplotypes using polymorphic microsatellites. Anim Genet 2010; 41(Suppl 2):150-153.
42. Wagner B, Hillegas JM, Brinker DR, Horohov DW, Antczak DF : Characterization of monoclonal antibodies to equine interleukin-10 and detection of T regulatory 1 cells in horses. Vet Immunol Immunopathol 2008; 122:57-64.
43. Ellis WA, Bryson DG, O'Brien JJ, Neill SD : Leptospiral infection in aborted equine foetuses. Equine Vet J 1983; 15:321-324.
44. Givens MD, Marley MS : Infectious causes of embryonic and fetal mortality. Theriogenology 2008; 70:270-285.
45. Lunn DP, Davis-Poynter N, Flaminio MJ, Horohov DW, Osterrieder K, Pusterla N, Townsend HG : Equine herpesvirus-1 consensus statement. J Vet Intern Med 2009; 23:450-461.
46. Edington N, Smyth B, Griffiths L : The role of endothelial cell infection in the endometrium, placenta and foetus of equid herpesvirus 1 (EHV-1) abortions. J Comp Pathol 1991; 104:379-387.
47. Paillot R, Daly JM, Luce R, Montesso F, Davis-Poynter N, Hannant D, Kydd JH : Frequency and phenotype of EHV-1 specific, IFN-gamma synthesising lymphocytes in ponies: the effects of age, pregnancy and infection. Dev Comp Immunol 2007; 31:202-214.
48. Lissauer D, Choudhary M, Pachnio A, Goodyear O, Moss PA, Kilby MD : Cytomegalovirus sero positivity dramatically alters the maternal CD8+ T cell repertoire and leads to the accumulation of highly differentiated memory cells during human pregnancy. Hum Reprod 2011; 26:3355-3365.
49. Agricola R, Carvalho H, Barbosa M, Pereira M, Medeiros JA, Ferreira-Dias G : Blood lymphocyte subpopulations, neutrophil phagocytosis and proteinogram during late pregnancy and postpartum in mares. Reprod Domest Anim 2008; 43:212-217.
50. de Mestre A, Noronha L, Wagner B, Antczak DF : Split immunological tolerance to trophoblast. Int J Dev Biol 2010; 54:445-455.
51. Krakowski L, Krawczyk CH, Wrona Z, Dabrowski R, Jarosz L : Levels of selected T lymphocyte subpopulations in peripheral blood of mares which experienced early embryonic death. Anim Reprod Sci 2010; 120:71-77.
52. Beagley KW, Gockel CM : Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol Med Microbiol 2003; 38:13-22.
53. White HD, Crassi KM, Givan AL, Stern JE, Gonzalez JL, Memoli VA, Green WR, Wira CR : CD3+ CD8+ CTL activity within the human female reproductive tract: influence of stage of the menstrual cycle and menopause. J Immunol 1997; 158:3017-3027.
54. Watson ED, Stokes CR, Bourne FJ : Influence of administration of ovarian steroids on the function of neutrophils isolated from the blood and uterus of ovariectomized mares. J Endocrinol 1987; 112:443-448.
55. Pap E, Pallinger E, Falus A, Kiss AA, Kittel A, Kovacs P, Buzas EI : T lymphocytes are targets for platelet- and trophoblast-derived microvesicles during pregnancy. Placenta 2008; 29:826-832.
56. Morales PJ, Pace JL, Platt JS, Phillips TA, Morgan K, Fazleabas AT, Hunt JS : Placental cell expression of HLA-G2 isoforms is limited to the invasive trophoblast phenotype. J Immunol 2003; 171:6215-6224.
57. Roth TL, White KL, Thompson DL Jr, Rahmanian S, Horohov DW : Involvement of interleukin 2 receptors in conceptus-derived suppression of T and B cell proliferation in horses. J Reprod Fertil 1992; 96:309-322.
58. Lea RG, Bolton AE : The effect of horse placental tissue extracts and equine chorionic gonadotrophin on the proliferation of horse lymphocytes stimulated in vitro. J Reprod Immunol 1991; 19:13-23.
59. Flaminio MJ, Yen A, Antczak DF : The proliferation inhibitory proteins p27(Kip1) and retinoblastoma are involved in the control of equine lymphocyte proliferation. Vet Immunol Immunopathol 2004; 102:363-377.
60. Flaminio MJ, Antczak DF : Inhibition of lymphocyte proliferation and activation: a mechanism used by equine invasive trophoblast to escape the maternal immune response. Placenta 2005; 26:148-159.
61. Watson ED, Zanecosky HG : Regulation of mitogen- and TCGF-induced lymphocyte blastogenesis by prostaglandins and supernatant from equine embryos and endometrium. Res Vet Sci 1991; 51:61-65.
62. Watson ED : Suppression of lymphocyte reactivity by culture supernatant from horse embryos and endometrium. Biol Reprod 1990; 42:294-300.
63. Aluvihare VR, Kallikourdis M, Betz AG : Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5:266-271.
64. Leber A, Teles A, Zenclussen AC : Regulatory T cells and their role in pregnancy. Am J Reprod Immunol 2010; 63:445-459.
65. Polanczyk MJ, Carson BD, Subramanian S, Afentoulis M, Vandenbark AA, Ziegler SF, Offner H : Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J Immunol 2004; 173:2227-2230.
66. 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.
67. Aung S, Tang YW, Graham BS : Interleukin-4 diminishes CD8(+) respiratory syncytial virus-specific cytotoxic T-lymphocyte activity in vivo. J Virol 1999; 73:8944-8949.
68. Gao Q, Chen N, Rouse TM, Field EH : The role of interleukin-4 in the induction phase of allogeneic neonatal tolerance. Transplantation 1996; 62:1847-1854.
69. Hepworth MR, Hardman MJ, Grencis RK : The role of sex hormones in the development of Th2 immunity in a gender-biased model of Trichuris muris infection. Eur J Immunol 2010; 40:406-416.
70. Druckmann R, Druckmann MA : Progesterone and the immunology of pregnancy. J Steroid Biochem Mol Biol 2005; 97:389-396.