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Seminal fluid and reproduction: much more than previously thought

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Abstract

The influence of seminal plasma on the cytokine and immune uterine environment is well characterised in mice and humans, while the effects of disruption to uterine seminal plasma exposure on pregnancy and offspring health is becoming more clearly understood. The cellular and molecular environment of the uterus during the pre- and peri-implantation period of early pregnancy is critical for implantation success and optimal foetal and placental development. Perturbations to this environment not only have consequences for the success of pregnancy and neonatal health and viability, but can also drive adverse health outcomes in the offspring after birth, particularly the development of metabolic disorders such as obesity, hypertension and insulin resistance. It is now reported that an absence of seminal plasma at conception in mice promotes increased fat accumulation, altered metabolism and hypertension in offspring. The evidence reviewed here demonstrates that seminal plasma is not simply a transport medium for sperm, but acts also as a key regulator of the female tract environment providing optimal support for the developing embryo and benefiting future health of offspring.

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References

  1. Queen K, Dhabuwala CB, Pierrepoint CG. The effect of the removal of the various accessory sex glands on the fertility of male rats. J Reprod Fertil. 1981;62(2):423–6.

    CAS  PubMed  Google Scholar 

  2. Black CA, Rohan LC, Cost M, Watkins SC, Draviam R, Alber S, et al. Vaginal mucosa serves as an inductive site for tolerance. J Immunol. 2000;165(9):5077–83.

    CAS  PubMed  Google Scholar 

  3. Cukierski MA, Sina JL, Prahalada S, Robertson RT. Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reprod Toxicol. 1991;5(4):347–52.

    CAS  PubMed  Google Scholar 

  4. Chan OC, Chow PH, O WS. Total ablation of paternal accessory sex glands curtails developmental potential in preimplantation embryos in the golden hamster. Anat Embryol (Berl). 2001;204 (2):117–22.

  5. Tremellen KP, Valbuena D, Landeras J, Ballesteros A, Martinez J, Mendoza S, et al. The effect of intercourse on pregnancy rates during assisted human reproduction. Hum Reprod. 2000;15(12):2653–8.

    CAS  PubMed  Google Scholar 

  6. Maxwell WM, Evans G, Mortimer ST, Gillan L, Gellatly ES, McPhie CA. Normal fertility in ewes after cervical insemination with frozen-thawed spermatozoa supplemented with seminal plasma. Reprod Fertil Dev. 1999;11(2):123–6.

    CAS  PubMed  Google Scholar 

  7. Tremellen KP, Seamark RF, Robertson SA. Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod. 1998;58(5):1217–25.

    CAS  PubMed  Google Scholar 

  8. Robertson SA, Mau VJ, Tremellen KP, Seamark RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil. 1996;107(2):265–77.

    CAS  PubMed  Google Scholar 

  9. Robertson SA, Mau VJ, Hudson SN, Tremellen KP. Cytokine-leukocyte networks and the establishment of pregnancy. Am J Reprod Immunol. 1997;37(6):438–42.

    CAS  PubMed  Google Scholar 

  10. Robertson SA, Prins JR, Sharkey DJ, Moldenhauer LM. Seminal fluid and the generation of regulatory T cells for embryo implantation. Am J Reprod Immunol. 2013;69(4):315–30. doi:10.1111/aji.12107.

    CAS  PubMed  Google Scholar 

  11. Sharkey DJ, Macpherson AM, Tremellen KP, Mottershead DG, Gilchrist RB, Robertson SA. TGF-beta mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J Immunol. 2012;189(2):1024–35. doi:10.4049/jimmunol.1200005.

    CAS  PubMed  Google Scholar 

  12. Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol. 2012;188(5):2445–54. doi:10.4049/jimmunol.1102736.

    CAS  PubMed  Google Scholar 

  13. Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci U S A. 2014;111(6):2200–5. doi:10.1073/pnas.1305609111.

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Tremellen KP. Seminal priming for successful mammalian pregnancy. In: Gupta S, editor. Reproductive Immunology. New Delhi: Narosa Publishing House; 1999. p. 88–96.

    Google Scholar 

  15. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Bmj. 1989;298(6673):564–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Barker DJ. Mothers, Babies and Health in Later Life. Edinburgh, NY: Churchill Livingstone; 1998.

    Google Scholar 

  17. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001;185(1–2):93–8.

    CAS  PubMed  Google Scholar 

  18. Kind KL, Roberts CT, Sohlstrom AI. Katsman A. Robinson JS et al. Chronic maternal feed restriction impairs growth but increases adiposity of the fetal guinea pig. Am J Physiol Regul Integr Comp Physiol: Clifton PM; 2004.

    Google Scholar 

  19. Desai M, Gayle D, Babu J, Ross MG. Programmed Obesity in Intrauterine Growth Restricted Newborns: Modulation by Newborn Nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R91–6.

    CAS  PubMed  Google Scholar 

  20. Robinson JS, Falconer J, Owens JA. Intrauterine growth retardation: clinical and experimental. Acta Paediatr Scand Suppl. 1985;319:135–42.

    CAS  PubMed  Google Scholar 

  21. Elias SG, Peeters PH, Grobbee DE, van Noord PA. Breast cancer risk after caloric restriction during the 1944–1945 Dutch famine. J Natl Cancer Inst. 2004;96(7):539–46.

    PubMed  Google Scholar 

  22. Elias SG, Peeters PH, Grobbee DE, van Noord PA. The 1944–1945 Dutch famine and subsequent overall cancer incidence. Cancer Epidemiol Biomarkers Prev. 2005;14(8):1981–5.

    PubMed  Google Scholar 

  23. Elias SG, van Noord PA, Peeters PH, den Tonkelaar I, Grobbee DE. Childhood exposure to the 1944–1945 Dutch famine and subsequent female reproductive function. Hum Reprod. 2005;20(9):2483–8.

    PubMed  Google Scholar 

  24. Kind KL, Clifton PM, Katsman AI, Tsiounis M, Robinson JS, Owens JA. Restricted fetal growth and the response to dietary cholesterol in the guinea pig. Am J Physiol. 1999;277(6 Pt 2):R1675–82.

    CAS  PubMed  Google Scholar 

  25. Belobrajdic D, McIntosh G, Owens J. The effects of dietary protein on rat growth, body composition and insulin sensitivity. Asia Pac J Clin Nutr. 2003;12 Suppl:S42.

  26. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127(19):4195–202.

    CAS  PubMed  Google Scholar 

  27. Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134(9):2169–72.

    CAS  PubMed  Google Scholar 

  28. McConnell JM, Petrie L. Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod Biomed Online. 2004;9(4):418–24.

    CAS  PubMed  Google Scholar 

  29. Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare-Anane H, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R134–9.

    CAS  PubMed  Google Scholar 

  30. Sayer AA, Cooper C. Fetal programming of body composition and musculoskeletal development. Early Hum Dev. 2005;81(9):735–44.

    PubMed  Google Scholar 

  31. Fowden AL, Forhead AJ. Endocrine mechanisms of intrauterine programming. Reproduction. 2004;127(5):515–26.

    CAS  PubMed  Google Scholar 

  32. Fowden AL, Giussani DA, Forhead AJ. Endocrine and metabolic programming during intrauterine development. Early Hum Dev. 2005;81(9):723–34.

    CAS  PubMed  Google Scholar 

  33. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963–6. doi:10.1038/nature09491.

    CAS  PubMed  Google Scholar 

  34. Gardner DK, Lane M. Ex vivo early embryo development and effects on gene expression and imprinting. Reprod Fertil Dev. 2005;17(3):361–70.

    PubMed  Google Scholar 

  35. Lane M, Gardner DK. Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol Reprod. 2003;69(4):1109–17.

    CAS  PubMed  Google Scholar 

  36. Lane M, Gardner DK. Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod Fertil Dev. 2005;17(3):371–8.

    CAS  PubMed  Google Scholar 

  37. Robertson SA, Mayrhofer G, Seamark RF. Ovarian steroid hormones regulate granulocyte-macrophage colony-stimulating factor synthesis by uterine epithelial cells in the mouse. Biol Reprod. 1996;54(1):183–96.

    CAS  PubMed  Google Scholar 

  38. Robertson SA. Granulocyte-Macrophage Colony Stimulating Factor (GM-CSF): A Paracrine Regulator in the Pre-Implantation Mouse Uterus. Adelaide: University of Adelaide; 1993.

    Google Scholar 

  39. Sjoblom C, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor (GM-CSF) acts independently of the beta common subunit of the GM-CSF receptor to prevent inner cell mass apoptosis in human embryos. Biol Reprod. 2002;67(6):1817–23.

    CAS  PubMed  Google Scholar 

  40. Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF. Granulocyte-macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod. 2001;64(4):1206–15.

    CAS  PubMed  Google Scholar 

  41. Lavranos TC, Rathjen PD, Seamark RF. Trophic effects of myeloid leukaemia inhibitory factor (LIF) on mouse embryos. J Reprod Fertil. 1995;105(2):331–8.

    CAS  PubMed  Google Scholar 

  42. Hardy K, Spanos S. Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol. 2002;172(2):221–36.

    CAS  PubMed  Google Scholar 

  43. Schultz GA, Heyner S. Growth factors in preimplantation mammalian embryos. Oxf Rev Reprod Biol. 1993;15:43–81.

    CAS  PubMed  Google Scholar 

  44. Harvey MB, Kaye PL. Mediation of the actions of insulin and insulin-like growth factor-1 on preimplantation mouse embryos in vitro. Mol Reprod Dev. 1992;33(3):270–5.

    CAS  PubMed  Google Scholar 

  45. Brice EC, Wu JX, Muraro R, Adamson ED, Wiley LM. Modulation of mouse preimplantation development by epidermal growth factor receptor antibodies, antisense RNA, and deoxyoligonucleotides. Dev Genet. 1993;14(3):174–84.

    CAS  PubMed  Google Scholar 

  46. Tamada H, Higashiyama C, Takano H, Kawate N, Inaba T, Sawada T. The effects of heparin-binding epidermal growth factor-like growth factor on preimplantation-embryo development and implantation in the rat. Life Sci. 1999;64(22):1967–73.

    CAS  PubMed  Google Scholar 

  47. Sjoblom C, Roberts CT, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology. 2005;146(5):2142–53.

    PubMed  Google Scholar 

  48. Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online. 2003;7(1):65–70.

    CAS  PubMed  Google Scholar 

  49. Sanocka D, Miesel R, Jedrzejczak P, Chelmonska-Soyta AC, Kurpisz M. Effect of reactive oxygen species and the activity of antioxidant systems on human semen; association with male infertility. Int J Androl. 1997;20(5):255–64.

    CAS  PubMed  Google Scholar 

  50. Garrido N, Meseguer M, Simon C, Pellicer A, Remohi J. Pro-oxidative and anti-oxidative imbalance in human semen and its relation with male fertility. Asian J Androl. 2004;6(1):59–65.

    CAS  PubMed  Google Scholar 

  51. Wolters-Everhardt E, Dony JM, Lemmens WA, Doesburg WH, De Pont JJ. Buffering capacity of human semen. Fertil Steril. 1986;46(1):114–9.

    CAS  PubMed  Google Scholar 

  52. Wolters-Everhardt E, Dony JM, Peters WH, De Pont JJ. Buffering substances of human semen. Fertil Steril. 1987;48(1):159–61.

    CAS  PubMed  Google Scholar 

  53. Kelly RW. Prostaglandins in primate semen: biasing the immune system to benefit spermatozoa and virus? Prostaglandins Leukot Essent Fatty Acids. 1997;57(2):113–8.

    CAS  PubMed  Google Scholar 

  54. Peitz B, Olds-Clarke P. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod. 1986;35(3):608–17.

    CAS  PubMed  Google Scholar 

  55. Ying Y, Chow PH. Cheung MP. O WS Effects of male accessory sex glands on sperm decondensation and oocyte activation during in vivo fertilization in golden hamsters Int J Androl. 1999;22:68–76.

    CAS  Google Scholar 

  56. Pang SF, Chow PH, Wong TM. The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J Reprod Fertil. 1979;56(1):129–32.

    CAS  PubMed  Google Scholar 

  57. WS O, Chen HQ, Chow PH. Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J Reprod Fertil. 1988;84(1):341–4.

    Google Scholar 

  58. Jiang HY, O WS, Lee KH, Tang PL, Chow PH. Ablation of paternal accessory sex glands is detrimental to embryo development during implantation. Anat Embryol (Berl). 2001;203 (4):255–63.

  59. De M. Determination of the number and distribution of macrophages, lymphocytes and granulocytes in the mouse uterus from mating through implantation. J Leukoc Biol. 1991;50:252–62.

    CAS  PubMed  Google Scholar 

  60. Thompson LA, Barratt CL, Bolton AE, Cooke ID. The leukocytic reaction of the human uterine cervix. Am J Reprod Immunol. 1992;28(2):85–9.

    CAS  PubMed  Google Scholar 

  61. Phillips DM, Mahler S. Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat Rec. 1977;189(1):45–59.

    CAS  PubMed  Google Scholar 

  62. O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction. 2004;128(2):237–47.

    PubMed  Google Scholar 

  63. Pandya IJ, Cohen J. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril. 1985;43(3):417–21.

    CAS  PubMed  Google Scholar 

  64. Troedsson MH, Loset K, Alghamdi AM, Dahms B, Crabo BG. Interaction between equine semen and the endometrium: the inflammatory response to semen. Anim Reprod Sci. 2001;68(3–4):273–8.

    CAS  PubMed  Google Scholar 

  65. Anderson DJ, Tarter TH. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J Immunol. 1982;128(2):535–9.

    CAS  PubMed  Google Scholar 

  66. Fahmi HA, Hunter AG, Markham RJ, Seguin BE. Immunosuppressive activity of bovine seminal plasma on bovine lymphocytes in vitro. J Dairy Sci. 1985;68(9):2315–21.

    CAS  PubMed  Google Scholar 

  67. Saxena S, Jha P, Farooq A. Immunosuppression by human seminal plasma. Immunol Invest. 1985;14(3):255–69.

    CAS  PubMed  Google Scholar 

  68. James K. Immunosuppression by seminal plasma and its possible clinical significance. Immunol Today. 1984;5(12):357–63.

    Google Scholar 

  69. Anderson DJ, Tarter TH. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J Immunol. 1982;128(2):535–9.

    CAS  PubMed  Google Scholar 

  70. Kelly RW, Carr GG, Critchley HO. A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease. Hum Reprod. 1997;12(4):677–81.

    CAS  PubMed  Google Scholar 

  71. Robertson S, Sharkey D. The role of semen in induction of maternal immune tolerance to pregnancy. Semin Immunol. 2001;13(4):243–54.

    CAS  PubMed  Google Scholar 

  72. Thaler CJ. Immunological role for seminal plasma in insemination and pregnancy. Am J Reprod Immunol. 1989;21(3–4):147–50.

    CAS  PubMed  Google Scholar 

  73. Quayle AJ, Xu C, Mayer KH, Anderson DJ. T lymphocytes and macrophages, but not motile spermatozoa, are a significant source of human immunodeficiency virus in semen. J Infect Dis. 1997;176(4):960–8.

    CAS  PubMed  Google Scholar 

  74. Uyenoyama MK. Coevolution of the major histocompatibility complex and the t-complex in the mouse. I Generation and maintenance of high complementarity associations Genetics. 1989;121(1):139–51.

    CAS  Google Scholar 

  75. Iyer SV, Nandedkar TD, Hegde UC. Production of H-Y antibody in the ascites fluid of mouse and localization of the antigen on cells and tissues. Gamete Res. 1989;22(1):37–49.

    CAS  PubMed  Google Scholar 

  76. Anderson DJ, Bach DL, Yunis EJ, DeWolf WC. Major histocompatibility antigens are not expressed on human epididymal sperm. J Immunol. 1982;129(2):452–4.

    CAS  PubMed  Google Scholar 

  77. Hutter H, Dohr G. HLA expression on immature and mature human germ cells. J Reprod Immunol. 1998;38(2):101–22.

    CAS  PubMed  Google Scholar 

  78. Yao GD, Shu YM, Shi SL, Peng ZF, Song WY, Jin HX, et al. Expression and Potential Roles of HLA-G in Human Spermatogenesis and Early Embryonic Development. PloS one. 2014;9(3):e92889. doi:10.1371/journal.pone.0092889.

    PubMed Central  PubMed  Google Scholar 

  79. Beer AE, Billingham RE. Host responses to intra-uterine tissue, cellular and fetal allografts. J Reprod Fertil, Suppl. 1974;21:59–88.

    Google Scholar 

  80. Watson JG, Chaykin S, Carroll J. Repoduction in mice: The fate of sprematozoa not involved in fertilisation. Gamete Res. 1983;7:75–84.

    Google Scholar 

  81. Parr MB, Parr EL. Antigen recognition in the female reproductive tract: I. Uptake of intraluminal protein tracers in the mouse vagina J Reprod Immunol. 1990;17(2):101–14.

    CAS  Google Scholar 

  82. Parr EL, Parr MB, Zheng LM, Young JD. Mouse granulated metrial gland cells originate by local activation of uterine natural killer lymphocytes. Biol Reprod. 1991;44(5):834–41.

    CAS  PubMed  Google Scholar 

  83. Johansson M, Bromfield JJ, Jasper MJ, Robertson SA. Semen activates the female immune response during early pregnancy in mice. Immunology. 2004;112(2):290–300.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Piazzon I, Matusevich M, Deroche A, Nepomnaschy I, Pasqualini CD. Early increase in graft-versus-host reactivity during pregnancy in the mouse. J Reprod Immunol. 1985;8(2–3):129–37.

    CAS  PubMed  Google Scholar 

  85. O'Hearn M, Hilgard HR. Pregnancy-induced alterations in graft-versus-host responsiveness of uterine-draining and peripheral lymph node cells toward fetal alloantigens. Transplantation. 1981;32(5):389–91.

    PubMed  Google Scholar 

  86. Kapovic M, Rukavina D. Kinetics of lymphoproliferative responses of lymphocytes harvested from the uterine draining lymph nodes during pregnancy in rats. J Reprod Immunol. 1991;20:93–101.

    CAS  PubMed  Google Scholar 

  87. Clark D. Contoversies in reproductive immunology. Crit Rev Immunol. 1991;11 (3,4):215–47.

  88. Beer AE, Scott JR, Billingham RE. Histoincompatibility and maternal immunological status as determinants of fetoplacental weight and litter size in rodents. J Exp Med. 1975;142(1):180–96.

    CAS  PubMed  Google Scholar 

  89. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 2004;5(3):266–71.

    CAS  PubMed  Google Scholar 

  90. 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(2):397–408. doi:10.1095/biolreprod.110.088591.

    CAS  PubMed  Google Scholar 

  91. Vacchio MS, Jiang SP. The fetus and the maternal immune system: pregnancy as a model to study peripheral T-cell tolerance. Crit Rev Immunol. 1999;19(5–6):461–80.

    CAS  PubMed  Google Scholar 

  92. Billingham R. Transplantation immunity and the maternal-fetal relation. N Engl J Med. 1964;270(13):667–71.

    CAS  PubMed  Google Scholar 

  93. Daimon E, Wada Y. Role of neutrophils in matrix metalloproteinase activity in the preimplantation mouse uterus. Biol Reprod. 2005;73(1):163–71.

    CAS  PubMed  Google Scholar 

  94. Chow PH, Jiang HY, Poon HK, Lee KH, O WS. Embryos sired by males without accessory sex glands induce failure of uterine support: a study of VEGF, MMP and TGF expression in the golden hamster. Anat Embryol (Berl). 2003;206 (3):203–13.

  95. van der Heijden OW, Essers YP, Spaanderman ME, De Mey JG, van Eys GJ, Peeters LL. Uterine Artery Remodeling in Pseudopregnancy Is Comparable to that in Early Pregnancy. Biol Reprod. 2005;73(6):1289–93.

    PubMed  Google Scholar 

  96. Kosaka K, Fujiwara H, Tatsumi K, Yoshioka S, Higuchi T, Sato Y, et al. Human peripheral blood mononuclear cells enhance cell-cell interaction between human endometrial epithelial cells and BeWo-cell spheroids. Hum Reprod. 2003;18(1):19–25.

    CAS  PubMed  Google Scholar 

  97. Hill JA. T-helper 1-type immunity to trophoblast: evidence for a new immunological mechanism for recurrent abortion in women. Hum Reprod. 1995;10 Suppl 2:114–20.

    CAS  PubMed  Google Scholar 

  98. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today. 1997;18(10):478–82.

    CAS  PubMed  Google Scholar 

  99. Kanbour A, Ho HN, Misra DN, MacPherson TA, Kunz HW, Gill TJ. Differential expression of MHC class I antigens on the placenta of the rat. A mechanism for the survival of the fetal allograft J Exp Med. 1987;166(6):1861–82.

    CAS  Google Scholar 

  100. Kiger N, Chaouat G, Kolb JP, Wegmann TG, Guenet JL. Immunogenetic studies of spontaneous abortion in mice. Preimmunization of females with allogeneic cells J Immunol. 1985;134(5):2966–70.

    CAS  Google Scholar 

  101. Klonoff-Cohen HS, Savitz DA, Celafo RC, McCann MF. An epidemiologic study of contraception and preeclampsia. Journal of the American Medical association. 1989;262:3143–7.

    CAS  PubMed  Google Scholar 

  102. Robillard PY, Hulsey TC, Perianin J, Janky E, Miri EH, Papiernik E. Association of pregnancy-induced hypertension with duration of sexual cohabitation before conception. The Lancet. 1995;344:973–5.

    Google Scholar 

  103. Dekker GA, Robillard PY, Hulsey TC. Immune maladaptation in the etiology of preeclampsia: a review of corroborative epidemiologic studies. ObstetGynecolSurv. 1998;53(6):377–82.

    CAS  Google Scholar 

  104. Robertson SA, Bromfield JJ, Tremellen KP. Seminal 'priming' for protection from pre-eclampsia-a unifying hypothesis. J Reprod Immunol. 2003;59(2):253–65.

    PubMed  Google Scholar 

  105. Lambert RD. Safety issues in assisted reproductive technology: aetiology of health problems in singleton ART babies. Hum Reprod. 2003;18(10):1987–91.

    PubMed  Google Scholar 

  106. Perri T, Chen R, Yoeli R, Merlob P, Orvieto R, Shalev Y, et al. Are singleton assisted reproductive technology pregnancies at risk of prematurity? J Assist Reprod Genet. 2001;18(5):245–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  107. Wang JX, Norman RJ, Kristiansson P. The effect of various infertility treatments on the risk of preterm birth. Hum Reprod. 2002;17(4):945–9.

    CAS  PubMed  Google Scholar 

  108. Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med. 2002;346(10):731–7.

    PubMed  Google Scholar 

  109. Ochsenkuhn R, Strowitzki T, Gurtner M, Strauss A, Schulze A, Hepp H, et al. Pregnancy complications, obstetric risks, and neonatal outcome in singleton and twin pregnancies after GIFT and IVF. Arch Gynecol Obstet. 2003;268(4):256–61.

    PubMed  Google Scholar 

  110. Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med. 2002;346(10):725–30.

    PubMed  Google Scholar 

  111. Marchand E, Poncelet C, Carbillon L, Pharisien I, Tigaizin A, Chanelles O. Is there more complications with pregnancies from the assisted reproductive technology than spontaneous pregnancies? A retrospective study over 6 years. Journal de gynecologie, obstetrique et biologie de la reproduction. 2011;40(6):522–8. doi:10.1016/j.jgyn.2011.06.010.

    CAS  PubMed  Google Scholar 

  112. Berry KA, Baron IS, Weiss BA, Baker R, Ahronovich MD, Litman FR. In vitro fertilization and late preterm preschoolers' neuropsychological outcomes: the PETIT study. Am J Obstet Gynecol. 2013;209 (4):356 e1-6. doi:10.1016/j.ajog.2013.06.041.

  113. Thompson JG, Kind KL, Roberts CT, Robertson SA, Robinson JS. Epigenetic risks related to assisted reproductive technologies: short- and long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod. 2002;17(11):2783–6.

    CAS  PubMed  Google Scholar 

  114. Carp HJ, Serr DM, Mashiach S, Nebel L. Influence of insemination on the implantation of transferred rat blastocysts. Gynecol Obstet Invest. 1984;18(4):194–8.

    CAS  PubMed  Google Scholar 

  115. Coulam CB, Stern JJ. Effect of seminal plasma on implantation rates. Early Pregnancy. 1995;1(1):33–6.

    CAS  PubMed  Google Scholar 

  116. Marconi G, Auge L, Oses R, Quintana R, Raffo F, Young E. Does sexual intercourse improve pregnancy rates in gamete intrafallopian transfer? Fertil Steril. 1989;51(2):357–9.

    CAS  PubMed  Google Scholar 

  117. Bellinge BS, Copeland CM, Thomas TD, Mazzucchelli RE, O‶Neil G, Cohen MJ. The influence of patient insemination on the implantation rate in an in vitro fertilization and embryo transfer program. Fertil Steril. 1986;46(2):252–6.

    CAS  PubMed  Google Scholar 

  118. Fishel S, Webster J, Jackson P, Faratian B. Evaluation of high vaginal insemination at oocyte recovery in patients undergoing in vitro fertilization. Fertil Steril. 1989;51(1):135–8.

    CAS  PubMed  Google Scholar 

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Acknowledgments

I would like to thank Sarah Robertson who pioneered this field of investigation and has been an supportive mentor. I would also like to thank David Albertini for his support and critical evaluation of the manuscript.

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  1. Department of Animal Sciences, University of Florida, PO Box 110910, Gainesville, FL, 32611-0910, USA

    John J. Bromfield

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  1. John J. Bromfield
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Correspondence to John J. Bromfield.

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Capsule Seminal fluid exposure promotes healthy pregnancy outcomes.

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Bromfield, J.J. Seminal fluid and reproduction: much more than previously thought. J Assist Reprod Genet 31, 627–636 (2014). https://doi.org/10.1007/s10815-014-0243-y

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  • DOI: https://doi.org/10.1007/s10815-014-0243-y

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