Embryotoxic cytokines—Potential roles in embryo loss and fetal programming

Journal of Reproductive Immunology

Volumn 125, Issue , 2018, Pages 80-88

  Robertson, Sarah A ^a   Chin, Peck Yin ^a   Femia, Joseph G ^a   Brown, Hannah M ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Apoptosis; Cytokines; Embryo; IFNG; Stress response; TNF; TRAIL

Indexed keywords

COLONY STIMULATING FACTOR 1; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; LEUKEMIA INHIBITORY FACTOR; SOMATOMEDIN B; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; BLASTOCYST; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DIABETES MELLITUS; EMBRYO DEATH; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; ENDOMETRIOSIS; ENDOMETRIUM; EPIGENETICS; FEMALE INFERTILITY; FETUS GROWTH; GENE EXPRESSION; GENITAL TRACT INFECTION; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATION; NIDATION; NONHUMAN; OBESITY; OVARY POLYCYSTIC DISEASE; OVIDUCT; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROGENY; REVIEW; SPONTANEOUS ABORTION; UTERUS; ANIMAL; BLOOD; FEMALE; FETUS DEVELOPMENT; IMMUNOLOGY; INFERTILITY; INTRAUTERINE GROWTH RETARDATION; MAMMALIAN EMBRYO; METABOLIC DISORDER; METABOLISM; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; CYTOKINES; EMBRYO LOSS; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; HUMANS; INFERTILITY; METABOLIC DISEASES; PLACENTATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 85039950515     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2017.12.003     Document Type: Review

References (125)

1. Al Naib, A., Mamo, S., O'gorman, G.M., Lonergan, P., Swales, A., Fair, T., Regulation of non-classical major histocompatability complex class I mRNA expression in bovine embryos. J. Reprod. Immunol. 91 (2011), 31–40.
2. Almasan, A., Ashkenazi, A., Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev. 14 (2003), 337–348.
3. Bao, H., Qu, Q., Huang, X., Wang, M., Wang, X., Hao, C., Impact of hydrosalpinx fluid on early human embryos. Syst. Biol. Reprod. Med. 63 (2017), 279–284.
4. Bedaiwy, M.A., Falcone, T., Goldberg, J.M., Attaran, M., Sharma, R., Miller, K., Nelson, D.R., Agarwal, A., Relationship between cytokines and the embryotoxicity of hydrosalpingeal fluid. J. Assist. Reprod. Genet. 22 (2005), 161–165.
5. Beltman, M.E., Forde, N., Lonergan, P., Crowe, M.A., Altered endometrial immune gene expression in beef heifers with retarded embryos. Reprod. Fertil. Dev. 25 (2013), 966–970.
6. Ben-Yair, E., Less, A., Lev, S., Ben-Yehoshua, L., Tartakovsky, B., Tumour necrosis factor alpha binding to human and mouse trophoblast. Cytokine 9 (1997), 830–836.
7. Boehm, U., Klamp, T., Groot, M., Howard, J.C., Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15 (1997), 749–795.
8. Boomsma, C.M., Kavelaars, A., Eijkemans, M.J., Lentjes, E.G., Fauser, B.C., Heijnen, C.J., Macklon, N.S., Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum. Reprod. 24 (2009), 1427–1435.
9. Brison, D.R., Schultz, R.M., Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol. Reprod. 56 (1997), 1088–1096.
10. Bromfield, J.J., Schjenken, J.E., Chin, P.Y., Care, A.S., Jasper, M.J., Robertson, S.A., Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 2200–2205.
11. Brown, H.B., Green, E.S., Tan, T., Gonzalez, M., Rumbold, A.R., Hull, M.L., Norman, R.J., Packer, N., Robertson, S.A., Thompson, J.G., Periconception onset diabetes is associated with embryopathy and fetal growth retardation, reproductive tract hyperglycosylation and impaired immune adaptation to pregnancy. Sci. Rep., 2018 (in press).
12. Buckner, L.R., Lewis, M.E., Greene, S.J., Foster, T.P., Quayle, A.J., Chlamydia trachomatis infection results in a modest pro-inflammatory cytokine response and a decrease in T cell chemokine secretion in human polarized endocervical epithelial cells. Cytokine 63 (2013), 151–165.
13. Bulletti, C., De Ziegler, D., Giacomucci, E., Polli, V., Rossi, S., Alfieri, S., Flamigni, C., Vaginal drug delivery: the first uterine pass effect. Ann. N. Y. Acad. Sci. 828 (1997), 285–290.
14. Byrne, A.T., Southgate, J., Brison, D.R., Leese, H.J., Effects of insulin-like growth factors I and II on tumour-necrosis-factor-alpha-induced apoptosis in early murine embryos. Reprod. Fertil. Dev. 14 (2002), 79–83.
15. Cameo, M., Fontana, V., Cameo, P., Vauthay, L.G., Kaplan, J., Tesone, M., Similar embryotoxic effects of sera from infertile patients and exogenous interferon-gamma on long-term in-vitro development of mouse embryos. Hum. Reprod. 14 (1999), 959–963.
16. Chaouat, G., Menu, E., Clark, D.A., Dy, M., Minkowski, M., Wegmann, T.G., Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J. Reprod. Fertil. 89 (1990), 447–458.
17. Chen, H.L., Yelavarthi, K.K., Hunt, J.S., Identification of transforming growth factor-beta 1 mRNA in virgin and pregnant rat uteri by in situ hybridization. J. Reprod. Immunol. 25 (1993), 221–233.
18. Chen, J.C., Johnson, B.A., Erikson, D.W., Piltonen, T.T., Barragan, F., Chu, S., Kohgadai, N., Irwin, J.C., Greene, W.C., Giudice, L.C., Roan, N.R., Seminal plasma induces global transcriptomic changes associated with cell migration, proliferation and viability in endometrial epithelial cells and stromal fibroblasts. Hum. Reprod. 29 (2014), 1255–1270.
19. Cheung, L.P., Leung, H.Y., Bongso, A., Effect of supplementation of leukemia inhibitory factor and epidermal growth factor on murine embryonic development in vitro, implantation, and outcome of offspring. Fertil. Steril. 80:Suppl. 2 (2003), 727–735.
20. Chin, P.Y., Macpherson, A.M., Thompson, J.G., Lane, M., Robertson, S.A., Stress response genes are suppressed in mouse preimplantation embryos by granulocyte-macrophage colony-stimulating factor (GM-CSF). Hum. Reprod. 24 (2009), 2997–3009.
21. Chin, P.Y., Thompson, J.G., Robertson, S.A., A Modest Inflammatory Insult in the Pre-implantation Period Alters Oviduct Cytokine Expression and Programs Fetal Development. 2010, Society for Reproductive Biology, Sydney, Australia (pp. Abstract 172).
22. Chin, P.Y., Cytokines and Programming the Preimplantation Embryo Paediatrics and Reproductive Health. 2014, University of Adelaide, Adelaide.
23. Chu, T.M., Nocera, M.A., Flanders, K.C., Kawinski, E., Localization of seminal plasma transforming growth factor-beta1 on human spermatozoa: an immunocytochemical study. Fertil. Steril. 66 (1996), 327–330.
24. Clark, D.A., Chaouat, G., Arck, P.C., Mittruecker, H.W., Levy, G.A., Cytokine-dependent abortion in CBA x DBA/2 mice is mediated by the procoagulant fgl2 prothombinase. J. Immunol. 160 (1998), 545–549.
25. Croy, B.A., Van Den Heuvel, M.J., Borzychowski, A.M., Tayade, C., Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 214 (2006), 161–185.
26. Cummins, N., Badley, A., The TRAIL to viral pathogenesis: the good, the bad and the ugly. Curr. Mol. Med. 9 (2009), 495–505.
27. De Rycke, M., Liebaers, I., Van Steirteghem, A., Epigenetic risks related to assisted reproductive technologies: risk analysis and epigenetic inheritance. Hum. Reprod. 17 (2002), 2487–2494.
28. Dimitriadis, E., White, C.A., Jones, R.L., Salamonsen, L.A., Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 11 (2005), 613–630.
29. Doherty, A.S., Mann, M.R., Tremblay, K.D., Bartolomei, M.S., Schultz, R.M., Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62 (2000), 1526–1535.
30. Duleba, A.J., Dokras, A., Is PCOS an inflammatory process?. Fertil. Steril. 97 (2012), 7–12.
31. Eberhard, W.G., Postcopulatory sexual selection: darwin's omission and its consequences. Proc. Natl. Acad. Sci. U. S. A. 106:Suppl. 1 (2009), 10025–10032.
32. Fabian, D., Juhas, S., Il'kova, G., Koppel, J., Dose- and time-dependent effects of TNFalpha and actinomycin D on cell death incidence and embryo growth in mouse blastocysts. Zygote 15 (2007), 241–249.
33. Falschlehner, C., Schaefer, U., Walczak, H., Following TRAIL's path in the immune system. Immunology 127 (2009), 145–154.
34. Fichorova, R.N., Anderson, D.J., Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol. Reprod. 60 (1999), 508–514.
35. Fluhr, H., Sauter, G., Steinmuller, F., Licht, P., Zygmunt, M., Nonapoptotic effects of tumor necrosis factor-related apoptosis-inducing ligand on interleukin-6, leukemia inhibitory factor, interleukin-8, and monocyte chemoattractant protein 1 vary between undifferentiated and decidualized human endometrial stromal cells. Fertil. Steril. 92 (2009), 1420–1423.
36. Fontana, V., Choren, V., Vauthay, L., Calvo, J.C., Calvo, L., Cameo, M., Exogenous interferon-gamma alters murine inner cell mass and trophoblast development. Effect on the expression of ErbB1, ErbB4 and heparan sulfate proteoglycan (perlecan). Reproduction 128 (2004), 717–725.
37. Foote, R.H., Carney, E.W., Factors limiting reproductive efficiency in selected laboratory animals. Ann. N. Y. Acad. Sci. 541 (1988), 683–696.
38. Gillott, C., Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev. Entomol. 48 (2003), 163–184.
39. Glabowski, W., Kurzawa, R., Wiszniewska, B., Baczkowski, T., Marchlewicz, M., Brelik, P., Growth factors effects on preimplantation development of mouse embryos exposed to tumor necrosis factor alpha. Reprod. Biol. 5 (2005), 83–99.
40. Glynn, D.J., Sharkey, D.J., Robertson, S.A., Interferon-gamma inhibits female reproductive tract responsiveness to seminal plasma. Biology of Reproduction. 37th Annual Meeting of the Society for the Study of Reproduction, 2004, 242.
41. Groebner, A.E., Schulke, K., Unterseer, S., Reichenbach, H.D., Reichenbach, M., Buttner, M., Wolf, E., Meyer, H.H., Ulbrich, S.E., Enhanced proapoptotic gene expression of XAF1, CASP8 and TNFSF10 in the bovine endometrium during early pregnancy is not correlated with augmented apoptosis. Placenta 31 (2010), 168–177.
42. Guerin, L.R., Prins, J.R., Robertson, S.A., Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment?. Hum. Reprod. Update 15 (2009), 517–535.
43. Gutsche, S., Von Wolff, M., Strowitzki, T., Thaler, C.J., Seminal plasma induces mRNA expression of IL-1beta, IL-6 and LIF in endometrial epithelial cells in vitro. Mol. Hum. Reprod. 9 (2003), 785–791.
44. Haimovici, F., Hill, J.A., Anderson, D.J., Variables affecting toxicity of human sera in mouse embryo cultures. J. In Vitro Fert. Embryo Transf. 5 (1988), 202–206.
45. Hannan, N.J., Paiva, P., Meehan, K.L., Rombauts, L.J., Gardner, D.K., Salamonsen, L.A., Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152 (2011), 4948–4956.
46. Hansen, P.J., Soto, P., Natzke, R.P., Mastitis and fertility in cattle − possible involvement of inflammation or immune activation in embryonic mortality. Am. J. Reprod. Immunol. 51 (2004), 294–301.
47. Hansen, P.J., Dobbs, K.B., Denicol, A.C., Programming of the preimplantation embryo by the embryokine colony stimulating factor 2. Anim. Reprod. Sci. 149 (2014), 59–66.
48. Hardy, K., Spanos, S., Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172 (2002), 221–236.
49. Hardy, K., Apoptosis in the human embryo. Rev. Reprod. 4 (1999), 125–134.
50. Harith, H.H., Morris, M.J., Kavurma, M.M., On the TRAIL of obesity and diabetes. Trends Endocrinol. Metab. 24 (2013), 578–587.
51. Heikkinen, J., Mottonen, M., Komi, J., Alanen, A., Lassila, O., Phenotypic characterization of human decidual macrophages. Clin. Exp. Immunol. 131 (2003), 498–505.
52. Hill, J.A., Haimovici, F., Anderson, D.J., Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro. J. Immunol. 139 (1987), 2250–2254.
53. Hill, J.A., Polgar, K., Harlow, B.L., Anderson, D.J., Evidence of embryo- and trophoblast-toxic cellular immune response(s) in women with recurrent spontaneous abortion. Am. J. Obstet. Gynecol. 166 (1992), 1044–1052.
54. Hochberg, Z., Feil, R., Constancia, M., Fraga, M., Junien, C., Carel, J.C., Boileau, P., Le Bouc, Y., Deal, C.L., Lillycrop, K., Scharfmann, R., Sheppard, A., Skinner, M., Szyf, M., Waterland, R.A., Waxman, D.J., Whitelaw, E., Ong, K., Albertsson-Wikland, K., Child health, developmental plasticity, and epigenetic programming. Endocr. Rev. 32 (2011), 159–224.
55. Hunt, J.S., Expression and regulation of the tumour necrosis factor-alpha gene in the female reproductive tract. Reprod. Fertil. Dev. 5 (1993), 141–153.
56. Jenkins, C., Roberts, J., Wilson, R., Maclean, M.A., Shilito, J., Walker, J.J., Evidence of a T(H) 1 type response associated with recurrent miscarriage. Fertil. Steril. 73 (2000), 1206–1208.
57. Jokhi, P.P., King, A., Sharkey, A.M., Smith, S.K., Loke, Y.W., Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse- transcriptase polymerase chain reaction. J. Immunol. 153 (1994), 4427–4435.
58. Kafka, J.K., Sheth, P.M., Nazli, A., Osborne, B.J., Kovacs, C., Kaul, R., Kaushic, C., Endometrial epithelial cell response to semen from HIV-infected men during different stages of infection is distinct and can drive HIV-1-long terminal repeat. AIDS 26 (2012), 27–36.
59. Kanno, Y., Vahedi, G., Hirahara, K., Singleton, K., O'shea, J.J., Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Annu. Rev. Immunol. 30 (2012), 707–731.
60. Kaushic, C., Grant, K., Crane, M., Wira, C.R., Infection of polarized primary epithelial cells from rat uterus with Chlamydia trachomatis: cell–cell interaction and cytokine secretion. Am. J. Reprod. Immunol. 44 (2000), 73–79.
61. Kawamura, K., Kawamura, N., Kumagai, J., Fukuda, J., Tanaka, T., Tumor necrosis factor regulation of apoptosis in mouse preimplantation embryos and its antagonism by transforming growth factor alpha/phosphatidylionsitol 3-kinase signaling system. Biol. Reprod. 76 (2007), 611–618.
62. Keogh, R.J., Harris, L.K., Freeman, A., Baker, P.N., Aplin, J.D., Whitley, G.S., Cartwright, J.E., Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-alpha-related apoptosis-inducing ligand to induce smooth muscle cell death. Circ. Res. 100 (2007), 834–841.
63. Khosla, S., Dean, W., Brown, D., Reik, W., Feil, R., Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol. Reprod. 64 (2001), 918–926.
64. Kittan, N.A., Allen, R.M., Dhaliwal, A., Cavassani, K.A., Schaller, M., Gallagher, K.A., Carson, W.F.T., Mukherjee, S., Grembecka, J., Cierpicki, T., Jarai, G., Westwick, J., Kunkel, S.L., Hogaboam, C.M., Cytokine induced phenotypic and epigenetic signatures are key to establishing specific macrophage phenotypes. PLoS One, 8, 2013, e78045.
65. Koot, Y.E., Teklenburg, G., Salker, M.S., Brosens, J.J., Macklon, N.S., Molecular aspects of implantation failure. Biochim. Biophys. Acta 1822 (2012), 1943–1950.
66. Lachapelle, M.H., Miron, P., Hemmings, R., Falcone, T., Granger, L., Bourque, J., Langlais, J., Embryonic resistance to tumour necrosis factor-alpha mediated cytotoxicity: novel mechanism underlying maternal immunological tolerance to the fetal allograft. Hum. Reprod. 8 (1993), 1032–1038.
67. Ledee, N., Munaut, C., Aubert, J., Serazin, V., Rahmati, M., Chaouat, G., Sandra, O., Foidart, J.M., Specific and extensive endometrial deregulation is present before conception in IVF/ICSI repeated implantation failures (IF) or recurrent miscarriages. J. Pathol. 225 (2011), 554–564.
68. Leese, H.J., Human embryo culture: back to nature. J. Assist. Reprod. Genet. 15 (1998), 466–468.
69. Li, H.Z., Sun, X., Stavreus-Evers, A., Gemzell-Danielsson, K., Effect of mifepristone on the expression of cytokines in the human Fallopian tube. Mol. Hum. Reprod. 10 (2004), 489–493.
70. Lotti, F., Corona, G., Colpi, G.M., Filimberti, E., Degli Innocenti, S., Mancini, M., Baldi, E., Noci, I., Forti, G., Adorini, L., Maggi, M., Elevated body mass index correlates with higher seminal plasma interleukin 8 levels and ultrasonographic abnormalities of the prostate in men attending an andrology clinic for infertility. J. Endocrinol. Invest. 34 (2011), e336–42.
71. Loureiro, B., Brad, A.M., Hansen, P.J., Heat shock and tumor necrosis factor-alpha induce apoptosis in bovine preimplantation embryos through a caspase-9-dependent mechanism. Reproduction 133 (2007), 1129–1137.
72. Lumicisi, B.A., Cartwright, J.E., Leslie, K., Wallace, A.E., Whitley, G.S., Inhibition of DDAH1, but not DDAH2, results in apoptosis of a human trophoblast cell line in response to TRAIL. Hum. Reprod. 30 (2015), 1813–1819.
73. Macklon, N.S., Brosens, J.J., The human endometrium as a sensor of embryo quality. Biol. Reprod., 91, 2014, 98.
74. Marey, M.A., Yousef, M.S., Kowsar, R., Hambruch, N., Shimizu, T., Pfarrer, C., Miyamoto, A., Local immune system in oviduct physiology and pathophysiology: attack or tolerance?. Domest. Anim. Endocrinol. 56:Suppl (2016), S204–S211.
75. Martal, J., Chene, N., Camous, S., Huynh, L., Lantier, F., Hermier, P., L'haridon, R., Charpigny, G., Charlier, M., Chaouat, G., Recent developments and potentialities for reducing embryo mortality in ruminants: the role of IFN-tau and other cytokines in early pregnancy. Reprod. Fertil. Dev. 9 (1997), 355–380.
76. Mor, G., Aldo, P., Alvero, A.B., The unique immunological and microbial aspects of pregnancy. Nat. Rev. Immunol. 17 (2017), 469–482.
77. Morgan, H.D., Santos, F., Green, K., Dean, W., Reik, W., Epigenetic reprogramming in mammals. Hum. Mol. Genet., 14, 2005 (Spec No 1, R47-58).
78. Murphy, S.P., Tayade, C., Ashkar, A.A., Hatta, K., Zhang, J., Croy, B.A., Interferon gamma in successful pregnancies. Biol. Reprod. 80 (2009), 848–859.
79. Norwitz, E.R., Schust, D.J., Fisher, S.J., Implantation and the survival of early pregnancy. N. Engl. J. Med. 345 (2001), 1400–1408.
80. O'Neill, C., The potential roles for embryotrophic ligands in preimplantation embryo development. Hum. Reprod. Update 14 (2008), 275–288.
81. Pampfer, S., Moulaert, B., Vanderheyden, I., Wuu, Y.D., De Hertogh, R., Effect of tumour necrosis factor alpha on rat blastocyst growth and glucose metabolism. J. Reprod. Fertil. 101 (1994), 199–206.
82. Pampfer, S., Vanderheyden, I., Mccracken, J.E., Vesela, J., De Hertogh, R., Increased cell death in rat blastocysts exposed to maternal diabetes in utero and to high glucose or tumor necrosis factor-alpha in vitro. Development 124 (1997), 4827–4836.
83. Pampfer, S., Dysregulation of the cytokine network in the uterus of the diabetic rat. Am. J. Reprod. Immunol. 45 (2001), 375–381.
84. Phillips, T.A., Ni, J., Hunt, J.S., Death-inducing tumour necrosis factor (TNF) superfamily ligands and receptors are transcribed in human placentae cytotrophoblasts, placental macrophages and placental cell lines. Placenta 22 (2001), 663–672.
85. Piccinni, M.P., Romagnani, S., Regulation of fetal allograft survival by a hormone-controlled Th1- and Th2-type cytokines. Immunol. Res. 15 (1996), 141–150.
86. Plante, M.K., Arscott, W.T., Folsom, J.B., Tighe, S.W., Dempsey, R.J., Wesley, U.V., Ethanol promotes cytotoxic effects of tumor necrosis factor-related apoptosis-inducing ligand through induction of reactive oxygen species in prostate cancer cells. Prostate Cancer Prostatic Dis. 16 (2013), 16–22.
87. Rasmussen, S.J., Eckmann, L., Quayle, A.J., Shen, L., Zhang, Y.X., Anderson, D.J., Fierer, J., Stephens, R.S., Kagnoff, M.F., Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J. Clin. Invest. 99 (1997), 77–87.
88. Richter, K.S., The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr. Opin. Obstet. Gynecol. 20 (2008), 292–304.
89. Riley, J.K., Heeley, J.M., Wyman, A.H., Schlichting, E.L., Moley, K.H., TRAIL and KILLER are expressed and induce apoptosis in the murine preimplantation embryo. Biol. Reprod. 71 (2004), 871–877.
90. Robertson, S.A., Sharkey, D.J., Seminal fluid and fertility in women. Fertil. Steril. 106 (2016), 511–519.
91. Robertson, S.A., Chin, P.Y., Glynn, D.J., Thompson, J.G., Peri-conceptual cytokines–setting the trajectory for embryo implantation, pregnancy and beyond. Am. J. Reprod. Immunol. 66:Suppl. 1 (2011), 2–10.
92. Robertson, S.A., Chin, P.Y., Schjenken, J.E., Thompson, J.G., Female tract cytokines and developmental programming in embryos. Adv. Exp. Med. Biol. 843 (2015), 173–213.
93. Robertson, S.A., Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res. 322 (2005), 43–52.
94. Robertson, S.A., Immune regulation of conception and embryo implantation—all about quality control?. J. Reprod. Immunol. 85 (2010), 51–57.
95. Rull, K., Tomberg, K., Koks, S., Mannik, J., Mols, M., Sirotkina, M., Varv, S., Laan, M., Increased placental expression and maternal serum levels of apoptosis-inducing TRAIL in recurrent miscarriage. Placenta 34 (2013), 141–148.
96. Salamonsen, L.A., Zhang, J., Brasted, M., Leukocyte networks and human endometrial remodelling. J. Reprod. Immunol. 57 (2002), 95–108.
97. Sanford, T.R., De, M., Wood, G.W., Expression of colony-stimulating factors and inflammatory cytokines in the uterus of CD1 mice during days 1–3 of pregnancy. J. Reprod. Fertil. 94 (1992), 213–220.
98. Schaefer, T.M., Fahey, J.V., Wright, J.A., Wira, C.R., Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 174 (2005), 992–1002.
99. Schjenken, J.E., Robertson, S.A., Seminal fluid and immune adaptation for pregnancy?comparative biology in mammalian species. Reprod. Domest. Anim. 49:Suppl. 3 (2014), 27–36.
100. Sedger, L.M., Shows, D.M., Blanton, R.A., Peschon, J.J., Goodwin, R.G., Cosman, D., Wiley, S.R., IFN-gamma mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163 (1999), 920–926.
101. Sharkey, D.J., Macpherson, A.M., Tremellen, K.P., Robertson, S.A., Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod. 13 (2007), 491–501.
102. Sharkey, D.J., Tremellen, K.P., Jasper, M.J., Gemzell-Danielsson, K., Robertson, S.A., Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J. Immunol. 188 (2012), 2445–2454.
103. Sharkey, D.J., Tremellen, K.P., Briggs, N.E., Dekker, G.A., Robertson, S.A., Seminal plasma transforming growth factor-beta, activin A and follistatin fluctuate within men over time. Hum. Reprod. 31 (2016), 2183–2191.
104. Singer, M., Ouburg, S., Effect of cytokine level variations in individuals on the progression and outcome of bacterial urogenital infections–a meta-analysis. Pathog. Dis., 74, 2016.
105. Sjoblom, C., Roberts, C.T., Wikland, M., Robertson, S.A., Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146 (2005), 2142–2153.
106. Soto, P., Natzke, R.P., Hansen, P.J., Actions of tumor necrosis factor-alpha on oocyte maturation and embryonic development in cattle. Am. J. Reprod. Immunol. 50 (2003), 380–388.
107. Stilley, J.A., Birt, J.A., Sharpe-Timms, K.L., Cellular and molecular basis for endometriosis-associated infertility. Cell Tissue Res. 349 (2012), 849–862.
108. Tabibzadeh, S., Sun, X.Z., Cytokine expression in human endometrium throughout the menstrual cycle. Hum. Reprod. 7 (1992), 1214–1221.
109. Talukder, A.K., Yousef, M.S., Rashid, M.B., Awai, K., Acosta, T.J., Shimizu, T., Okuda, K., Shimada, M., Imakawa, K., Miyamoto, A., Bovine embryo induces an anti-inflammatory response in uterine epithelial cells and immune cells in vitro: possible involvement of interferon tau as an intermediator. J. Reprod. Dev. 63 (2017), 425–434.
110. Teklenburg, G., Salker, M., Heijnen, C., Macklon, N.S., Brosens, J.J., The molecular basis of recurrent pregnancy loss: impaired natural embryo selection. Mol. Hum. Reprod. 16 (2010), 886–895.
111. Thompson, J.G., Kind, K.L., Roberts, C.T., Robertson, S.A., Robinson, J.S., 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. 17 (2002), 2783–2786.
112. Thouas, G.A., Dominguez, F., Green, M.P., Vilella, F., Simon, C., Gardner, D.K., Soluble ligands and their receptors in human embryo development and implantation. Endocr. Rev. 36 (2015), 92–130.
113. Ting, A.T., Bertrand, M.J., More to life than NF-kappaB in TNFR1 signaling. Trends Immunol. 37 (2016), 535–545.
114. Torchinsky, A., Toder, V., TNFalpha in the pathogenesis of diabetes-induced embryopathies: functions and targets. Rev. Diabet. Stud. 4 (2007), 200–209.
115. Torchinsky, A., Gongadze, M., Orenstein, H., Savion, S., Fein, A., Toder, V., TNF-alpha acts to prevent occurrence of malformed fetuses in diabetic mice. Diabetologia 47 (2004), 132–139.
116. Truchet, S., Wietzerbin, J., Debey, P., Mouse oocytes and preimplantation embryos bear the two sub-units of interferon-gamma receptor. Mol. Reprod. Dev. 60 (2001), 319–330.
117. Tzanavari, T., Giannogonas, P., Karalis, K.P., TNF-alpha and obesity. Curr. Dir. Autoimmun. 11 (2010), 145–156.
118. Vaculova, A., Hofmanova, J., Soucek, K., Andera, L., Kozubik, A., Ethanol acts as a potent agent sensitizing colon cancer cells to the TRAIL-induced apoptosis. FEBS Lett. 577 (2004), 309–313.
119. Wang, S., El-Deiry, W.S., TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 22 (2003), 8628–8633.
120. Waterland, R.A., Jirtle, R.L., Early nutrition, epigenetic changes at transposons and imprinted genes: and enhanced susceptibility to adult chronic diseases. Nutrition 20 (2004), 63–68.
121. Whiteside, E.J., Boucaut, K.J., Teh, A., Garcia-Aragon, J., Harvey, M.B., Herington, A.C., Elevated concentration of TNF-alpha induces trophoblast differentiation in mouse blastocyst outgrowths. Cell Tissue Res. 314 (2003), 275–280.
122. Williams, C.L., Teeling, J.L., Perry, V.H., Fleming, T.P., Mouse maternal systemic inflammation at the zygote stage causes blunted cytokine responsiveness in lipopolysaccharide-challenged adult offspring. BMC Biol., 9, 2011, 49.
123. Wuu, Y.D., Pampfer, S., Becquet, P., Vanderheyden, I., Lee, K.H., De Hertogh, R., Tumor necrosis factor alpha decreases the viability of mouse blastocysts in vitro and in vivo. Biol. Reprod. 60 (1999), 479–483.
124. Young, L.E., Imprinting of genes and the Barker hypothesis. Twin Res. 4 (2001), 307–317.
125. Zhao, X.Y., Sakashita, K., Kamijo, T., Hidaka, E., Sugane, K., Kubota, T., Koike, K., Granulocyte-macrophage colony-stimulating factor induces de novo methylation of the p15 CpG island in hematopoietic cells. Cytokine 31 (2005), 203–212.