medigraphic.com

2006, Number 3

<< Back Next >>

Vet Mex 2006; 37 (3)

Role of cytokines in embryo implantation in domestic mammals

Betancourt-Alonso MA, Flores-Pérez FI, Rosas-Velasco C, Pérez-Martínez M

Language: English/Spanish
References: 86
Page: 335-350
PDF size: 308.90 Kb.


ABSTRACT

In the embryo implantation process there are various molecular mediators, including cytokines and growth factors, which act in an autocrine, paracrine, or juxtacrine manner. Although we know that the interactions between these factors are necessary, as a whole and in chronological order, their precise participation is not yet known in the different stages of early embryonic develop-ment. In this article we review different aspects related to the functional participation of cytokines, identifi ed up to this point, in embryo implantation in domestic mammals such as interferon-tau (IFN-τ) in ruminants, transforming growth factor (TGF) in pigs, and insulin growth factor (IGF) in horses.


REFERENCES

  1. Sharkey A. Cytokines and implantation. Rev Reprod 1998;3:52-61.

  2. Tizard IR. Veterinary Immunology: an introduction. 6a ed. Philadelphia: McGraw-Hill Interamericana, 2000.

  3. Abbas AK. Inmunología celular y molecular. 4ª ed. New York: W. B. Saunders Company, 2000

  4. Kuby J. Immunology. 4a ed . New York: W. H. Freeman and Company, 2000

  5. Viganó P, Mangioni S, Pompei F, Chiodo I. Maternal-conceptus Cross Talk-A Review. Placenta 2003;24:S56-S61.

  6. Salamonsen LA, Guiying N, Findlay K. Newly identi-fi ed endometrial genes of importance for implanta-tion. J Reprod Immunol 2002;53:215-225.

  7. Paria BC, Lim H, Das SK, Reese J, Dey SK. Molecular signaling in uterine receptivity for implantation. Cell Develop Biol 2000;11:67-76.

  8. Kovats S, Main EK, Librach C, Stubbleine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990;248:220-223.

  9. Ellis S. HLA-G: at the interface. Am J Reprod Immnunol 1990;23:84-86.

  10. Schmidt CM, Garret E, Orr HT. Cytotoxic T lympho-cite recognition of HLA-G in mice. Hum Immunol 1997;55:127-139.

  11. Soderstrom K, Corliss B, Lanier LL, Phillips JH. CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J Immunol 1997;159:1072-1075.

  12. Linnemeyer PA, Pollack SB. Prostaglandin E2-induced changes in the phenotype, morphology, and lytic activ-ity of IL-2 activated natural killer cells. J Immunol 1993;150:3747-3754.

  13. Ouellete MJ, Dubois CM, Bergeron D, Roy R, Lambert RD. TGFβ2 in rabbit blastocoelic fl uid regulates CD4 membrane expression: possible role in the success of gestation. Am J Reprod Immunol 1997;37:125-136.

  14. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Weg-mann TG. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993;151:4562-4573.

  15. Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidi-rectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenom-enon? Immunol Today 1993;14:353-356.

  16. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L. Progesterone as an immu-nomodulatory molecule. Int Immunopharmacol 2001;1:1037-1048.

  17. Hansen PJ. Interactions between the immune system and the ruminant conceptus. J Reprod Fertil 1995;49(Suppl 1):69-82.18.19.20.21.

  18. Stewart HJ, McCann SH, Barker PJ, Lee KE, Lamming GE, Flint AP. Interferon sequence homology and recep-tor binding activity of ovine trophoblast antiluteolytic protein. J Endocrinol 1987;115:R13-15.

  19. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophecto-derm. Nature 1987;330:377-379.

  20. Charpigny G, Reinaud P, Huet JC, Guillomot M, Char-lier M, Pernollet JC et al. High homology between a tro-phoblastic protein (Trophoblastin) isolated from ovine embryo and α-interferons. FEBS Lett 1988;228:12-16.

  21. Imakawa K, Hansen TR, Malathy PV, Anthony RV, Poites HG, Marotti KR et al. Molecular cloning and characterization of complementary deoxyribonucleic acids corresponding to bovine trophoblast protein-1: a comparison with ovine trophoblast protein –1 and bovine interferon-α II. Mol Endocrinol 1989;3:127-139.

  22. Stewart HJ, McCann SH, Flint AP. Structure of an interferon-α 2 gene expressed in the bovine conceptus early in gestation. J Mol Endocrinol 1990;4:275-282.

  23. Cross JC, Roberts RM. Porcine conceptuses secrete an interferon during preattachment period of early preg-nancy. Biol Reprod 1989;40:1109-1118.

  24. Aboagye-Mathiesen G, Toth FD, Zdravkovic M, Ebbesen P. Human trophoblast interferons: production and possible roles in early pregnancy. Early Pregnancy 1995;1:41-53.

  25. Spencer TE, Becker WC, George P, Mirando MA, Ogle TF, Bazer FW. Ovine interferon-τ inhibits estrogen receptor up-regulation and estrogen-induced luteoly-sis in cyclic ewes. Endocrinology 1995;136:4932-4944.

  26. Spencer TE, Bazer FW. Ovine interferon-τ suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinol-ogy 1996;137:1144-1147.

  27. Newton GR, Vallet JL, Hansen PJ, Bazer FW. Inhibition of lymphocyte proliferation by ovine trophoblast protein-1 and a high molecular weight glycoprotein pro-duced by the peri-implantation sheep conceptus. Am J Reprod Immunol 1989;19:99-107.

  28. Pontzer CH, Bazer FW, Johnson HM. Antiproliferative activity of a pregnancy recognition hormone, ovine trophoblast protein-1. Cancer Res 1991;51:5304-5307.

  29. Subramaniam PS, Khan Sa, Pontzer CH, Johnson HM. Differential recognition of the type I interferon receptor by interferons τ and α is responsible for their disparate cytotoxicities. Proc Natl Acad Sci USA 1995;92:12270-12274.

  30. Ott TL, Mirando Ma, Davis MA, Bazer FW. Effects of ovine conceptus secretory proteins and progesterone on oxytocin-stimulated endometrial production of prostaglandin and turnover of inositol phosphate in ovariectomized ewes. J Reprod Fertil 1992;95:19-29.

  31. Johnson GA, Spencer TE, Burghardt RC, Joyce MM, Bazer FW. Interferon-Tau and progesterone regulate ubiquitin cross-reactive protein expression in the ovine uterus. Biol Reprod 2000;62:622-627.

  32. Asselin E, Johnson GA, Spencer TE, Bazer FW. Monocyte Chemotactic protein-1 and –2 messenger ribonucleic acids in the ovine uterus: regulation by pregnancy, progesterone, and interferon-τ. Biol Reprod 2001;64:992-1000.

  33. Fortin M, Oullete MJ, Lambert RD. TGFβ2 and PGE2 in rabbit blastocoelic fl uid can modulate GM-CSF pro-duction by human lymphocytes. Am J Reprod Immu-nol 1997;38:129-139.

  34. Emond V, Fortier Ma, Murphy BD, Lambert RD. Prostaglandin E2 regulates both interleukin-2 and granulocyte-macrophage colony stimulating factor gene expression in bovine lymphocytes. Biol Reprod 1998;58:143-151.

  35. Winkelman GL, Roberts MR, Peterson AJ, Alexenko AP, Ealy AD. Identifi cation of the expressed forms of ovine interferon-tau in the periimplantation concep-tus: sequence relationships and comparative biological activities. Biol Reprod 1999;61:1592-1600.

  36. Ealy AD, Larson SF, Liu L, Alexenko AP, Winkelman GL, Kubisch HM, et al. Polymorphic forms of expressed bovine interferon-τ genes: relative transcript abun-dance during early placental development, promoter sequences of genes and biological activity of protein products. Endocrinology 2001;7:2906-2915.

  37. Cann CH, Fairclough RJ, Sutton R, Gow CB. Endo-metrial expression of mRNA encoding insuline-like growth factors I and II and IGF-binding proteins 1 and 2 in early pregnant ewes. J Reprod Fertil 1997;111:7-13.

  38. Reynolds TS, Stevenson KR, Wathes DC. Pregnancy-specifi c alterations in the expression of the insuline-like growth factor system during early placental develop-ment in the ewe. Endocrinology 1997;138:886-897.

  39. Wathes DC, Reynolds TS, Robinson RS, Stevenson KR. Role of the insuline-like growth factor system in uter-ine function and placental development in ruminants. J Dairy Sci 1998;81:1778-1789.

  40. Vogiagis D, Fry RC, Sanderman RM, Salomonsen LA. Leukaemia inhibitory factor in endometrium during the oestrous cycle, early pregnancy and in ovariectomized steroid-treated ewes. J Reprod Fertil 1997;109:279-288.

  41. Flores JM, Sanchez MA, Garcia P, Sanchez B, Nieto A. Immunohistochemical localization of epidermal growth, transforming growth factor-α and growth factor-β in the caprine peri-implantation period. The-riogenology 1998;50:931-944.

  42. Dinarello CA. The interleukin-1 family : 10 years of dis-covery. FASEB J 1994;8:1314-1325.

  43. Arend WP. Interleukin 1 receptor antagonist. A new member of the interleukin 1 family. J Clin Invest 1991;88:1445-1451.

  44. Paula-Lopes FF, de Moraes AA, Edwards JL, Justice JE, Hansen PJ. Regulation of preimplantation develop-ment of bovine embryos by interleukin-1β. Biol Reprod 1998;59:1406-1412.

  45. Asselin E, Johnson GA, Spencer TE, Bazer FW. Monocyte chemotactic protein-1 and –2 messenger ribonucleic acids in the ovine uterus: regulation by pregnancy, progesterone, and interferon-τ. Biol Reprod 2001;64:992-1000.

  46. Gupta A, Ing NH, Bazer FW, Bustamante LS, Jaeger LA. Beta transforming growth factors (TGFβ) at the porcine conceptus-maternal interface. Part 1: expres-sion of TGFβ1, TGFβ2 and TGFβ3 messenger ribonu-cleic acids. Biol Reprod 1998;59:905-910.

  47. Gupta A, Bazer FW, Jaeger LA. Differential expresión of beta transforming growth factors (TGFβ1, TGFβ2 and TGFβ3) and their receptors (Type I and Type II) in peri-implantation porcine conceptuses. Biol Reprod 1996;56:796-802.

  48. Van Obberghen-Schilling E, Roche NS, Flanders NS, Sporn MB, Roberts AB. Transforming growth factor-beta 1 positively regulates its own expression in normal and transformed cells. J Biol Chem 1988;263:7741-7746.

  49. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol 1990;6:597-641.

  50. Gupta A, Dekaney CM, Bazer FW, Madrigal MM. Beta transforming growth factors (TGFβ) at the porcine conceptus-maternal interface. Part II: Uterine TGFβ bioactivity and expression of immunoreactive TGFβs (TGFβ1, TGFβ2, and TGFβ3) and their receptors (Type I and Type II). Biol Reprod 1998;59:911-917.

  51. Fazleaba AT, Strakova Z. Endometrial functions: cell specifi c changes in the uterine enviroment. Mol Cell Endocrinol 2002;186:143-147.

  52. Jaeger LA, Johnson GA, Ka H, Garlow JG, Burghardt RC, Spencer TE et al. Functional analysis of autocrine and paracrine signalling at the uterine-conceptus interface in pigs. Reproduction 2001;58(Suppl 1):191-207.

  53. Modric T, Kowalski AA, Green ML, Simmen RC, Simmen FA. Pregnancy-dependant expression of leukaemia inhibitory factor (LIF), LIF receptor-beta and interleukin-6 (IL-6) messenger ribonucleic acids in the porcine female reproductive tract. Placenta 2000;21;345-353.

  54. Chabot V, Lambert RD, Laforest JP, St-Jacques S, Matte JJ, Guay F et al. Effect of oestrous cycle and early pregnancy on uterine production and expression of immune regulatory factors in gilts. Anim Reprod Sci 2004;81:137-149.

  55. Lennard SN, Stewart F, Allen WR. Insulin-like growth factor II gene expression in the fetus and placenta of the horse during the fi rst half of gestation. J Reprod Fertil 1995;103:169-179.

  56. Herrler A, Pell JM, Allen WR, Beier HM, Stewart F. Horse conceptuses secrete insuline-like growth factor-binding protein 3. Biol Reprod 2000;62:1804-1811.

  57. Lennard SN, Stewart F, Allen WR. Transforming growth factor β 1 expression in the endometrium of the mare during placentation. Mol Reprod Dev 1995;42:131-140.

  58. Gruning G, Antczak DF. Horse trophoblast produce tumor necrosis factor α but not interleukin 2, interleu-kin 4, or interferon γ. Biol Reprod 1995;52:531-539.

  59. Evans JM, Anderton DJ. Pregnancy diagnosis in the bitch: the development of a test based on the measure-ment of acute phase proteins in the blood. Ann Zoo-tech 1992;41:397-405.

  60. Yamashita K, Fujinaga T, Miyamoto T, Hagio T, Izumi-sawa Y, Kotani T. Canine acute phase response: rela-tionship between serum cytokine activity and acute phase protein in dogs. J Vet Med Sci 1994;56:487-492.

  61. Surveyor GA, Wilson AK, Brigstock DR. CTGF in the mouse uterus and early embryo. Biol Reprod 1998;59:1207-1213.

  62. Vogiagis D, Salomonsen LA. Review: the role of leu-kaemia inhibitory factor in the establishment of preg-nancy. J Endocrinol 1999;160:181-190.

  63. Chen JR, Gang-Cheng J, Shatzer T. Leukemia inhibi-tory factor can substitute for nidatiry estrogen and is essential to inducing a receptive uterus for implanta-tion but is not essential for subsequent embryogenesis. Endocrinology 2000;12:4365-4372.

  64. Liu CQ, Yuan Y, Wang ZX. Effects of leukaemia inhibi-tory factor on endometrial receptivity and its hormonal regulation in rabbits. Cell Biol Int 2001;25:1029-1032.

  65. Reese J, Binart N, Brown N. Implantation and Decidu-alization defects in prolactin receptor (PRLR)- deficient mice are mediated by ovarian but not uterine PRLR . Endocrinology 2000;5:1872-1881.

  66. Tan J, Paria BC, Dey SK, Das SK. Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 1999;140:5310-5321.

  67. Das SK, Chakraborty I, Paria BC, Wang XN, Plowman G, Dey SK. Amphiregulin is an implantation-specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol 1995;9:691-705.

  68. Raab G, Kover K, Paria BC, Dey SK, Ezzel RM. Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor. Development 1996;122:637-645.

  69. Paria BC, Elenius K, Klagsbrun M, Dey SK. Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently on ErbB1: a posible role for heparin sulfate proteoglycans and ErbB4 in blastocyst. Implantation. Development 1999;126:1997-2005.

  70. Klonisch T, Wolf P, Hombach-Klonisch S. Epidermal growth factor-like ligands and erbB genes in the peri-implantation rabbit uterus and blastocyst. Biol Reprod 2001;64:1835-1844.

  71. Breard E, Benhaim A, Feral C, Leymarie P. Role of IL-6 in rabbit ovary. J Endocrinol 1998;159:479-487.

  72. Kurago ZB, Lutz CT, Smith KD, Colonna M. NK cell natural cytotoxicity and IFN-gamma production are not always coordinately regulated: engagment of DX9 KIR + NK cells by HLA-B/ variants and target cells. J Immunol 1998;160:1573-1580.

  73. Boehm U, Klamp M, Howard JC. Cellular responses to interferon-gamma. Annu Rev Immunol 1997;15:749-795.

  74. Ashkar AA, Di Santo JP, Croy BA. Interferon con-tributes initiation of uterine vascular modifi cation, decidual integrity, and uterine natural killer cell mat-uration during normal murin pregnancy. J Exp Med 2000;192:259-269.

  75. Wang C, Umesaki N, Nakamura H, Tanaka T, Nakatani K, Sakaguchi I et al. Expression of vascular endothe-lial growth factor by granulated metrial gland cells in pregnant murine uteri. Cell Tissue Res 2000;300:285-293.

  76. Ashkar AA, Anne B. Functions of uterine natural killer cells are mediated by interferon gamma pro-duction during murine pregnancy. Semin Immunol 2001;13:235-241.

  77. Surveyor GA, Wilson AK, Brigstock DR. CTGF in the mouse uterus and early embryo. Biol Reprod1998;59:1207-1213.

  78. Dvorak P, Flechon JE, Thompson EM, Horak V, Adenot P, Renard JP. Embryoglycans regulate FGF-2 mediated mesoderm induction in the rabbit embryo. J Cell Sci-ence 1997;110:1101-1110.

  79. Knobil E, Neill JD. The Phisiology of Reproduction. 2a ed. New York:Raven Press Ltd 1994.

  80. Chi MM, Schelein Al, Moley KH. High insuline like growth factor-I (IGF-I) and insulin concentra-tions trigger apoptosis in the mouse blastocyst via down-regulation of the igf-1 receptor. Endocrinology 2000;141:4784-4792.

  81. Nason KS, Binder ND, Labarta JI, Gargasky SE. IGF-II and IGF-binding proteins increase dramatically during rabbit pregnancy. J Endocrinol 1996;148:121-130.

  82. Sherwin J, Freeman T, Stephens R, Kimber S, Smith A, Chambers I et al. Identifi cation of genes regulated by leukaemia inhibitory factor in the mouse uterus at the time of implantation. Mol Endocrinol 2004;18:2185-2195.

  83. Krussel JS, Bielfeld P, Poland MP, Simon C. Regula-tion of embryonic implantation. Eur J Obstet Gynecol Reprod Biol 2003;110:2-9.

  84. Wolf E, Arnold GJ, Bauersachs S, Beier HM, Blum H, Einspanier R et al. Embryo-maternal communication in bovine-strategies for deciphering a complex cross-talk. Reprod Domest Anim 2003;38:276-289.

  85. Diaz-Cueto L, Gerton GL. The infl uence of growth factors on the development of preimplantation mam-malian embryos. Arch Med Res 2001; 32:619-626.

  86. Hansen PJ, Soto P, Natzke RP. Mastitis and fertil-ity in cattle-possible involvement of infl ammation or immune activation in embryonic mortality. Am J Reprod Immunol 2004;51:294-301.




2020     |     www.medigraphic.com