Immunohistochemical localization of leukemia inhibitory factor, interleukins 1 and 6 at the primary implantation site in the rhesus monkey

Cytokine

Volumn 24, Issue 6, 2003, Pages 277-285

  Sengupta, Jayasree ^a   Dhawan, Latika ^a   Ghosh, D ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

IL 1; IL 6; Implantation site; LIF; Rhesus monkey

Indexed keywords

INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHORION VILLUS; CYTOTROPHOBLAST; EMBRYO; EPITHELIUM CELL; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MESENCHYME CELL; NIDATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RHESUS MONKEY; SMOOTH MUSCLE FIBER; TROPHOBLAST; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

MACACA MULATTA;

EID: 0242594535     PISSN: 10434666     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cyto.2003.08.010     Document Type: Article

References (70)

1. Finn C.A. Implantation, menstruation and inflammation. Biol Rev Camb Philos Soc. 61:1986;313-328.
2. Ghosh D., Sengupta J. Recent developments in endocrinology and paracrinology of blastocyst implantation in the primates. Hum Reprod Update. 4:1998;153-168.
3. Simon C., Moreno C., Remohi J., Pellicer A. Cytokines and embryo implantation. J Reprod Immunol. 39:1998;117-131.
4. Kauma S.W. Cytokines in implantation. J Reprod Fertil (Suppl.). 55:2000;31-42.
5. Das C., Kumar V.S., Gupta S., Kumar S. Network of cytokines, integrins and hormones in human trophoblast cells. J Reprod Immunol. 53:2002;257-268.
6. Lindhard A., Bentin-Ley U., Ravn V., Islin H., Hviid T., Rex S., et al. Biochemical evaluation of endometrial function at the time of implantation. Fertil Steril. 78:2002;221-233.
7. Hendrickx A.G., Houston M.L. Description of stages IV, V, VI, VII, and VIII. Hendrickx A.G. Embryology of the baboon. 1976;53-57 The University of Chicago, Chicago, U.S.A.
8. Enders A.C. Overview of the morphology of implantation in primates. Wolff D.P., et al. In vitro fertilization and embryo transfer in the primates. 1993;145-157 Springer-Verlag, New York, U.S.A.
9. Sunder S., Lenton E.A. Endocrinology of the peri-implantation period. Baillieres Best Pract Res Clin Obstet Gynaecol. 14:2000;789-800.
10. Hilton D.J., Gough N.M. Leukemia inhibitory factor: a biological perspective. J Cell Biochem. 46:1991;21-26.
11. Bischof P., Martelli M., Campana A., Itoh Y., Ogata Y., Nagase H. Importance of matrix metalloproteinases in human trophoblast invasion. Early Pregnancy. 1:1995;263-269.
12. Nachtigall M.J., Kliman H.J., Feinberg R.F., Olive D.L., Engin O., Arici A. The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J Clin Endocrinol Metab. 81:1996;801-806.
13. Licht P., Russu V., Wildt L. On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: implications for differentiation and implantation. Semin Reprod Med. 19:2001;37-47.
14. Sawai K., Matsuzaki N., Kameda T., Hashimoto K., Okada T., Shimoya K., et al. Leukemia inhibitory factor produced at the fetomaternal interface stimulates chorionic gonadotropin production: its possible implication during pregnancy, including implantation period. J Clin Endocrinol Metab. 80:1995;1449-1456.
15. Harvey M.B., Leco K.J., Arcellana-Panlilio M.Y., Zhang X., Edwards D.R., Schultz G.A. Proteinase expression in early mouse embryos is regulated by leukemia inhibitory factor and epidermal growth factor. Development. 121:1995;1005-1014.
16. Varghese S., Yu K., Canalis E. Leukemia inhibitory factor and oncostatin M stimulate collagenase-3 expression in osteoblasts. Am J Physiol. 276:1999;E465-E471.
17. Damiens C., Fortun Y., Charrier C., Heymann D., Padrines M. Modulation by soluble factors of gelatinase activities released by osteoblastic cells. Cytokine. 12:2000;1727-1731.
18. Cullinan E.B., Abbondanzo S.J., Anderson P.S., Pollard J.W., Lessey B.A., Stewart C.L. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc Natl Acad Sci U S A. 93:1996;3115-3120.
19. Lass A., Weiser W., Munafo A., Loumaye E. Leukemia inhibitory factor in human reproduction. Fertil Steril. 76:2001;1091-1096.
20. Laird S.M., Tuckerman E.M., Dalton C.F. The production of leukemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture. Hum Reprod. 12:1997;569-574.
21. Hambartsoumian E. Endometrial leukemia inhibitory factor (LIF) as a possible cause of unexplained infertility and multiple failures of implantation. Am J Reprod Immunol. 39:1998;137-143.
22. Yue Z.P., Yang Z.M., Wei P., Li S.J., Wang H.B., Tan J.H., et al. Leukemia inhibitory factor, leukemia inhibitory factor receptor, and glycoprotein 130 in rhesus monkey uterus during menstrual cycle and early pregnancy. Biol Reprod. 63:2000;508-512.
23. Mitchell M.H., Swanson R.J., Oehninger S. In vivo effect of leukemia inhibitory factor (LIF) and an anti-LIF polyclonal antibody on murine embryo and fetal development following exposure at the time of transcervical blastocyst transfer. Biol Reprod. 67:2002;460-464.
24. Piccinni M.P., Scaletti C., Vultaggio A., Maggi E., Romagnani S. Defective production of LIF, M-CSF and Th2-type cytokines by T cells at fetomaternal interface is associated with pregnancy loss. J Reprod Immunol. 52:2001;35-43.
25. Simon C., Frances A., Lee B.Y., Mercader A., Huynh T., Remohi J., et al. Immunohistochemical localization, identification and regulation of the interleukin-1 receptor antagonist in the human endometrium. Hum Reprod. 10:1995;2472-2477.
26. De los Santos M.J., Mercader A., Frances A., Portoles E., Remohi J., Pellicer A., et al. Role of endometrial factors in regulating secretion of components of the immunoreactive human embryonic interleukin-1 system during embryonic development. Biol Reprod. 54:1996;563-574.
27. Arici A., Engin O., Attar E., Olive D.L. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. J Clin Endocrinol Metab. 80:1995;1908-1915.
28. Elias J.A., Zheng T., Whiting N.L., Marcovici A., Trow T.K. Cytokine-cytokine synergy and protein kinase C in the regulation of lung fibroblast leukemia inhibitory factor. Am J Physiol. 266:1994;L426-L435.
29. Sawai K., Matsuzaki N., Okada T., Shimoya K., Koyama M., Azuma C., et al. Human decidual cell biosynthesis of leukemia inhibitory factor: regulation by decidual cytokines and steroid hormones. Biol Reprod. 56:1997;1274-1280.
30. Ghosh D., Dhara S., Kumar A., Sengupta J. Immunohistochemical localization of receptors for progesterone and oestradiol-17β in the implantation site of the rhesus monkey. Hum Reprod. 14:1999;505-514.
31. Ishihara O., Khan H., Sullivan M.H., Elder M.G. Interleukin-1 beta stimulates decidual stromal cell cyclo-oxygenase enzyme and prostaglandin production. Prostaglandins. 44:1992;43-52.
32. Ishihara O., Numari H., Saitoh M., Arai Y., Takanashi H., Kitagawa H., et al. Prostaglandin E2 production by endogenous secretion of interleukin-1 in decidual cells from term fetal membrane. Adv Exp Med Biol. 433:1997;419-422.
33. Kennard E.A., Zimmerman P.D., Friedman C.I., Kniss D.A. Interleukin-1β induces cyclooxygenase-2 in cultured human decidual cells. Am J Reprod Immunol. 34:1995;65-71.
34. Rauk P.N., Chiao J.P. Interleukin-1 stimulates human uterine prostaglandin production through induction of cyclooxygenase-2 expression. Am J Reprod Immunol. 43:2000;152-159.
35. Lala P.K., Kearns M., Parhar R.S., Scodras J., Johnson S. Immunological role of the cellular constituents of the decidua in the maintenance of semiallogeneic pregnancy. Ann N Y Acad Sci. 476:1986;183-205.
36. Strakova Z., Srisuparp S., Fazleabas A.T. Interleukin-1β induces the expression of insulin-like growth factor binding protein-1 during decidualization in the primate. Endocrinology. 141:2000;4664-4670.
37. Lebovic D.I., Bentzien F., Chao V.A., Garrett E.N., Meng Y.G., Taylor R.N. Induction of an angiogenic phenotype in endometriotic stromal cell cultures by interleukin-1β Mol Hum Reprod. 6:2000;269-275.
38. Jung Y.D., Liu W., Reinmuth N., Ahmad S.A., Fan F., Gallick G.E., et al. Vascular endothelial growth factor is upregulated by interleukin-1 beta in human vascular smooth muscle cells via the P38 mitogen-activated protein kinase pathway. Angiogenesis. 4:2001;155-162.
39. Coxon A., Bolon B., Estrada J., Kaufman S., Scully S., Rattan A., et al. Inhibition of interleukin-1 but not tumor necrosis factor suppresses neovascularization in rat models of corneal angiogenesis and adjuvant arthritis. Arthritis Rheum. 46:2002;2604-2612.
40. Salven P., Hattori K., Heissig B., Rafii S. Interleukin-1α promotes angiogenesis in vivo via VEGFR-2 pathway by inducing inflammatory cell VEGF synthesis and secretion. FASEB J. 16:2002;1471-1473.
41. Simon C., Gimeno M.J., Mercader A., O'Connor J.E., Remoti J., Polan M.L., et al. Embryonic regulation of integrins β3, α4, and α1 in human endometrial epithelial cells in vitro. J Clin Endocrinol Metab. 82:1997;2607-2616.
42. Matsumoto K., Nakamura T. Emerging multipotent aspects of hepatocyte growth factor. J Biochem. 119:1996;591-600.
43. Stella M.C., Comoglio P.M. HGF: a multifunctional growth factor controlling cell scattering. Int J Biochem Cell Biol. 31:1999;1357-1362.
44. Kataoka H., Shimomura T., Kawaguchi T., Hamasuna R., Itoh H., Kitamura N., et al. Hepatocyte growth factor activator inhibitor type 1 is a specific cell surface binding protein of hepatocyte growth factor activator (HGFA) and regulates HGFA activity in the pericellular microenvironment. J Biol Chem. 275:2000;40453-40462.
45. Kataoka H., Meng J.Y., Itoh H., Hamasuna R., Shimomura T., Suganuma T., et al. Localization of hepatocyte growth factor activator inhibitor type 1 in Langhans' cells of human placenta. Histochem Cell Biol. 114:2000;469-475.
46. Bischof P., Meisser A., Campana A. Mechanisms of endometrial control of trophoblast invasion. J Reprod Fertil (Suppl.). 55:2000;65-71.
47. Simon C., Frances A., Piquette G.N., el Danasouri I., Zurawski G., Dang W., et al. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology. 134:1994;521-528.
48. Laird S.M., Tuckerman E., Li T.C., Bolton A.E. Stimulation of human endometrial epithelial cell interleukin 6 production by interleukin 1 and placental protein 14. Hum Reprod. 9:1994;1339-1343.
49. Tabibzadeh S., Kong Q.F., Babaknia A., May L.T. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum Reprod. 10:1995;2793-2799.
50. Tabibzadeh S.S., Santhanam U., Sehgal P.B., May L.T. Cytokine-induced production of IFN-β 2/IL-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17 β J Immunol. 142:1989;3134-3139.
51. Girasole G., Jilka R.L., Passeri G., Boswell S., Boder G., Williams D.C. 17 Beta-estradiol inhibits interleukin-6 production by bone marrow-derived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens. J Clin Invest. 89:1992;883-891.
52. Ray A., Zhang D.H., Siegel M.D., Ray P. Regulation of interleukin-6 gene expression by steroids. Ann N Y Acad Sci. 762:1995;79-87.
53. De M., Sanford T.R., Wood G.W. Expression of interleukin 1, interleukin 6 and tumour necrosis factor alpha in mouse uterus during the peri-implantation period of pregnancy. J Reprod Fertil. 97:1993;83-89.
54. Ammala M., Nyman T., Strengell L., Rutanen E.M. Effect of intrauterine contraceptive devices on cytokine messenger ribonucleic acid expression in the human endometrium. Fertil Steril. 63:1995;773-778.
55. Sharkey A.M., Dellow K., Blayney M., Macnamee M., Charnock-Jones S., Smith S.K. Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos. Biol Reprod. 53:1995;974-981.
56. Tseng J.F., Ryan I.P., Milam T.D., Murai J.T., Schriock E.D., Landers D.V., et al. Interleukin-6 secretion in vitro is up-regulated in ectopic and eutopic endometrial stromal cells from women with endometriosis. J Clin Endocrinol Metab. 81:1996;1118-1122.
57. Smith S.K., Charnock-Jones D.S., Sharkey A.M. The role of leukemia inhibitory factor and interleukin-6 in human reproduction. Hum Reprod. 13: (Suppl 3):1998;237-246.
58. Salamonnsen L.A., Dimitriadis E., Robb L. Cytokines in implantation. Semin Reprod Med. 18:2000;299-310.
59. Basak S., Dubanchet S., Zourbas S., Chaouat G., Das C. Expression of pro-inflammatory cytokines in mouse blastocysts during implantation: modulation by steroid hormones. Am J Reprod Immunol. 47:2002;2-11.
60. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., et al. Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature. 359:1992;76-79.
61. Kopf M., Baumann H., Freer G., Freudenberg M., Lamers M., Kishimoto T., et al. Impaired immune and acute-phase responses in interleukin-6 deficient mice. Nature. 368:1994;339-342.
62. Ernst M., Inglese M., Waring P., Campbell I.K., Bao S., Clay F.J., et al. Defective gp130-mediated signal transducer and activator of transcription (STAT) signalling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med. 194:2001;189-203.
63. Cheng J.G., Chen J.R., Hernandez L., Alvord W.G., Stewart C.L. Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. Proc Natl Acad Sci U S A. 98:2001;8680-8685.
64. Ghosh D., Sengupta J., Hendrickx A.G. Effect of single-dose, early luteal phase administration of mifepristone (RU486) on implantation stage endometrium in the rhesus monkey. Hum Reprod. 11:1996;2026-2035.
65. Ghosh D., Stewart D.R., Nayak N.R., Lasley B.L., Overstreet J.W., Hendrickx A.G., et al. Serum concentrations of oestradiol-17β, progesterone, relaxin and chorionic gonadotrophin during blastocyst implantation in natural pregnancy cycle and in embryo transfer cycle in the rhesus monkey. Hum Reprod. 12:1997;914-920.
66. Ghosh D., Sharkey A.M., Charnock-Jones D.S., Dhawan L., Dhara S., Smith S.K., et al. Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) in conceptus and endometrium during implantation in the rhesus monkey. Mol Hum Reprod. 6:2000;935-941.
67. Dhara S., Lalitkumar P.G.L., Sengupta J., Ghosh D. Immunohistochemical localization of insulin-like growth factors I and II at the primary implantation site in the Rhesus monkey. Mol Hum Reprod. 7:2001;365-371.
68. Blankenship T.N., Enders A.C. Expression of platelet-endothelial cell adhesion molecule-1 (PECAM) by macaque trophoblast cells during invasion of the spiral arteries. Anat Rec. 247:1997;413-419.
69. Sengupta J., Ghosh D. Blastocyst-endometrium interaction at implantation in the rhesus monkey. J Reprod Immunol. 53:2002;227-239.
70. Robertson W.B. The endometrium. 1981;7-44 Butterworths, London, U.K.