Role of leukemia inhibitor factor (LIF) in decidualisation of murine uterine stromal cells in vitro

Journal of Endocrinology

Volumn 181, Issue 3, 2004, Pages 477-492

  Fouladi Nashta, A A ^a,d   Andreu, C V ^a,c   Nijjar, N ^a   Heath, J K ^b   Kimber, Susan J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; INDOMETACIN; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; MESSENGER RNA; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREEDING; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; DECIDUALIZATION; ENZYME ACTIVITY; ENZYME REPRESSION; FEMALE; FETAL CALF SERUM; HORMONE RECEPTOR INTERACTION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; STROMA CELL; UTERUS;

ALKALINE PHOSPHATASE; ANIMALS; CELLS, CULTURED; DECIDUA; DINOPROSTONE; FEMALE; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED STRAINS; MOLECULAR CHAPERONES; PREGNANCY; PROTEINS; RECEPTORS, CYTOKINE; RECEPTORS, OSM-LIF; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UTERUS;

EID: 3042850568     PISSN: 00220795     EISSN: None     Source Type: Journal    
DOI: 10.1677/joe.0.1810477     Document Type: Article

References (82)

1. Abrahamsohn PA & Zorn TM 1993 Implantation and decidualization in rodents. Journal of Experimental Zoology 266 603-628.
2. Ansell JD, Barlow PW & McLaren A 1974 Binucleate and polyploid cells in the decidua of the mouse. Journal of Embryology and Experimental Morphology 31 223-227.
3. Arnold JT, Kaufman DG, Seppala M & Lessey BA 2001 Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Human Reproduction 16 836-845.
4. Aubert J, Dessolin S, Belmonte N, Li M, McKenzie FR, Staccini L, Villageois P, Barhanin B, Vernallis A, Smith AG et al. 1999 Leukemia inhibitory factor and its receptor promote adipocyte differentiation via the mitogen-activated protein kinase cascade. Journal of Biological Chemistry 274 24965-24972.
5. Bany BM & Kennedy TG 1999 Role of interleukin 1 in the regulation of cyclooxygenase gene expression in rat endometrial strmal cells. Journal of Reproduction and Fertility 115 125-131.
6. Bany BM, Zhang X & Kennedy TG 1998 Effects of epidermal growth factor and interleukin-1 alpha on plasminogen activator secretion and decidualization in rat endometrial stromal cells. Biology of Reproduction 59 131-135.
7. Benson GV, Lim H, Paria BC, Satokata I, Dey SK & Maas RL 1996 Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122 2687-2696.
8. Bhatt H, Brunet LJ & Stewart CL 1991 Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. PNAS 88 11408-11412.
9. Bucci M & Murphy CR 1995 Alkaline phosphatase distribution in the plasma membrane of uterine epithelial cells is markedly altered during early pregnancy in the rat. Cell Biology International 19 921-928.
10. Buxton LE & Murdoch RN 1980 Behaviour and properties of membrane-bound mouse uterine alkaline phosphatase during early pregnancy. Australian Journal of Biological Sciences 33 539-548.
11. Chakraborty I, Das SK, Wang J & Dey SK 1996 Developmental expression of the cyclo-oxygenase-1 and cyclo-oxygenase-2 genes in the peri-implantation mouse uterus and their differential regulation by the blastocyst and ovarian steroids. Journal of Molecular Endocrinology 16 107-122.
12. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L & Stewart CL 2000 Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 141 4365-4372.
13. Cheng JG, Chen JR, Hernandez L, Alvord WG & Stewart CL 2001 Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. PNAS 98 8680-8685.
14. Cheng JG, Rodriguez CI & Stewart CL 2002 Control of uterine receptivity and embryo implantation by steroid hormone regulation of LIF production and LIF receptor activity: towards a molecular understanding of 'the window of implantation'. Reviews in Endocrine and Metabolic Disorders 3 119-126.
15. 2 enhances uterine stromal cell alkaline phosphatase activity in vitro. Prostaglandins 33 241-252.
16. Evans CA, Kennedy TG, Patrick JE & Challis JR 1982 The effects of indomethacin on uterine activity and prostaglandin (PG) concentrations during labor induced by administering ACTH to fetal sheep. Canadian Journal of Physiology and Pharmacology 60 1200-1209.
17. Finn CA 1966 Endocrine control of endometrial sensitivity during the induction of the decidual cell reaction in the mouse. Journal of Endocrinology 36 239-248.
18. Finn CA & McLaren A 1967 A study of the early stages of implantation in mice. Journal of Reproduction and Fertility 13 259-267.
19. Fox NW, Damjanov I, Knowles BB & Solter D 1984 Stage-specific embryonic antigen 3 as a market of visceral extraembryonic endoderm. Developmental Biology 103 263-266.
20. 2 enhances human endometrial stromal cell differentiation. Endocrinology 134 258-263.
21. Gambel P, Rossant J, Hunziker RD & Wegmann TG 1985 Origin of decidual cells in murine pregnancy and pseudopregnancy. Transplantation 39 443-445.
22. Gearing DP, Thut CJ, VandeBos T, Gimpel SD, Delaney PB, King J, Price V, Cosman D & Beckmann MP 1991 Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO Journal 10 2839-2848.
23. Gearing DP, VandenBos T, Beckmann MP, Thut CJ, Comeau MR, Mosley B & Ziegler SF 1992 Reconstitution of high affinity leukaemia inhibitory factor (LIF) receptors in haemopoietic cells transfected with the cloned human LIF receptor. Ciba Foundation Symposium 167 245-255.
24. Gendron RL, Paradis H, Hsieh-Li HM, Lee DW, Potter SS & Markoff E 1997 Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biology of Reproduction 56 1097-1105.
25. Glasser SK & McCormack SA 1979 Estrogen-modulated uterine gene transcription in relation to decidualization. Endocrinology 104 1112-1118.
26. Glasser SR & Julian J 1986 Intermediate filament protein as a marker of uterine stromal cell decidualization. Biology of Reproduction 35 463-474.
27. Glasser SR, Lampelo S, Munir MI & Julian J 1987 Expression of desmin, laminin and fibronectin during in situ differentiation (decidualization) of rat uterine stromal cells. Differentiation 35 132-142.
28. Granstrom E & Kindahl H 1983 Assay methods for prostaglandins and related compounds. Advances in Prostaglandin, Thromboxane, and Leukotriene Research 11 173-179.
29. Haines BP, Voyle RB & Rathjen PD 2000 Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Molecular Biology of the Cell 11 1369-1383.
30. 2 to rats sensitized for the decidual cell reaction. Biology of Reproduction 50 757-764.
31. Hudson KR, Vernallis AB & Heath JK 1996 Characterization of the receptor binding sites of human leukemia inhibitory factor and creation of antagonists. Journal of Biological Chemistry 271 11971-11978.
32. Inaba T, Wiest WG, Strickler KC & Mori J 1988 Augmentation of the response of mouse uterine epithelial cells to estradiol by uterine stroma. Endocrinology 123 1253-1258.
33. 2 alpha secretion by uterine stromal cells in vitro. Endocrinology 132 300-308.
34. Johansson S & Wide M 1994 Changes in the pattern of expression of alkaline phosphatase in the mouse uterus and placenta during gestation. Anatomy and Enbryology 190 287-296.
35. Jones CJ, Aplin JD, Mulholland J & Glasser SR 1993 Patterns of sialylation in differentiating rat decidual cells as revealed by lectin histochemistry. Journal of Reproduction and Fertility 99 635-645.
36. Jones CJ, Kimber SJ, Illingworth I & Aplin JD 1996 Decidual sialylation shows species-specific differences in the pregnant mouse and rat. Journal of Reproduction and Fertility 106 241-250.
37. Kennedy TG 1985 Evidence for the involvement of prostaglandins throughout the decidual cell reaction in the rat. Biology of Reproduction 33 140-146.
38. Kennedy TG 1986 Intrauterine infusion of prostaglandins and decidualization in rats with uteri differentially sensitized for the decidual cell reaction. Biology of Reproduction 34 327-335.
39. Kennedy TG & Lukash LA 1982 Induction of decidualization in rats by the intrauterine infusion of prostaglandins. Biology of Reproduction 27 253-260.
40. Kennedy TG & Doktorcik PE 1988 Effects of analogues of prostaglandin E2 and F2 alpha on the decidual cell reaction in the rat. Prostaglandins 35 207-219.
41. Kennedy TG & Ross HE 1993 Effect of prostaglandin E2 on rate of decidualization in rats. Prostaglandins 46 243-250.
42. Kennedy TG & Ross HE 1997 Temporal- and hormone-dependent changes in uterine sensitization for the decidual cell reaction and decidualization in vitro of rat endometrial stromal cells. Journal of Reproduction and Fertility 109 129-136.
43. Kennedy TG, Ross HE, Bathe GJ, Shu MA & Zhang X 1998 Secretion of plasminogen activator by cultured rat endometrial stromal cells from uteri differentially sensitized for the decidual cell reaction. Molecular Reproduction and Development 49 268-276.
44. Kikuchi H, Sugiyama S & Imajoh-Ohmi S 1995 A novel anti-apoptosis serum factor that down-regulates fas-mediated apoptosis. Journal of Biochemistry (Tokyo) 117 936-939.
45. Kimber SJ, Lindenberg S & Lundblad A 1988 Distribution of some Gal beta 1-3(4)GlcNAc related carbohydrate antigens on the mouse uterine epithelium in relation to the peri-implantational period. Journal Reproduction and Immunology 12 297-313.
46. Kurita T, Lee K, Saunders PT, Cooke PS, Taylor JA, Lubahn DB, Zhao C, Makela S, Gustafsson JA, Dahiya R & Cunha GR 2001 Regulation of progesterone receptors and decidualization in uterine stroma of the estrogen receptor-alpha knockout mouse. Biology of Reproduction 64 272-283.
47. Lim H & Dey SK 1997 Prostaglandin E2 receptor subtype EP2 gene expression in the mouse uterus coincides with differentiation of the luminal epithelium for implantation. Endocrinology 138 4599-4606.
48. Lim H, Gupta RA, Ma WG, Paria BC, Moller DE, Morrow JD, DuBois RN, Trzaskos JM & Dey SK 1999 Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARdelta. Genes and Developmennt 13 1561-1574.
49. Malaval L, Gupta AK & Aubin JE 1995 Leukemia inhibitory factor inhibits osteogenic differentiation in rat calvaria cell cultures. Endocrinology 136 1411-1418.
50. McCormack SA & Glasser SR 1980 Differential response of individual uterine cell types from immature rats treated with estradiol. Endocrinology 106 1634-1649.
51. Milligan SR, Cohen PE & Finn CA 1995 The minimum requirements for oestradiol to induce uterine sensitivity for implantation and decidualization in mice. Human Reproduction 10 1502-1506.
52. Monice FL, Andrade CG, Abrahamsohn PA, Soto-Suazo M, Oliveira SF & Zorn TM 2001 Granulated decidual cells in the mouse deciduoma: a putative source of decidual prolactin in mice. Cells, Tissues, Organs 168 252-263.
53. Murdoch RN, Kay DJ & Cross M 1978 Activity and subcellular distribution of mouse uterine alkaline phosphatase during pregnancy and pseudopregnancy. Journal of Reproduction and Fertility 54 293-300.
54. Ni H, Ding NZ, Harper MJ & Yang ZM 2002a Expression of leukemia inhibitory factor receptor and gp130 in mouse uterus during early pregnancy. Molecular Reproduction and Development 63 143-150.
55. Ni H, Sun T, Ding NZ, Ma XH & Yang ZM 2002b Differential expression of microsomal prostaglandin e synthase at implantation sites and in decidual cells of mouse uterus. Biology of Reproduction 67 351-358.
56. O'Neill C 1985 Partial characterization of the embryo-derived platelet-activating factor in mice. Journal of Reproduction and Fertility 75 375-380.
57. Pakrasi PL 1997 Prostaglandins and ovum implantation in mice. Journal of Experimental Zoology 278 53-57.
58. Papay KD & Kennedy TG 2000 Characterization of temporal and cell-specific changes in transcripts for prostaglandin E(2) receptors in pseudopregnant rat endometrium. Biology of Reproduction 62 1515-1525.
59. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK & Hogan BL 2001 Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. PNAS 98 1047-1052.
60. Pennica D, Shaw KJ, Swanson TA, Moore MW, Shelton DL, Zioncheck KA, Rosenthal A, Taga T, Paoni NF & Wood WI 1995 Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex. Journal Biological Chemistry 270 10915-10922.
61. Pollard JW, Jahan M & Butterworth PJ 1990 Characterization and expression of uterine and placental alkaline phosphatases in the mouse. Journal of Reproduction and Fertility 89 735-742.
62. Psychoyos A 1993 Uterine receptivity for egg-implantation and scanning electron microscopy. Acta Europaca Fertilitatis 24 41-42.
63. Rankin JC, Ledford BE, Jonsson HT, Jr. & Baggett B 1979 Prostaglandins, indomethacin and the decidual cell reaction in the mouse uterus. Biology of Reproduction 20 399-404.
64. Reese J, Brown N, Paria BC, Morrow J & Dey SK 1999 COX-2 compensation in the uterus of COX-1 deficient mice during the pre-implantation period. Molecular and Cellular Endocrinology 150 23-31.
65. Sananes N, Baulieu EE & Le Goascogne C 1976 Prostaglandin(s) as inductive factor of decidualization in the rat uterus. Molecular and Cellular Endocrinology 6 153-158.
66. Satyaswaroop PG, Bressler RS, de la Pena MM & Gurpide E 1979 Isolation and culture of human endometrial glands. The Journal of Clinical Endocrinology and Metabolism 48 639-641.
67. Shen MM & Leder P 1992 Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro. PNAS 89 8240-8244.
68. Shevinsky LH, Knowles BB, Damjanov I & Solter D 1982 Monoclonal antibody to murine embryos defines a stage-specific embryonic antigen expressed on mouse embryos and human teratocarcinoma cells. Cell 30 697-705.
69. Siegfried JM, Nelson KG, Martin JL & Kaufman DG 1984 Promotional effect of diethylstilbestrol on human endometrial stromal cells pretreated with a direct-acting carcinogen. Carcinogenesis 5 641-646.
70. Sisk MA, Lohmann CH, Cochran DL, Sylvia VL, Simpson JP, Dean DD, Boyan BD & Schwartz Z 2001 Inhibition of cyclooxygenase by indomethacin modulates osteoblast response to titanium surface roughness in a time-dependent manner. Clinical Oral Implants Research 12 52-61.
71. Song H, Lim H, Das SK, Paria BC & Dey SK 2000 Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Molecular Endocrinology 14 1147-1161
72. Stewart CL & Cullinan EB 1997 Preimplantation development of the mammalian embryo and its regulation by growth factors. Developmental Genetics 21 91-101.
73. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F & Abbondanzo SJ 1992 Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359 76-79.
74. Thiede MA, Yoon K, Golub EE, Noda M & Rodan GA 1988 Structure and expression of rat osteosarcoma (ROS 17/2.8) alkaline phosphatase: product of a single copy gene. PNAS 85 319-323.
75. Ushikubi F, Segi E, Sugimoto Y, Murata T, Matsuoka T, Kobayashi T, Hizaki H, Tuboi K, Katsuyama M, Ichikawa A et al. 1998 Impaired febrile response in mice lacking the prostaglandin E receptor subtype EP3. Nature 395 281-284.
76. Vernallis AB, Hudson KR & Heath JK 1997 An antagonist for the leukemia inhibitory factor receptor inhibits leukemia inhibitory factor, cardiotrophin-1, ciliary neurotrophic factor, and oncostatin M. Journal Biological Chemistry 272 26947-26952.
77. Weitlauf HM & Suda-Hartman M 1988 Changes in secreted uterine proteins associated with embryo implantation in the mouse. Journal of Reproduction and Fertility 84 539-549.
78. Yang ZM, Le SP, Chen DB, Cota J, Siero V, Yasukawa K & Harper MJ 1995 Leukemia inhibitory factor, LIF receptor, and gp130 in the mouse uterus during early pregnancy. Molecular Reproduction and Development 42 407-414.
79. Yang ZM, Das SK, Wang J, Sugimoto Y, Ichikawa A & Dey SK 1997 Potential sites of prostaglandin actions in the periimplantation mouse uterus: differential expression and regulation of prostaglandin receptor genes. Biology of Reproduction 56 368-379.
80. Yee GM & Kennedy TG 1991 Role of cyclic adenosine 3′,5′-monophosphate in mediating the effect of prostaglandin E2 on decidualization in vitro. Biology of Reproduction 45 163-171.
81. Ying Y & Zhao GQ 2000 Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biology of Reproduction 63 1781-1786.
82. Zhang X & Croy BA 1996 Maintenance of decidual cell reaction by androgens in the mouse. Biology of Reproduction 55 519-524.