Endometrial receptivity defects and impaired implantation in diabetic NOD mice

Biology of Reproduction

Volumn 87, Issue 2, 2012, Pages

  Albaghdadi, Ahmad J H ^a   Kan, Frederick W K ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Ifn ; Implantation failure in type 1 diabetes; Muc1; Nf b; NOD mice; Piasy; Progesterone receptor; Stat3; Uterodomes

Indexed keywords

CONCANAVALIN A; LEUKEMIA INHIBITORY FACTOR; MUCIN 1; PROGESTERONE RECEPTOR; STAT3 PROTEIN; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CLINICAL FEATURE; CONTROLLED STUDY; DECIDUALIZATION; DISEASE ASSOCIATION; ENDOMETRIUM; FEMALE; HORMONE RELEASE; IMPLANTATION FAILURE; INSULIN DEPENDENT DIABETES MELLITUS; MORPHOLOGY; MOUSE; NIDATION; NONHUMAN; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PREGNANCY DISORDER; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSEUDOPREGNANCY;

ABORTION, SPONTANEOUS; ANIMALS; CONCANAVALIN A; DIABETES MELLITUS, TYPE 1; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MUCIN-1; PREGNANCY; PROTEIN INHIBITORS OF ACTIVATED STAT; RECEPTORS, PROGESTERONE; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA;

MUS;

EID: 84869387810     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.100016     Document Type: Article

References (53)

1. Platt MJ, Stanisstreet M, Casson IF, Howard CV, Walkinshaw S, Pennycook S, McKendrick O. St Vincent's declaration 10 years on: outcomes of diabetic pregnancies. Diabet Med 2002; 19:216-220.
2. Casson IF, Clarke CA, Howard CV, McKendrick O, Pennycook S, Pharoah PO, Platt MJ, Stanisstreet M, van Velszen D, Walkinshaw S. Outcomes of pregnancy in insulin dependent diabetic women: results of a five year population cohort study. BMJ 1997; 315:275-278.
3. Burke SD, Dong H, Hazan AD, Croy BA. Aberrant endometrial features of pregnancy in diabetic NOD mice. Diabetes 2007; 56:2919-2926.
4. Psychoyos A, Nikas G. Uterine pinopodes as markers of uterine receptivity. Assist Reprod Rev 1994; 4:26-32.
5. Murphy CR, Shaw TJ. Plasma membrane transformation: a common response of uterine epithelial cells during the peri-implantation period. Cell Biol Int 1994; 18:1115-1128.
6. Psychoyos A. Hormonal control of ovoimplantation. Vitam Horm 1973; 31:201-256.
7. Kaneko Y, Lindsay LA, Murphy CR. Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells. Reprod Fertil Dev 2008; 20: 892-899.
8. Nakamura H, Kimura T, Ogita K, et al. NFjB activation at implantation window of the mouse uterus. Am J Reprod Immunol 2004; 51:16-21.
9. Teng CB, Diao HL, Ma XH, Xu LB, Yang ZM. Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol Reprod Dev 2004; 69:1-10.
10. Chen JR, Cheng J, Shatzer T, Sewell L, Hernandez L and Stewart CL. 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. Endocrinol 2000; 141:4365-4372.
11. Arici A, Engin O, Attar E, and Olive DL. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. J Clin Endocrinol Metab 1995; 80:1908-1915.
12. Raghupathy, R, Makhseed M, Azizieh F, Omu A, Gupta M and Farhat R. Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Hum Reprod 2000; 15:713-718.
13. Singh, H Nardo, L Kimber SJ, Aplin JD. Early stages of implantation as revealed by an in vitro model. Reproduction 2010; 139:905-914.
14. Gendler SJ, Spicer AP. Epithelial mucin genes. Annu Rev Physiol 1995; 57:607-634.
15. Brayman M, Thathiah A, Carson DD. MUC1: a multifunctional cell surface component of reproductive tissue epithelia. Reprod Biol Endocrinol 2004; 7; 2:4.
16. Surveyor GA, Gendler SJ, Pemberton L, Das SK, Chakraborty I, Julian J, Pimental RA, Wegner CC, Dey SK, Carson DD. Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinol 1995; 136: 3639-3647.
17. Horne AW, Lalani EN, Margara RA, Ryder TA, Mobberley MA, White JO. The expression pattern of MUC1 glycoforms and other biomarkers of endometrial receptivity in fertile and infertile women. Mol Reprod Dev 2005; 72:216-229.
18. Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nature Med 1998; 4:303-308.
19. Palfi M, Jablonowska B, Matthiesen L. Circulating interferon-gamma- and interleukin-4-secreting cells in recurrent spontaneous abortions. Am J Reprod Immunol 1999; l 41:257-263.
20. Dharmaraj N, Wang P and Carson DD. Cytokine and progesterone receptor interplay in the regulation of MUC1 gene expression. Mol Endocrinol 2010; 24:2253-2266.
21. Brayman MJ, Dharmaraj N, Lagow E, Carson DD. MUC1 expression is repressed by protein inhibitor of activated signal transducer and activator of transcription-y. Mol Endocrinol 2007; 21:2725-2737.
22. Zoumpoulidou G, Jones MC, de Mattos SF, Francis JM, Fusi L, Lee YS, Christian M, Varshochi R, Lam EF, Brosens JJ. Convergence of interferon-c and progesterone signaling pathways in human endometrium: role of PIASy (protein inhibitor of activated signal transducer and activator of transcription-y) Mol Endocrinol 2004; 18:1988-1999.
23. Herington JL, Underwood T, McConaha M, Bany BM. Paracrine signals from the mouse conceptus are not required for the normal progression of decidualization. Endocrinol 2009; 150:4404-4413.
24. Bindali, B, Kaliwal, BB. Anti-implantation activity of carbamate fungicide mancozeb in albino mice. Ind Health 2002; 40:191-197.
25. Mikel UV (ed). Advanced Laboratory Methods in Histology and Pathology. Washington, DC: Armed Forces Institute of Pathology: 1994.
26. Qi L, Anthony L, Terence J, Fordyce L, Christopher B, Elise SFA. Syntaxin 1, GaO, and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 2004; 24:4070-4081.
27. Adams Susan M, Gayer Nalini, Terry Vera, Murphy CR. Manipulation of the follicular phase: uterodomes and pregnancy-is there a correlation? BMC Pregnancy Childbirth 2001; 1:2.
28. Kibbe WA. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 2007; 35(suppl 2):W43-W46.
29. Nolan T, Hands RE, Bustin SA. Quantification of mRNA using real-time RT-PCR. Nat Protocols 2006; 1:1559-1582.
30. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferong: implications for immune responses and autoimmune diseases. Immunity 2009; 31:539-550.
31. Leiter EH. The NOD mouse: a model for insulin-dependent diabetes mellitus. Curr Protoc Immunol 1997; 24(suppl):15.9.1-15.9.23.
32. Platt JS, Hunt JS. Interferon-gamma gene expression in cycling and pregnant mouse uterus: temporal aspects and cellular localization. J Leukoc Biol 1998; 64:393-400.
33. 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.
34. Fraser RB, Waite SL, Wood KA, Martin KL. Impact of hyperglycemia on early embryo development and embryopathy: in vitro experiments using a mouse model. Hum Reprod 2007; 22:3059-3068.
35. Seaward VC, Burke SD, Croy. BA. Interferon gamma contributes to preimplantation embryonic development and to implantation site structure in NOD mice. Hum Reprod 2010; 25:2829-2839.
36. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today 1997; 18:478-482.
37. Glynn DJ, Sharkey DJ, Robertson SA. Interferon-gamma inhibits female reproductive tract responsiveness to seminal plasma. In: Proceedings of the 37th Annual Meeting of the Society for the Study of Reproduction, Vancouver, British Columbia, Canada, Aug 1-4, 2004. Biol Reprod 2004; 70(suppl 1):242.
38. Fontana V, Choren V, Vauthay1 L, Calvo JC, Calvo L, Cameo M. Exogenous interferon-c alters murine inner cell mass and trophoblast development. Effect on the expression of ErbB1, ErbB4 and heparan sulfate proteoglycan (perlecan). Reproduction 2004; 128:717-725.
39. Cameo M, Fontana V, Cameo P, Vauthay LG, Kaplan J, Tesone M. Similar embryotoxic effects of sera from infertile patients and exogenous interferon-g on long-term in vitro development of mouse embryos. Hum Reprod 1999; 14:959-963.
40. Hunt JS, Atherton RA. Differential responses of rat trophoblast cells and embryonic fibroblasts to cytokines that regulate proliferation and class I MHC antigen expression. J Immunol 1990; 145:184-189.
41. Hibbert L, Pflanz S, De Waal Malefyt R, Kastelein RA. IL-27 and IFNalpha signal via Stat1 and Stat3 and induce T-Bet and IL-12Rbeta2 in naive T cells. J Interferon Cytokine Res 2003; 23(9):513-522.
42. Kniss DA, Rovin B, Fertel RH, Zimmerman PD. Blockade NF-kB activation prohibits TNF-a-induced cyclooygenase-2 gene expression in ED27 trophoblast-like cells. Placenta 2001; 22:80-89.
43. Paulesu L, Jantra S, Ietta F, Brizzi R, Bigliardi E. Interleukin-1 in reproductive strategies. Evol Dev 2008; 10:778-788.
44. Dhananjaya VK. Alternate interferon signaling pathways. Pharmacol Ther 2003; 100(1):1-29.
45. Xia HF, Sun QH, Peng JP. Effect of interferon-gamma treatment on the expression of interleukin-1beta at the maternal-fetal interface of pregnant rats. Reprod Fertil Dev 2007; 19(3):510-519.
46. Geisert R, Fazleabas A, Lucy M, Mathew D. Interaction of the conceptus and endometrium to establish pregnancy in mammals: role of interleukin 1b. Cell Tissue Res 2012; (in press). Epub ahead of print March 2, 2012. DOI: 10.1007/s00441-012-1356-1.
47. Illingworth IM, Kiszka I, Bagley S, Ireland GW, Garrod DR, Kimber SJ. Desmosomes are reduced in the mouse uterine luminal epithelium during the preimplantation period of pregnancy: a mechanism for facilitation of implantation. Biol Reprod 2000; 63:1764-1773.
48. Kondo K, Kohno N, Yokoyama A, Hiwada K. Decreased MUC1 expression induces E-cadherin-mediated cell adhesion of breast cancer cell lines. Cancer Res 1998; 58:2014-2019.
49. Utech M, Ivanov AI, Samarin SN, Bruewer M, Turner JR, Mrsny RJ, Parkos CA, Nusrat A. Mechanism of IFNc-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 2005; 16:5040-5052.
50. Cheng JG, Chen JR, Hernandez L, Alvord WG, Stewart CL. Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. Proc Nat Acad Sci U S A 2001; 98:8680-8685.
51. Fouladi-Nashta AA, Jones CJ, Nijjar N, Mohamet L, Smith A, Chambers I, Kimber SJ. Characterization of the uterine phenotype during the periimplantation period for LIF-null, MF1 strain mice. Dev Biol 2005; 281: 1-21.
52. Nelson V, Davis GE, Maxwell SA. A putative protein inhibitor of activated STAT (PIASy) interacts with p53 and inhibits p53-mediated transactivation but not apoptosis. Apoptosis 2001; 6:221-234.
53. Hu W, Feng Z, Teresky AK, Levine AJ. p53 regulates maternal reproduction through LIF. Nature 2007; 450:721-72.