Implantation failure in female Kiss1-/- mice is independent of their hypogonadic state and can be partially rescued by leukemia inhibitory factor

Endocrinology

Volumn 155, Issue 8, 2014, Pages 3065-3078

  Calder, Michele ^a,b,c   Chan, Yee Ming ^d,e   Raj, Renju ^d,f   Pampillo, Macarena ^a,b,c   Elbert, Adrienne ^a,b,g   Noonan, Michelle ^g   Gillio Meina, Carolina ^a,b   Caligioni, Claudia ^d   Bérubé, Nathalie G ^a,b,g   Bhattacharya, Moshmi ^g   Watson, Andrew J ^a,b,c,g   Seminara, Stephanie B ^d   Babwah, Andy V ^a,b,c,g  

^a CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c Department of Obstetrics and Gynaecology ^*  (Canada)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF VERMONT   (United States)

^g UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; EMBRYO IMPLANTATION; ESTRADIOL; FEMALE; GONADOTROPINS; KISSPEPTINS; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PREGNANCY; PREGNANCY, ANIMAL; PROGESTERONE; SUPEROVULATION; UTERUS;

EID: 84905028672     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1916     Document Type: Article

References (33)

1. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain J.L., Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor KISS1R. Proc Natl Acad Sci USA. 2003; 100:10972-10976.
2. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003; 349:1614-1627.
3. Funes S, Hedrick JA, Vassileva G, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun. 2003; 312:1357-1363.
4. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, et al. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci USA. 2007; 104:10714-10719.
5. -/- mice. Endocrinology. 2007; 148:4927-4936.
6. Chan YM, Broder-Fingert S, Paraschos S, et al. GnRH-deficient phenotypes in humans and mice with heterozygous variants in KISS1/Kiss1. J Clin Endocrinol Metab. 2011; 96:E1771-E1781.
7. Topaloglu AK, Tello JA, Kotan LD, et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med. 2012; 366:629-635.
8. Bilban M, Ghaffari-Tabrizi N, Hintermann E, et al. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci. 2004; 117: 1319-1328.
9. Horikoshi Y, Matsumoto H, Takatsu Y, et al. Dramatic elevation of plasma metastin concentrations in human pregnancy: metastin as a novel placenta-derived hormone in humans. J Clin Endocrinol Metab. 2003; 88:914-919.
10. Taylor J, Pampillo M, Bhattacharya M, Babwah AV. Kisspeptin/ KISS1R signaling potentiates extravillous trophoblast adhesion to type I collagen in a PKC- and ERK1/2-dependent manner. Mol Re-prod Dev. 2014; 81:42-54.
11. Cejudo Roman A, Pinto FM, Dorta I, et al. Analysis of the expression of neurokinin B, kisspeptin, and their cognate receptors NK3R and KISS1R in the human female genital tract. Fertil Steril. 2012; 97: 1213-1219.
12. -/--deficient mice. Endocrinology. 1999; 140:2704-2710.
13. Bell CE, Watson AJ. p38 MAPK regulates cavitation and tight junction function in the mouse blastocyst. PLoS One. 2013; 8:e59528.
14. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L., 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. Endocrinology. 2000; 141: 4365-4372.
15. Terakawa J, Watanabe T, Obara R, et al. The complete control of murine pregnancy from embryo implantation to parturition. Reproduction. 2012; 143:411-415.
16. Pau K-YF, Orstead KM, Hess D.L., Spies HG. Feedback effects of ovarian steroids on the hypothalamic-hypophyseal axis in the rabbit. Biol Reprod. 1986; 3:1009-1023.
17. Boyd-Leinen P, Gosse B, Rasmussen K, Martin-Dani G, Spelsberg TC. Regulation of nuclear binding of the avian oviduct progesterone receptor. Changes during estrogen-induced oviduct development, withdrawal, and secondary stimulation. J Biol Chem. 1984; 259: 2411-2421.
18. Wang XN, Greenwald GS. Synergistic effects of steroids with FSH on follicullogenesis, steroidogenesis and FSH- and hCG-receptors in hypophysectomized mice. J Reprod Fertil. 1999; 99:403-413.
19. Dey SK, Lim H, Das SK, et al. Molecular cues to implantation. Endocr Rev. 2004; 25:341-373.
20. Thompson EL, Murphy KG, Patterson M, et al. Chronic subcutaneous administration of kisspeptin-54 causes testicular degeneration in adult male rats. Am J Physiol Endocrinol Metab. 2006; 291: E1074-E1082.
21. Kirby DR, Potts DM, Wilson IB. On the orientation of the implanting blastocyst. J Embryol Exp Morphol. 1967; 17:527-532.
22. Smith LJ. Embryonic axis orientation in the mouse and its correlation with blastocyst relationships to the uterus. II. Relationships from 4 1/4 to 9 1/2 days. J Embryol Exp Morphol. 1985; 89:15-35.
23. Bhatt H, Brunet LJ, Stewart CL. Uterine expression of leukemia in hibitory factor coincides withthe onsetofblastocyst implantation. Proc Natl Acad Sci USA. 1991; 88:11408-11412.
24. Sun X, Bartos A, Whitsett JA, Dey SK. Uterine deletion of gp130 or stat3 shows implantation failure with increased estrogenic responses. Mol Endocrinol. 2013; 27:1492-1501.
25. Pawar S, Starosvetsky E, Orvis GD, Behringer R.R., Bagchi IC, Bagchi MK. STAT3 regulates uterine epithelial remodeling and epithe-lial-stromal crosstalk during implantation. Mol Endocrinol. 2013; 227:1996-2012.
26. Singh M, Chaudhry P, Asselin E. Bridging endometrial receptivity and implantation: networkofhormones, cytokines, and growth factors. J Endocrinol. 2011; 210:5-14.
27. Liu Z, Ren C, Jones W, et al. LC-MS/MS quantification of a neuropeptide fragment kisspeptin-10 (NSC 741805) and characterization of its decomposition product and pharmacokinetics in rats. J Chromatogr B Analyt Technol Biomed Life. 2013; 926:1-8.
28. Castellano JM, Gaytan M, Roa J, et al. Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology. 2006; 147:4852-4862.
29. Gaytán M, Castellano JM, Roa J, Sánchez-Criado JE, Tena-Sempere M, Gaytán F. Expression of KiSS-1 in rat oviduct: possible involvement in prevention of ectopic implantation? Cell Tissue Res. 2007; 329:571-579.
30. Gaytán F, Gaytán M, Castellano J.M., et al. KiSS-1 in the mammalian ovary: distribution of kisspeptin in human and marmoset and alterations in KiSS-1 mRNA levels in a rat model of ovulatory dysfunction. Am J Physiol Endocrinol Metab. 2009; 296:E520-E531.
31. Tenenbaum-Rakover Y, Commenges-Ducos M, Iovane A, Aumas C., Admoni O, de Roux N. Neuroendocrine phenotype analysis in five patients with isolated hypogonadotropic hypogonadism due to a L102P inactivating mutation of GPR54. J Clin Endocrinol Metab. 2007; 92:1137-1144.
32. Pallais JC, Bo-Abbas Y, Pitteloud N, Crowley WF Jr, Seminara SB. Neuroendocrine, gonadal, placental, and obstetric phenotypes in patients with IHH and mutations in the G-protein coupled receptor, GPR54. Mol Cell Endocrinol. 2006; 254-255:70-77.
33. Coulam CB, Chapman C, Rinehart JS. What is a preclinical pregnancy loss? J Assist Reprod Genet. 1998; 15:184-187. of Canada