FSH receptor (FSHR) expression in human extragonadal reproductive tissues and the developing placenta, and the impact of its deletion on pregnancy in mice

Biology of Reproduction

Volumn 91, Issue 3, 2014, Pages

  Stilley, Julie A W ^a   Christensen, Debora E ^a   Dahlem, Kristin B ^a   Guan, Rongbin ^a   Santillan, Donna A ^a   England, Sarah K ^b   Al Hendy, Ayman ^c   Kirby, Patricia A ^a   Segaloff, Deborah L ^a  

^a UNIVERSITY OF IOWA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

Cervix; Follicle stimulating hormone; FSH receptor; Gonadotropin; Placenta; Pregnancy; Uterus

Indexed keywords

CHORIONIC GONADOTROPIN ALPHA SUBUNIT; FOLLITROPIN BETA SUBUNIT; FOLLITROPIN RECEPTOR; MESSENGER RNA;

ADVERSE OUTCOME; AMNION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL; CELLULAR DISTRIBUTION; CERVICAL GLAND; CERVICAL STROMA; CONTROLLED STUDY; DECIDUALIZATION; ENDOMETRIAL GLAND; ENDOMETRIUM; ENDOTHELIUM CELL; EXTRAGONADAL FEMALE REPRODUCTIVE TISSUE; FEMALE; FEMALE GENITAL SYSTEM; FETOPLACENTAL UNIT; FETUS DEVELOPMENT; GESTATIONAL AGE; HORMONE DETERMINATION; HUMAN; HUMAN TISSUE; MOUSE; MUSCLE CELL; MYOMETRIUM; NONHUMAN; PLACENTA; PLACENTA DEVELOPMENT; PLACENTA WEIGHT; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STROMA CELL; TRANSGENIC MOUSE; UMBILICAL CORD; UPREGULATION; UTERINE CERVIX; UTERUS; ADULT; ANIMAL; CYTOLOGY; EMBRYO MEMBRANE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; REPRODUCTION; VASCULAR ENDOTHELIUM; VASCULARIZATION;

MUS;

ADULT; ANIMALS; CERVIX UTERI; ENDOMETRIUM; ENDOTHELIUM, VASCULAR; EXTRAEMBRYONIC MEMBRANES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; MICE, KNOCKOUT; MYOMETRIUM; PLACENTA; PLACENTATION; PREGNANCY; RECEPTORS, FSH; RNA, MESSENGER; STROMAL CELLS; UMBILICAL CORD; UP-REGULATION;

EID: 84926657026     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.118562     Document Type: Article

References (48)

1. Sun L, Peng Y, Sharrow AC, Iqbal J, Zhang Z, Papachristou DJ, Zaidi S, Zhu LL, Yaroslavskiy BB, Zhou H, Zallone A, Sairam MR, et al. FSH directly regulates bone mass. Cell 2006; 125:247-260.
2. Zhu LL, Blair H, Cao J, Yuen T, Latif R, Guo L, Tourkova IL, Li J, Davies TF, Sun L, Bian Z, Rosen C, et al. Blocking antibody to the betasubunit of FSH prevents bone loss by inhibiting bone resorption and stimulating bone synthesis. Proc Natl Acad Sci U S A 2012; 109:14574-14579.
3. Radu A, Pichon C, Camparo P, Antoine M, Allory Y, Couvelard A, Fromont G, Hai MT, Ghinea N. Expression of follicle-stimulating hormone receptor in tumor blood vessels. N Engl J Med 2010; 363:1621-1630.
4. Mizrachi D, Shemesh M. Follicle-stimulating hormone receptor and its messenger ribonucleic acid are present in the bovine cervix and can regulate cervical prostanoid synthesis. Biol Reprod 1999; 61:776-784.
5. Popovici RM, Kao LC, Giudice LC. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology 2000; 141:3510-3513.
6. Celik O, Tagluk ME, Hascalik S, Elter K, Celik N, Aydin NE. Spectrotemporal changes in electrical activity of myometrium due to recombinant follicle-stimulating hormone preparations follitropin alfa and beta. Fertil Steril 2008; 90:1348-1356.
7. Hascalik S, Celik O, Tagluk ME, Yildirim A, Aydin NE. Effects of highly purified urinary FSH and human menopausal FSH on uterine myoelectrical dynamics. Mol Hum Reprod 2010; 16:200-206.
8. Stilley JA, Guan R, Duffy DM, Segaloff DL. Signaling through FSH receptors on human umbilical vein endothelial cells promotes angiogenesis. J Clin Endocrinol Metab 2014; 99:E813-E820.
9. Robinson LJ, Tourkova I, Wang Y, Sharrow AC, Landau MS, Yaroslavskiy BB, Sun L, Zaidi M, Blair HC. FSH-receptor isoforms and FSH-dependent gene transcription in human monocytes and osteoclasts. Biochem Biophys Res Commun 2010; 394:12-17.
10. Zhu LL, Tourkova I, Yuen T, Robinson LJ, Bian Z, Zaidi M, Blair HC. Blocking FSH action attenuates osteoclastogenesis. Biochem Biophys Res Commun 2012; 422:54-58.
11. Plunkett J, Doniger S, Orabona G, Morgan T, Haataja R, Hallman M, Puttonen H, Menon R, Kuczynski E, Norwitz E, Snegovskikh V, Palotie A, et al. An evolutionary genomic approach to identify genes involved in human birth timing. PLoS Genet 2011; 7:e1001365.
12. Vannier B, Loosfelt H, Meduri G, Pichon C, Milgrom E. Anti-human FSH receptor monoclonal antibodies: immunochemical and immunocytochemical characterization of the receptor. Biochemistry 1996; 35:1358-1366.
13. Quintana J, Hipkin RW, Ascoli M. A polyclonal antibody to a synthetic peptide derived from the rat follicle-stimulating hormone receptor reveals the recombinant receptor as a 74-kilodalton protein. Endocrinology 1993; 133:2098-2104.
14. Zhang M, Guan R, Segaloff DL. Revisiting and questioning functional rescue between dimerized LH receptor mutants. Mol Endocrinol 2012; 26:655-668.
15. Gerasimova T, Thanasoula MN, Zattas D, Seli E, Sakkas D, Lalioti MD. Identification and in vitro characterization of follicle stimulating hormone (FSH) receptor variants associated with abnormal ovarian response to FSH. J Clin Endocrinol Metab 2010; 95:529-536.
16. Bieche I, Latil A, Parfait B, Vidaud D, Laurendeau I, Lidereau R, Cussenot O, Vidaud M. CGA gene (coding for the alpha subunit of glycoprotein hormones) overexpression in ER alpha-positive prostate tumors. Eur Urol 2002; 41:335-341.
17. Danilovich N, Babu PS, Xing W, Gerdes M, Krishnamurthy H, Sairam MR. Estrogen deficiency, obesity, and skeletal abnormalities in folliclestimulating hormone receptor knockout (FORKO) female mice. Endocrinology 2000; 141:4295-4308.
18. Danilovich N, Sairam MR. Haploinsufficiency of the follicle-stimulating hormone receptor accelerates oocyte loss inducing early reproductive senescence and biological aging in mice. Biol Reprod 2002; 67:361-369.
19. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M, Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 1998; 95:13612-13617.
20. Whitten WK. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 1956; 13:399-404.
21. Rossant J, Croy BA. Genetic identification of tissue of origin of cellular populations within the mouse placenta. J Embryol Exp Morphol 1985; 86:177-189.
22. Jaffe RB, Lee PA, Midgley AR Jr. Serum gonadotropins before, at the inception of, and following human pregnancy. J Clin Endocrinol Metab 1969; 29:1281-1283.
23. Terzidou V, Blanks AM, Kim SH, Thornton S, Bennett PR. Labor and inflammation increase the expression of oxytocin receptor in human amnion. Biol Reprod 2011; 84:546-552.
24. Mitchell BF, Fang X, Wong S. Oxytocin: a paracrine hormone in the regulation of parturition? Rev Reprod 1998; 3:113-122.
25. Ahmed A, Perkins J. Angiogenesis and intrauterine growth restriction. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14:981-998.
26. Arroyo JA, Winn VD. Vasculogenesis and angiogenesis in the IUGR placenta. Semin Perinatol 2008; 32:172-177.
27. Garite TJ, Clark R, Thorp JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 2004; 191:481-487.
28. Kinzler WL, Vintzileos AM. Fetal growth restriction: a modern approach. Curr Opin Obstet Gynecol 2008; 20:125-131.
29. Mayhew TM, Charnock-Jones DS, Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies.Placenta 2004; 25:127-139.
30. Barut F, Barut A, Gun BD, Kandemir NO, Harma MI, Harma M, Aktunc E, Ozdamar SO. Intrauterine growth restriction and placental angiogenesis. Diagn Pathol 2010; 5:24.
31. Khankin EV, Royle C, Karumanchi SA. Placental vasculature in health and disease. Semin Thromb Hemost 2010; 36:309-320.
32. Furuya M, Kurasawa K, Nagahama K, Kawachi K, Nozawa A, Takahashi T, Aoki I. Disrupted balance of angiogenic and antiangiogenic signalings in preeclampsia. J Pregnancy 2011; 2011:123717.
33. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 2000; 141:1795-1803.
34. Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Buchanan DS, Hafez SA, Grazul-Bilska AT, Redmer DA. Uteroplacental vascular development and placental function: an update. Int J Dev Biol 2010; 54:355-366.
35. Tang B, Gurpide E. Direct effect of gonadotropins on decidualization of human endometrial stroma cells. J Steroid Biochem Mol Biol 1993; 47:115-121.
36. Mitchell BF, Wong S. Metabolism of oxytocin in human decidua, chorion, and placenta. J Clin Endocrinol Metab 1995; 80:2729-2733.
37. Chibbar R, Miller FD, Mitchell BF. Synthesis of oxytocin in amnion, chorion, and decidua may influence the timing of human parturition. J Clin Invest 1993; 91:185-192.
38. Huuskonen P, Storvik M, Reinisalo M, Honkakoski P, Rysa J, Hakkola J, Pasanen M. Microarray analysis of the global alterations in the gene expression in the placentas from cigarette-smoking mothers. Clin Pharmacol Ther 2008; 83:542-550.
39. Mikheev AM, Nabekura T, Kaddoumi A, Bammler TK, Govindarajan R, Hebert MF, Unadkat JD. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study. Reprod Sci 2008; 15:866-877.
40. Votavova H, Dostalova Merkerova M, Fejglova K, Vasikova A, Krejcik Z, Pastorkova A, Tabashidze N, Topinka J, Veleminsky M, Jr., Sram RJ, Brdicka R. Transcriptome alterations in maternal and fetal cells induced by tobacco smoke. Placenta 2011; 32:763-770.
41. Winn VD, Haimov-Kochman R, Paquet AC, Yang YJ, Madhusudhan MS, Gormley M, Feng KT, Bernlohr DA, McDonagh S, Pereira L, Sali A, Fisher SJ. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term. Endocrinology 2007; 148:1059-1079.
42. Dezso Z, Nikolsky Y, Sviridov E, Shi W, Serebriyskaya T, Dosymbekov D, Bugrim A, Rakhmatulin E, Brennan RJ, Guryanov A, Li K, Blake J, et al. A comprehensive functional analysis of tissue specificity of human gene expression. BMC Biol 2008; 6:49.
43. Eyster KM, Klinkova O, Kennedy V, Hansen KA. Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium. Fertil Steril 2007; 88:1505-1533.
44. Hawkins SM, Creighton CJ, Han DY, Zariff A, Anderson ML, Gunaratne PH, Matzuk MM. Functional microRNA involved in endometriosis. Mol Endocrinol 2011; 25:821-832.
45. Mutter GL, Zahrieh D, Liu C, Neuberg D, Finkelstein D, Baker HE, Warrington JA. Comparison of frozen and RNALater solid tissue storage methods for use in RNA expression microarrays. BMC Genomics 2004; 5:88.
46. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 2004; 101:6062-6067.
47. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006; 147:1097-1121.
48. Romundstad LB, Romundstad PR, Sunde A, von During V, Skjaerven R, Gunnell D, Vatten LJ. Effects of technology or maternal factors on perinatal outcome after assisted fertilisation: a population-based cohort study. Lancet 2008; 372:737-743.