Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary

Journal of Clinical Endocrinology and Metabolism

Volumn 96, Issue 6, 2011, Pages 1754-1762

  Fowler, Paul A ^a   Anderson, Richard A ^b   Saunders, Philippa T ^b   Kinnell, Hazel ^b   Mason, J Ian ^b   Evans, Dean B ^c   Bhattacharya, Siladitya ^a   Flannigan, Samantha ^a,d   Franks, Stephen ^a,d   Monteiro, Ana ^e   O'Shaughnessy, Peter J ^e  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c NOVARTIS PHARMA AG   (Switzerland)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; ANDROGEN RECEPTOR; AROMATASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450 17; CYTOCHROME P450 17A1; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA; UNCLASSIFIED DRUG;

AR GENE; ARTICLE; CYP19A1 GENE; ESR2 GENE; FEMALE; FETUS; GENE; GERM CELL; GRANULOSA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MORPHOLOGY; OBSERVATIONAL STUDY; OOCYTE; OVARY DEVELOPMENT; OVARY FOLLICLE; PREGNANCY TERMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA TRANSCRIPTION; SECOND TRIMESTER PREGNANCY; SOMATIC CELL; UNITED KINGDOM;

ANALYSIS OF VARIANCE; AROMATASE; ESTROGEN RECEPTOR BETA; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; OOCYTES; OVARY; PREGNANCY; PREGNANCY TRIMESTER, SECOND; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 79956322789     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2010-2618     Document Type: Article

References (63)

1. Skinner MK 2005 Regulation of primordial follicle assembly and development. Hum Reprod Update 11:461-471 (Pubitemid 41418801)
2. Maheshwari A, Fowler PA 2008 Primordial follicular assembly in humans. Zygote 16:285-296
3. Laissue P, Vinci G, Veitia RA, Fellous M 2008 Recent advances in the study of genes involved in non-syndromic premature ovarian failure. Mol Cell Endocrinol 282:101-111
4. Laissue P, Christin-Maitre S, Touraine P, Kuttenn F, Ritvos O, Aittomaki K, Bourcigaux N, Jacquesson L, Bouchard P, Frydman R, Dewailly D, Reyss AC, Jeffery L, Bachelot A, Massin N, Fellous M, Veitia RA 2006 Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol 154:739-744 (Pubitemid 43810861)
5. Chen Y, Breen K, Pepling ME 2009 Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary. J Endocrinol 202:407-417
6. Pepe GJ, Billiar RB, Albrecht ED 2006 Regulation of baboon fetal ovarian folliculogenesis by estrogen. Mol Cell Endocrinol 247:41-46 (Pubitemid 43277706)
7. Bocca SM, Billiar RB, Albrecht ED, Pepe GJ 2008 Oocytes of baboon fetal primordial ovarian follicles express estrogen receptor β mRNA. Endocrine 33:254-260
8. Yang MY, Fortune JE 2008 The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during midgestation and is associated with meiotic arrest of oocytes. Biol Reprod 78:1153-1161 (Pubitemid 351749297)
9. George FW, Wilson JD 1978 Conversion of androgen to estrogen by the human fetal ovary. J Clin Endocrinol Metab 47:550-555 (Pubitemid 9010405)
10. Pezzi V, Mathis JM, Rainey WE, Carr BR 2003 Profiling transcript levels for steroidogenic enzymes in fetal tissues. J Steroid Biochem Mol Biol 87:181-189 (Pubitemid 37532525)
11. Cole B, Hensinger K, Maciel GA, Chang RJ, Erickson GF 2006 Human fetal ovary development involves the spatiotemporal expression of p450c17 protein. J Clin Endocrinol Metab 91:3654-3661 (Pubitemid 44402151)
12. Vaskivuo TE, Mäentausta M, Törn S, Oduwole O, Lönnberg A, Herva R, Isomaa V, Tapanainen JS 2005 Estrogen receptors and estrogen-metabolizing enzymes in human ovaries during fetal development. J Clin Endocrinol Metab 90:3752-3756 (Pubitemid 41024138)
13. Juengel JL, Heath DA, Quirke LD, McNatty KP 2006 Oestrogen receptor α and β, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reproduction 131:81-92 (Pubitemid 43230706)
14. Gould DA, Moscoso GJ, Young MP, Barton DP 2000 Human first trimester fetal ovaries express oncofetal antigens and steroid receptors. J Soc Gynecol Investig 7:131-138 (Pubitemid 30216527)
15. Wilson CM, McPhaul MJ 1996 A and B forms of the androgen receptor are expressed in a variety of human tissues. Mol Cell Endocrinol 120:51-57 (Pubitemid 26197261)
16. Brandenberger AW, Tee MK, Lee JY, Chao V, Jaffe RB 1997 Tissue distribution of estrogen receptors α (ER-α) and β (ER-β) mRNA in the midgestational human fetus. J Clin Endocrinol Metab 82:3509-3512 (Pubitemid 27419113)
17. Fowler PA, Bhattacharya S, Gromoll J, Monteiro A, O'Shaughnessy PJ 2009 Maternal smoking and developmental changes in luteinizing hormone (LH) and the LH receptor in the fetal testis. J Clin Endocrinol Metab 94:4688-4695
18. O'Shaughnessy PJ, Baker PJ, Monteiro A, Cassie S, Bhattacharya S, Fowler PA 2007 Developmental changes in human fetal testicular cell numbers and messenger ribonucleic acid levels during the second trimester. J Clin Endocrinol Metab 92:4792-4801
19. Fowler PA, Cassie S, Rhind SM, Brewer MJ, Collinson JM, Lea RG, Baker PJ, Bhattacharya S, O'Shaughnessy PJ 2008 Maternal smoking during pregnancy specifically reduces human fetal desert hedgehog gene expression during testis development. J Clin Endocrinol Metab 93:619-626
20. Fowler PA, Flannigan S, Mathers A, Gillanders K, Lea RG, Wood MJ, Maheshwari A, Bhattacharya S, Collie-Duguid ES, Baker PJ, Monteiro A, O'Shaughnessy PJ 2009 Gene expression analysis of human fetal ovarian primordial follicle formation. J Clin Endocrinol Metab 94:1427-1435
21. Nicol MR, Papacleovoulou G, Evans DB, Penning TM, Strachan MW, Advani A, Johnson SJ, Quinton R, Mason JI 2009 Estrogen biosynthesis in human H295 adrenocortical carcinoma cells. Mol Cell Endocrinol 300:115-120
22. Goto M, Piper Hanley K, Marcos J, Wood PJ, Wright S, Postle AD, Cameron IT, Mason JI, Wilson DI, Hanley NA 2006 In humans, early cortisol biosynthesis provides a mechanism to safeguard female sexual development. J Clin Invest 116:953-960
23. Papacleovoulou G, Edmondson RJ, Critchley HO, Hillier SG, Mason JI 2009 3β-Hydroxysteroid dehydrogenases and pre-receptor steroid metabolism in the human ovarian surface epithelium. Mol Cell Endocrinol 301:65-73
24. Gaskell TL, Esnal A, Robinson LL, Anderson RA, Saunders PT 2004 Immunohistochemical profiling of germ cells within the human fetal testis: identification of three subpopulations. Biol Reprod 71:2012-2021 (Pubitemid 39586949)
25. Saunders PT, Millar MR, Williams K, Macpherson S, Harkiss D, Anderson RA, Orr B, Groome NP, Scobie G, Fraser HM 2000 Differential expression of estrogen receptor-α and -β and androgen receptor in the ovaries of marmosets and humans. Biol Reprod 63:1098-1105
26. Gaskell TL, Robinson LL, Groome NP, Anderson RA, Saunders PT 2003 Differential expression of two estrogen receptor β isoforms in the human fetal testis during the second trimester of pregnancy. J Clin Endocrinol Metab 88:424-432 (Pubitemid 36115198)
27. O'Shaughnessy PJ, Willerton L, Baker PJ 2002 Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 66:966-975 (Pubitemid 34263116)
28. O'Shaughnessy PJ, Murphy L 1993 Cytochrome P-450 17 α-hydroxylase protein and mRNA in the testis of the testicular feminized (tfm) mouse. J Mol Endocrinol 11:77-82 (Pubitemid 23297953)
29. Albrecht ED, Pepe GJ 2010 Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int J Dev Biol 54:397-408
30. Smith ID, Shutt DA, Shearman RP 1975 Foetal plasma steroid concentrations related to gestational age and method of delivery. J Steroid Biochem 6:657-662
31. Shutt DA, Smith ID, Shearman RP 1974 Oestrone, oestradiol-17β and oestriol levels in human foetal plasma during gestation and at term. J Endocrinol 60:333-341
32. Quirke LD, Juengel JL, Tisdall DJ, Lun S, Heath DA, McNatty KP 2001 Ontogeny of steroidogenesis in the fetal sheep gonad. Biol Reprod 65:216-228 (Pubitemid 32574803)
33. Nilsson EE, Skinner MK 2009 Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Mol Cell Endocrinol 313:9-16
34. Collins F, MacPherson S, Brown P, Bombail V, Williams AR, Anderson RA, Jabbour HN, Saunders PT 2009 Expression of oestrogen receptors, ERα, ERβ, and ERβ variants, in endometrial cancers and evidence that prostaglandin F may play a role in regulating expression of ERα. BMC Cancer 9:330
35. Couse JF, Korach KS 2001 Contrasting phenotypes in reproductive tissues of female estrogen receptor null mice. Ann NY Acad Sci 948:1-8 (Pubitemid 34044525)
36. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M 2000 Effect of single andcompoundknockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development 127:4277-4291
37. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
38. Kezele P, Skinner MK 2003 Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology 144:3329-3337 (Pubitemid 36904407)
39. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME 2007 Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 148:3580-3590 (Pubitemid 47105867)
40. Fowler PA, Evans LW, Groome NP, Templeton A, Knight PG 1998 A longitudinal study of maternal serum inhibin-A, inhibin-B, activin-A, activin-AB, pro-αC and follistatin during pregnancy. Hum Reprod 13:3530-3536 (Pubitemid 29002653)
41. Sen A, Hammes SR 2010 Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol Endocrinol 24:1393-1403
42. Shiina H, Matsumoto T, Sato T, Igarashi K, Miyamoto J, Takemasa S, Sakari M, Takada I, Nakamura T, Metzger D, Chambon P, Kanno J, Yoshikawa H, Kato S 2006 Premature ovarian failure in androgen receptor-deficient mice. Proc Natl Acad Sci USA 103:224-229 (Pubitemid 43076131)
43. Dumesic DA, Patankar MS, Barnett DK, Lesnick TG, Hutcherson BA, Abbott DH 2009 Early prenatal androgenization results in diminished ovarian reserve in adult female rhesus monkeys. Hum Reprod 24:3188-3195
44. Sajjad Y, Quenby SM, Nickson P, Lewis-Jones DI, Vince G 2004 Expression of androgen receptors in upper human fetal reproductive tract. Hum Reprod 19:1659-1665 (Pubitemid 38997199)
45. Hickey M, Sloboda DM, Atkinson HC, Doherty DA, Franks S, Norman RJ, Newnham JP, Hart R 2009 The relationship between maternal and umbilical cord androgen levels and polycystic ovary syndrome in adolescence: a prospective cohort study. J Clin Endocrinol Metab 94:3714-3720
46. Hart R, Sloboda DM, Doherty DA, Norman RJ, Atkinson HC, Newnham JP, Dickinson JE, Hickey M 2010 Circulating maternal testosterone concentrations at 18 weeks of gestation predict circulating levels of antimullerian hormone in adolescence: a prospective cohort study. Fertil Steril 94:1544-1547
47. Pollack SE, Furth EE, Kallen CB, Arakane F, Kiriakidou M, Kozarsky KF, Strauss 3rd JF 1997 Localization of the steroidogenic acute regulatory protein in human tissues. J Clin Endocrinol Metab 82:4243-4251 (Pubitemid 27525548)
48. Mandon-Pépin B, Oustry-Vaiman A, Vigier B, Piumi F, Cribiu E, Cotinot C 2003 Expression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ovary. Biol Reprod 68:985-995 (Pubitemid 36245846)
49. Small CL, Shima JE, Uzumcu M, Skinner MK, Griswold MD 2005 Profiling gene expression during the differentiation and development of the murine embryonic gonad. Biol Reprod 72:492-501 (Pubitemid 40129727)
50. Herrera L, Ottolenghi C, Garcia-Ortiz JE, Pellegrini M, Manini F, Ko MS, Nagaraja R, Forabosco A, Schlessinger D 2005 Mouse ovary developmental RNA and protein markers from gene expression profiling. Dev Biol 279:271-290 (Pubitemid 40298738)
51. Yoon SJ, Kim KH, Chung HM, Choi DH, Lee WS, Cha KY, Lee KA 2006 Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fertil Steril 85:193-203
52. Kezele PR, Ague JM, Nilsson E, Skinner MK 2005 Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 72:241-255 (Pubitemid 40013778)
53. Arraztoa JA, Zhou J, Marcu D, Cheng C, Bonner R, Chen M, Xiang C, Brownstein M, Maisey K, Imarai M, Bondy C 2005 Identification of genes expressed in primate primordial oocytes. Hum Reprod 20:476-483 (Pubitemid 40277620)
54. Zhang P, Kerkelä E, Skottman H, Levkov L, Kivinen K, Lahesmaa R, Hovatta O, Kere J 2007 Distinct sets of developmentally regulated genes that are expressed by human oocytes and human embryonic stem cells. Fertil Steril 87:677-690 (Pubitemid 46385964)
55. Serafica MD, Goto T, Trounson AO 2005 Transcripts from a human primordial follicle cDNA library. Hum Reprod 20:2074-2091 (Pubitemid 41430103)
56. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S 2006 The human cumulus-oocyte complex gene-expression profile.HumReprod 21:1705-1719
57. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, Shea LD, Mayo KE, Woodruff TK 2006 Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol 298:132-148 (Pubitemid 44414802)
58. Nilsson E, Parrott JA, Skinner MK 2001 Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol 175:123-130 (Pubitemid 32372548)
59. Nilsson EE, Stanfield J, Skinner MK 2006 Interactions between progesterone and tumor necrosis factor-α in the regulation of primordial follicle assembly. Reproduction 132:877-886 (Pubitemid 46040658)
60. Martins da Silva SJ, Bayne RA, Cambray N, Hartley PS, McNeilly AS, Anderson RA 2004 Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation. Dev Biol 266:334-345 (Pubitemid 38102243)
61. Coutts SM, Childs AJ, Fulton N, Collins C, Bayne RA, McNeilly AS, Anderson RA 2008 Activin signals via SMAD2/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression. Dev Biol 314:189-199
62. Pepe GJ, Billiar RB, Leavitt MG, Zachos NC, Gustafsson JA, Albrecht ED 2002 Expression of estrogen receptors α and β in the baboon fetal ovary. Biol Reprod 66:1054-1060 (Pubitemid 34266088)
63. Dupont E, Labrie F, Luu-The V, Pelletier G 1992 Immunocytochemical localization of 3β-hydroxysteroid dehydrogenase/Δ5-Δ4-isomerase in human ovary. J Clin Endocrinol Metab 74:994-998