Different patterns of anti-Müllerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads

Developmental Dynamics

Volumn 225, Issue 3, 2002, Pages 221-232

  Oréal, Emmanuelle ^a   Mazaud, Séverine ^b   Picard, Jean Yves ^a   Magre, Solange ^b   Carré Eusébe, Daniéle ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

AMH; Aromatase; Chick embryo; Cvh; DMRT1; GATA 4; Lhx9; MIS; Ovary; Sex differentiation; SF 1; SOX9; Testis; Wnt 4; WT1

Indexed keywords

AROMATASE; MUELLERIAN INHIBITING FACTOR; PROTEIN; PROTEIN DMRT1; PROTEIN LHX9; PROTEIN SF1; PROTEIN WT1; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; WNT PROTEIN; WNT4 PROTEIN; CELL RECEPTOR; DMRT1 PROTEIN; DNA BINDING PROTEIN; FUSHI TARAZU PROTEIN; GLYCOPROTEIN; GROWTH INHIBITOR; HOMEODOMAIN PROTEIN; MESSENGER RNA; MULLERIAN INHIBITING HORMONE; MULLERIAN-INHIBITING HORMONE; STEROIDOGENIC FACTOR 1; TESTIS PEPTIDE HORMONE; TRANSCRIPTION FACTOR; WT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL AGGREGATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; GONAD DEVELOPMENT; GRANULOSA CELL; IN SITU HYBRIDIZATION; LEYDIG CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY DEVELOPMENT; OVARY FOLLICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; SEX DIFFERENCE; SEX DIFFERENTIATION; SPECIES DIFFERENCE; TESTIS DEVELOPMENT; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS; MUELLERIAN DUCT; OVARY; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEXUAL DEVELOPMENT; TESTIS;

AVES; GALLUS GALLUS; MAMMALIA;

ANIMALS; AROMATASE; CHICK EMBRYO; DNA-BINDING PROTEINS; FEMALE; FUSHI TARAZU TRANSCRIPTION FACTORS; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; GROWTH INHIBITORS; HOMEODOMAIN PROTEINS; MALE; MOLECULAR SEQUENCE DATA; MULLERIAN DUCTS; OVARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; SEX CHARACTERISTICS; SEX DIFFERENTIATION; TESTICULAR HORMONES; TESTIS; TRANSCRIPTION FACTORS; WT1 PROTEINS;

EID: 0036840341     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.10153     Document Type: Article

References (60)

1. Arango NA, Lovell-Badge R, Behringer RR. 1999. Targeted mutagenesis of the endogenous mouse MIS gene promoter: In vivo definition of genetic pathways of vertebrate sexual development. Cell 99:409-419.
2. Bézard J, Vigier B, Mauléon P, Josso N. 1987. Immunocytochemical study of anti-Müllerian hormone in sheep ovarian follicles during fetal and post-natal development. J Reprod Fertil 80:509-516.
3. Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Zhao Y, Grinberg A, Huang S, Kreidberg JA, Parker KL, Porter FD, Westphal H. 2000. The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403:909-913.
4. Capel B. 2000. The battle of sexes. Mech Dev 92:89-103.
5. Carré-Eusèbe D, di Clemente N, Rey R, Pieau C, Vigier B, Josso N, Picard JY. 1996. Cloning and expression of the chick anti-Müllerian hormone gene. J Biol Chem 271:4798-4804.
6. Ch'in Suang H, Gaginskaia ER, Kalinina EI. 1979. Characteristics of oogenesis in the chick. I. The extrafollicular period in the development of the oocytes. Ontogenez 10:340-349.
7. Chun SY, McGee EA, Hsu SY, Minami S, LaPolt PS, Yao HH, Bahr JM, Gougeon A, Schomberg DW, Hsueh AJ. 1999. Restricted expression of WT-1 messenger ribonucleic acid in immature ovarian follicles: Uniformity in mammalian and avian species and maintenance during reproductive senescence. Biol Reprod 60:365-373.
8. Clinton M. 1998. Sex determination and gonadal development: A birds' eye view. J Exp Zool 281:457-465.
9. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P. 1998. Direct interaction of SRY-related protein Sox9 and steroidogenic factor 1 regulates transcription of the human anti-Müllerian hormone gene. Mol Cell Biol 18:6653-6665.
10. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Kumar TR, Matzuk MM, Rose UM, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. 2001. Anti-Müllerian hormone attenuates the effect of FSH on follicle development in the mouse ovary. Endocrinology 142:4891-4899.
11. Ellegren H. 2001. Hens, cocks and avian sex determination. A quest for genes on Z or W? EMBO Rep 2:192-196.
12. Erickson GF. 1974. The control of the differentiation of female embryonic germ cells in the bird. Dev Biol 36:113-129.
13. Failli V, Rogard M, Mattei MG, Vernier P, Retaux S. 2000. Lhx9 and Lhx9α LIM-homeodomain factors: Genomic structure, expression patterns, chromosomal localization and phylogenetic analysis. Genomics 64:307-317.
14. Foster JW, Dominguez-Steglich MA, Guioli S, Kowk G, Weller PA, Stevanovic M, Weissenbach J, Mansour S, Young ID, Goodfellow PN. 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372:525-530.
15. Fridmacher V, Le Bert M, Guillou F, Magre S. 1995. Switch in the expression of the K19/K18 keratin genes as a very early evidence of testicular differentiation in the rat. Mech Dev 52:199-207.
16. Griffiths R. 1991. The isolation of conserved DNA sequences related to the human sex-determining region Y gene from the lesser black-backed gull (Larus fuscus). Proc R Soc Lond B Biol Sci 244:123-128.
17. Griffiths R, Daan S, Dijkstra C. 1996. Sex identification in birds using two CHD genes. Proc R Soc Lond B Biol Sci 263:1251-1256.
18. Hamburger V, Hamilton H. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
19. Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K. 1994. Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 12:2787-2797.
20. Hutson J, Ikawa H, Donahoe PK. 1981. The ontogeny of Müllerian inhibiting substance in the gonads of the chicken. J Pediatr Surg 16:822-827.
21. Jordan BK, Mohammed M, Ching ST, Délot E, Chen XN, Dewing P, Swain A, Rao PN, Elejalde BR, Vilain E. 2001. Up-regulation of WNT-4 signaling and dosage-sensitive sex reversal in humans. Am J Hum Genet 68:1102-1109.
22. Kent J, Coriat AM, Sharpe PT, Hastie ND, van Heyningen V. 1995. The evolution of WT1 sequence and expression pattern in the vertebrates. Oncogene 11:1781-1792.
23. Kispert A, Vainio S, McMahon AP. 1998. Wnt-4 is a mesenchymal signal for epithelial transformation of metanephric mesenchyme in the developing kidney. Development 125:4225-4234.
24. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. 1993. WT-1 is required for early kidney development. Cell 74:679-691.
25. Kuroda Y, Arai N, Arita M, Teranishi M, Hori T, Harata M, Mizuno S. 2001. Absence of Z-chromosome inactivation for five genes in male chickens. Chromosome Res 9:457-468.
26. Luo X, Ikeda Y, Parker KL. 1994. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77:481-490.
27. Lynch JP, Lala DS, Peluso JJ, Luo W, Parker KL, White BA. 1993. Steroidogenic factor 1, an orphan nuclear receptor, regulates the expression of rat aromatase gene in gonadal tissues. Mol Endocrinol 7:776-786.
28. McCoard SA, Wise TH, Fahrenkrug SC, Ford JJ. 2001. Temporal and spatial localization patterns of GATA4 during porcine gonadogenesis. Biol Reprod 65:366-374.
29. McGee EA, Smith R, Spears N, Nachtigal MW, Ingraham H, Huesh AJ. 2001. Müllerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol Reprod 64:293-298.
30. McQueen HA, McBride D, Miele G, Bird AP, Clinton M. 2001. Dosage compensation in birds. Curr Biol 11:253-257.
31. Merchant-Larios H, Popova L, Reyss-Brion M. 1984. Early morphogenesis of chick gonad in the absence of mesonephros. Dev Growth Differ 26:403-417.
32. Nachtigal MW, Hirokawa Y, Enyeart-VanHouten DL, Flanagan JN, Hammer GD, Ingraham HA. 1998. Wilms' tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93:445-454.
33. Nanda I, Shan Z, Schartl M, Burt D, Koehler M, Northwang H-G, Grfitzner F, Paton I, Windsor D, Dunn I, Engel W, Staeheli P, Mizuno S, Haaf T, Schmid M. 1999. 300 Million years of conserved synteny between chick Z and human chromosome 9. Nat Genet 21:258-259.
34. Nishikimi H, Kansaku N, Saito N, Usami M, Ohno Y, Shimada K. 2000. Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken. Mol Reprod Dev 55:20-30.
35. Nitta H, Osawa Y, Bahr JM. 1991. Multiple steroidogenic cell populations in the thecal layer of preovulatory follicles of the chicken ovary. Endocrinology 129:2033-2040.
36. Nohno T, Kawakami Y, Wada N, Ishikawa T, Ohuchi H, Noji S. 1997. Differential expression of the two closely related LIM-class homeobox genes LH-2A and LH-2B during limb development. Biochem Biophys Res Commun 238:506-511.
37. Nomura O, Nakabayashi O, Nishimori K, Yasue H, Mizuno S. 1999. Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos. J Steroid Biochem Mol Biol 71:103-109.
38. Oréal E, Pieau C, Mattei MG, Josso N, Picard JY, Carré-Eusébe D, Magre S. 1998. Early expression of AMH in chicken embryonic gonads precedes testicular SOX9 expression. Dev Dyn 212:522-532.
39. Racine C, Rey R, Forest MG, Louis F, Ferré A, Huhtaniemi I, Josso N, di Clemente N. 1998. Receptors for anti-Müllerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci U S A 95:594-599.
40. Raymond CS, Parker ED, Kettlewell JR, Brown LG, Page DC, Kusz KK, Jaruzelska J, Reinberg Y, Flejter WL, Bardwell VJ, Hirsh B, Zarkower D. 1999a. A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8:989-996.
41. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D. 1999b. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208-220.
42. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D. 2000. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587-2595.
43. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T. 2000. Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Cell Genet 89:252-257.
44. Shen WH, Moore CC, Ikeda Y, Parker KL, Ingraham HA. 1994. Nuclear receptor steroidogenic factor 1 regulates the Müllerian inhibiting substance gene: A link to the sex determination cascade. Cell 77:651-661.
45. Smith CA, Andrews JE, Sinclair AH. 1997. Gonadal sex differentiation in chicken embryos: Expression of estrogen receptor and aromatase genes. J Steroid Biochem Mol Biol 60:295-302.
46. Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH. 1999a. Conservation of a sex-determining gene. Nature 402:601-602.
47. Smith CA, Smith MJ, Sinclair AH. 1999b. Expression of chicken steroidogenic factor-1 during gonadal sex differentiation. Gen Comp Endocrinol 113:187-196.
48. Swain A, Lovell-Badge R. 1999. Mammalian sex determination: A molecular drama. Genes Dev 13:755-767.
49. Tremblay JJ, Viger RS. 2001. Nuclear receptor Dax-1 represses the transcriptional cooperation between GATA-4 and SF-1 in Sertoli cells. Biol Reprod 64:1191-1199.
50. Tremblay JJ, Robert NH, Viger RS. 2001. Modulation of endogenous GATA-4 activity reveals its dual contribution to Müllerian inhibiting substance gene transcription in Sertoli cells. Mol Endocrinol 15:1636-1650.
51. Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T. 2000. Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741-2750.
52. Ukeshima A, Fujimoto T. 1991. A fine morphological study of germ cells in asymmetrically developing right and left ovaries of the chick. Anat Rec 230:378-386.
53. Vaillant S, Magre S, Dorizzi M, Pieau C, Richard-Mercier N. 2001. Expression of AMH, SF1 and SOX9 in gonads of genetic female chickens during sex reversal induced by an aromatase inhibitor. Dev Dyn 222:228-237.
54. Vainio S, Heikkilä M, Kispert A, Chin N, McMahon AP. 1999. Female development in mammals is regulated by Wnt-4 signalling. Nature 397:405-409.
55. Van Limborgh J. 1968. Le premier indice de la différenciation sexuelle des gonades chez l'embryon de poulet. Arch Anat Microsc 57:79-90.
56. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. 2001. Sox9 induces testis development in XX transgenic mice. Nat Genet 28:216-217.
57. Viger RS, Mertineit C, Trasler JM, Nemer M. 1998. Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Müllerian inhibiting substance promoter. Development 125:2665-2675.
58. Vigier B, Tran D, du Mesnil du Buisson F, Heyman Y, Josso N. 1983. Use of monoclonal antibody techniques to study the ontogeny of bovine anti-Mullerian hormone. J Reprod Fertil 69:207-214.
59. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E. 1994. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79:1111-1120.
60. Yoshida K, Shimada K, Saito N. 1996. Expression of P450(17 alpha) hydroxylase and P450 aromatase genes in the chicken gonad before and after sexual differentiation. Gen Comp Endocrinol 102:233-240.