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Reproductive Biology and Endocrinology

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Open Access 01-12-2013 | Research

Sex-specific expression of CTNNB1 in the gonadal morphogenesis of the chicken

Authors: Seung-Min Bae, Whasun Lim, Wooyoung Jeong, Jin-Young Lee, Jinyoung Kim, Fuller W Bazer, Gwonhwa Song

Published in: Reproductive Biology and Endocrinology | Issue 1/2013

Abstract

Background

Beta-catenin (CTNNB1), as a key transcriptional regulator in the WNT signal transduction cascade, plays a pivotal role in multiple biological functions such as embryonic development and homeostasis in adults. Although it has been suggested that CTNNB1 is required for gonad development and maintenance of ovarian function in mice, little is known about the expression and functional role of CTNNB1 in gonadal development and differentiation in the chicken reproductive system.

Methods

To examine sex-specific, cell-specific and temporal expression of CTNNB1 mRNA and protein during gonadal development to maturation of reproductive organs, we collected left and right gonads apart from mesonephric kidney of chicken embryos on embryonic day (E) 6, E9, E14, E18, as well as testes, oviduct and ovaries from 12-week-old and adult chickens and performed quantitative PCR, in situ hybridization, and immunohistochemical analyses. In addition, localization of Sertoli cell markers such as anti-Müllerian hormone (AMH), estrogen receptor alpha (ESR1), cyclin D1 (CCND1) and N-cadherin (CDH2) during testicular development was evaluated.

Results

Results of the present study showed that CTNNB1 mRNA and protein are expressed predominantly in the seminiferous cords on E6 to E14 in the male embryonic gonad, and are mainly localized to the medullary region of female embryonic gonads from E6 to E9. In addition, CTNNB1 mRNA and protein are abundant in the Sertoli cells in the testes and expressed predominantly in luminal epithelial cells of the oviduct, but not in the ovaries from 12-week-old and adult chickens. Concomitant with CTNNB1, AMH, ESR1, CCND1 and CDH2 were detected predominantly in the seminiferous cord of the medullary region of male gonads at E9 (after sex determination) and then maintained or decreased until hatching. Interestingly, AMH, ESR1, CCND1 and CDH2 were located in seminiferous tubules of the testes from 12-weeks-old chickens and ESR1, CCND1 and CDH2 were expressed predominantly in the Sertoli cells within seminiferous tubules of adult testes.

Conclusions

Collectively, these results revealed that CTNNB1 is present in gonads of both sexes during embryonic development and it may play essential roles in differentiation of Sertoli cells during formation of seminiferous tubules during development of the testes.

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MacDonald BT, Tamai K, He X: Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009, 17: 9-26. 10.1016/j.devcel.2009.06.016.PubMedCentralCrossRefPubMed

Logan CY, Nusse R: The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004, 20: 781-810. 10.1146/annurev.cellbio.20.010403.113126.CrossRefPubMed

Kimelman D, Xu W: beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene. 2006, 25: 7482-7491. 10.1038/sj.onc.1210055.CrossRefPubMed

Polakis P: The many ways of Wnt in cancer. Curr Opin Genet Dev. 2007, 17: 45-51. 10.1016/j.gde.2006.12.007.CrossRefPubMed

Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R: Lack of beta-catenin affects mouse development at gastrulation. Development. 1995, 121: 3529-3537.PubMed

Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W: Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol. 2000, 148: 567-578. 10.1083/jcb.148.3.567.PubMedCentralCrossRefPubMed

Liu CF, Bingham N, Parker K, Yao HH: Sex-specific roles of beta-catenin in mouse gonadal development. Hum Mol Genet. 2009, 18: 405-417.PubMedCentralCrossRefPubMed

Hamburger V, Hamilton HL: A series of normal stages in the development of the chick embryo. J Morphol. 1951, 88: 49-10.1002/jmor.1050880104.CrossRefPubMed

Smith CA, Sinclair AH: Sex determination in the chicken embryo. J Exp Zool. 2001, 290: 691-699. 10.1002/jez.1119.CrossRefPubMed

10.

Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH: The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature. 2009, 461: 267-271. 10.1038/nature08298.CrossRefPubMed

11.

Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001, 25: 402-408. 10.1006/meth.2001.1262.CrossRefPubMed

12.

Rey R, Sabourin JC, Venara M, Long WQ, Jaubert F, Zeller WP, Duvillard P, Chemes H, Bidart JM: Anti-Mullerian hormone is a specific marker of sertoli- and granulosa-cell origin in gonadal tumors. Hum Pathol. 2000, 31: 1202-1208. 10.1053/hupa.2000.18498.CrossRefPubMed

13.

Saunders PT, Fisher JS, Sharpe RM, Millar MR: Expression of oestrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis. J Endocrinol. 1998, 156: R13-17. 10.1677/joe.0.156R013.CrossRefPubMed

14.

Yamashita S: Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats. Anat Rec A Discov Mol Cell Evol Biol. 2004, 279: 768-778.CrossRefPubMed

15.

Albrecht ED, Billiar RB, Aberdeen GW, Babischkin JS, Pepe GJ: Expression of estrogen receptors alpha and beta in the fetal baboon testis and epididymis. Biol Reprod. 2004, 70: 1106-1113.CrossRefPubMed

16.

Mruk DD, Cheng CY: Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev. 2004, 25: 747-806. 10.1210/er.2003-0022.CrossRefPubMed

17.

MacCalman CD, Getsios S, Farookhi R, Blaschuk OW: Estrogens potentiate the stimulatory effects of follicle-stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology. 1997, 138: 41-48. 10.1210/en.138.1.41.PubMed

18.

Xing Y, Takemaru K, Liu J, Berndt JD, Zheng JJ, Moon RT, Xu W: Crystal structure of a full-length beta-catenin. Structure. 2008, 16: 478-487. 10.1016/j.str.2007.12.021.PubMedCentralCrossRefPubMed

19.

Lu J, Chuong CM, Widelitz RB: Isolation and characterization of chicken beta-catenin. Gene. 1997, 196: 201-207. 10.1016/S0378-1119(97)00228-X.CrossRefPubMed

20.

Smith CA, Sinclair AH: Sex determination: insights from the chicken. Bioessays. 2004, 26: 120-132. 10.1002/bies.10400.CrossRefPubMed

21.

Behringer RR, Finegold MJ, Cate RL: Mullerian-inhibiting substance function during mammalian sexual development. Cell. 1994, 79: 415-425. 10.1016/0092-8674(94)90251-8.CrossRefPubMed

22.

Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR: Genetic studies of the AMH/MIS signaling pathway for Mullerian duct regression. Mol Cell Endocrinol. 2003, 211: 15-19. 10.1016/j.mce.2003.09.006.CrossRefPubMed

23.

Xavier F, Allard S: Anti-Mullerian hormone, beta-catenin and Mullerian duct regression. Mol Cell Endocrinol. 2003, 211: 115-121. 10.1016/j.mce.2003.09.022.CrossRefPubMed

24.

Allard S, Adin P, Gouedard L, di Clemente N, Josso N, Orgebin-Crist MC, Picard JY, Xavier F: Molecular mechanisms of hormone-mediated Mullerian duct regression: involvement of beta-catenin. Development. 2000, 127: 3349-3360.PubMed

25.

Trbovich AM, Martinelle N, O'Neill FH, Pearson EJ, Donahoe PK, Sluss PM, Teixeira J: Steroidogenic activities in MA-10 Leydig cells are differentially altered by cAMP and Mullerian inhibiting substance. J Steroid Biochem Mol Biol. 2004, 92: 199-208. 10.1016/j.jsbmb.2004.07.002.CrossRefPubMed

26.

Hess RA: Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol. 2003, 1: 52-10.1186/1477-7827-1-52.PubMedCentralCrossRefPubMed

27.

Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB, Korach KS: Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology. 1996, 137: 4796-4805. 10.1210/en.137.11.4796.PubMed

28.

Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O: Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA. 1993, 90: 11162-11166. 10.1073/pnas.90.23.11162.PubMedCentralCrossRefPubMed

29.

Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M: Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000, 127: 4277-4291.PubMed

30.

Nei H, Saito T, Yamasaki H, Mizumoto H, Ito E, Kudo R: Nuclear localization of beta-catenin in normal and carcinogenic endometrium. Mol Carcinog. 1999, 25: 207-218. 10.1002/(SICI)1098-2744(199907)25:3<207::AID-MC7>3.0.CO;2-4.CrossRefPubMed

31.

Hou X, Tan Y, Li M, Dey SK, Das SK: Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol. 2004, 18: 3035-3049. 10.1210/me.2004-0259.PubMedCentralCrossRefPubMed

32.

Lucas TF, Pimenta MT, Pisolato R, Lazari MF, Porto CS: 17beta-estradiol signaling and regulation of Sertoli cell function. Spermatogenesis. 2011, 1: 318-324. 10.4161/spmg.1.4.18903.PubMedCentralCrossRefPubMed

33.

Ravnik SE, Rhee K, Wolgemuth DJ: Distinct patterns of expression of the D-type cyclins during testicular development in the mouse. Dev Genet. 1995, 16: 171-178. 10.1002/dvg.1020160209.CrossRefPubMed

34.

Beumer TL, Roepers-Gajadien HL, Gademan IS, Kal HB, de Rooij DG: Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse. Biol Reprod. 2000, 63: 1893-1898. 10.1095/biolreprod63.6.1893.CrossRefPubMed

35.

Zhao J, Pestell R, Guan JL: Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol Biol Cell. 2001, 12: 4066-4077. 10.1091/mbc.12.12.4066.PubMedCentralCrossRefPubMed

36.

D'Amico M, Hulit J, Amanatullah DF, Zafonte BT, Albanese C, Bouzahzah B, Fu M, Augenlicht LH, Donehower LA, Takemaru K, et al: The integrin-linked kinase regulates the cyclin D1 gene through glycogen synthase kinase 3beta and cAMP-responsive element-binding protein-dependent pathways. J Biol Chem. 2000, 275: 32649-32657.CrossRefPubMed

37.

Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A: The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA. 1999, 96: 5522-5527. 10.1073/pnas.96.10.5522.PubMedCentralCrossRefPubMed

38.

Daugherty RL, Gottardi CJ: Phospho-regulation of Beta-catenin adhesion and signaling functions. Physiology (Bethesda). 2007, 22: 303-309. 10.1152/physiol.00020.2007.CrossRef

39.

Heidenberg DJ, Barton JH, Young D, Grinkemeyer M, Sesterhenn IA: N-cadherin expression in testicular germ cell and gonadal stromal tumors. J Cancer Educ. 2012, 3: 381-389.CrossRef

40.

Newton SC, Blaschuk OW, Millette CF: N-cadherin mediates Sertoli cell-spermatogenic cell adhesion. Dev Dyn. 1993, 197: 1-13. 10.1002/aja.1001970102.CrossRefPubMed

41.

Chang YF, Lee-Chang JS, Harris KY, Sinha-Hikim AP, Rao MK: Role of beta-catenin in post-meiotic male germ cell differentiation. PLoS One. 2011, 6: e28039-10.1371/journal.pone.0028039.PubMedCentralCrossRefPubMed

Title: Sex-specific expression of CTNNB1 in the gonadal morphogenesis of the chicken
Authors: Seung-Min Bae
Whasun Lim
Wooyoung Jeong
Jin-Young Lee
Jinyoung Kim
Fuller W Bazer
Gwonhwa Song
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2013
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-11-89

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Springer Medicine

Sex-specific expression of CTNNB1 in the gonadal morphogenesis of the chicken

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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