Please wait a minute...
Journal of Integrative Agriculture  2013, Vol. 12 Issue (1): 127-135    DOI: 10.1016/S2095-3119(13)60213-0
ANIMAL SCIENCE · VETERINARY SCIENCE Advanced Online Publication | Current Issue | Archive | Adv Search |
Expression of Sex-RelatedGenes in Chicken Embryos During Male-to-Female Sex Reversal Exposure to Diethylstilbestrol
 FANG Li-xiu, XIN Rui, CHEYi, XU Shi-qing
Department of Applied Biology, Medical College, Soochow University, Suzhou 215123, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  Sex emerges out of a delicate dance between a variety of promale, anti-male, and possibly profemale genes. To investigate the role that sex-related genes play in sex determination and gonadal differentiation of fowl, we constructed a male-tofemale sex-reversal model of chick induced by diethylstilbestrol (DES) at onset of incubation (E0). The results of semiquantitative PCR showed that the expression of Sf1, the orphan nuclear receptor steroidogenic factor-1 gene, was put forward from E7d to E5d and up-regulated during E5-7d; the Dmrt1, the double sex and the Mab-3 related to transcription factor 1 gene, was down-regulated during E3-7d. Meanwhile, anti-Müllerian hormone gene (Amh) expressed at a similar level in the genetic females and sex-reversal females before E7d, while no expression products of the three female-specific genes Wpkci, Fet1 and Foxl2 were detected in male-to-female embryos. These findings suggest that the expression of some certain sex-related genes, induced by the exogenous estrogen during period of sex determination and gonadal differentiation, results in the male-to-female sex reversal. Moreover, high activity of Sf1 gene during E5-7d might be related to the profemale process, while low activity of Dmrt1 gene during E3-5d might be anti-male. The expression activity of Amh gene might only contribute to the promale process after E7d, however, it is possibly not an anti-female gene in chick embryos.

Abstract  Sex emerges out of a delicate dance between a variety of promale, anti-male, and possibly profemale genes. To investigate the role that sex-related genes play in sex determination and gonadal differentiation of fowl, we constructed a male-tofemale sex-reversal model of chick induced by diethylstilbestrol (DES) at onset of incubation (E0). The results of semiquantitative PCR showed that the expression of Sf1, the orphan nuclear receptor steroidogenic factor-1 gene, was put forward from E7d to E5d and up-regulated during E5-7d; the Dmrt1, the double sex and the Mab-3 related to transcription factor 1 gene, was down-regulated during E3-7d. Meanwhile, anti-Müllerian hormone gene (Amh) expressed at a similar level in the genetic females and sex-reversal females before E7d, while no expression products of the three female-specific genes Wpkci, Fet1 and Foxl2 were detected in male-to-female embryos. These findings suggest that the expression of some certain sex-related genes, induced by the exogenous estrogen during period of sex determination and gonadal differentiation, results in the male-to-female sex reversal. Moreover, high activity of Sf1 gene during E5-7d might be related to the profemale process, while low activity of Dmrt1 gene during E3-5d might be anti-male. The expression activity of Amh gene might only contribute to the promale process after E7d, however, it is possibly not an anti-female gene in chick embryos.
Keywords:  sex reversal       diethylstilbestrol       chicken       sex determination       sexual differentiation       sex-related gene  
Received: 20 July 2011   Accepted:
Fund: 

This work was supported by the National Key Technology R&D Program of China (2007BAD72B01) and the National High Technology R&D Program of China (2011AA100306).

Corresponding Authors:  Correspondence XU Shi-qing, Tel: +86-512-65880185, Fax: +86-512-65880186, E-mail: szsqxu@suda.edu.cn   

Cite this article: 

FANG Li-xiu, XIN Rui, CHEYi , XU Shi-qing. 2013. Expression of Sex-RelatedGenes in Chicken Embryos During Male-to-Female Sex Reversal Exposure to Diethylstilbestrol. Journal of Integrative Agriculture, 12(1): 127-135.

[1]Berg C, Halldin K, Fridolfsson A K, Brandt I, Brunström B.1999. The avian egg as a test system for endocrinedisrupters : ef fects of di e thylst i lbest rol andethynylestradiol on sex organ development. Science ofthe Total Environment, 233, 57-66

[2]Ellegren H. 2002. Dosage compensation: do birds do it aswell? Trends in Genetics, 18, 25-28

[3]Feng Y, Zhang S, Peng X, Yuan J, Yang Y, Zhan H, Gong Y.2007. Expression analysis of genes putatively involvedin chicken gonadal development. Acta BiologicaHungarica, 58, 163-172

[4]Ferguson-Smith M. 2007. The evolution of sexchromosomes and sex determination in vertebrates andthe key role of DMRT. Sexual Development, 1, 2-11

[5]Govoroun M S, Pannetier M, Pailhoux E, Cocquet J, BrillardJ P, Couty I, Batellier F, Cotinot C. 2004. Isolation ofchicken homolog of the FOXL2 gene and comparisonof its expression patterns with those of aromatase duringovarian development. Developmental Dynamics, 231,859-870

[6]Guichard A, Cedard L, Mignot T M, Scheib D, Haffen K A.1979. Radioimmunoassay of steroids produced by chickembryo gonads cultured in the presence of someexogenous steroid precursors. General andComparative Endocrinology, 39, 9-19

[7]Hudson Q J, Smith C A, Sinclair A H. 2005. Aromataseinhibition reduces expression of FOXL2 in theembryonic chicken ovary. Developmental Dynamics,233, 1052-1055

[8]Ikeda Y, Shen W H, Ingraham H A, Parker K L.1994.Developmental expression of mouse steroidogenicfactor-1, an essential regulator of the steroidhydroxylases

[9]Molecular Endocrinology, 8, 654-662

[10]Kent J, Wheatley S C, Andrews J E, Sinclair A H, KoopmanP. 1996. A male-specific role for SOX9 in vertebrate sexdetermination. Development, 122, 2813-2822

[11]Kozelka A W, Gallagher T F. 1934. Effect of male hormoneextracts, theelin, and theelol on the chick embryo.Proceedings of the Society for Experimental Biologyand Medicine, 31, 1143-1144

[12]Luo X, Ikeda Y, Parker K L. 1994. A cell-specific nuclear receptor is essential for adrenal and gonadaldevelopment and sexual differention. Cell, 77, 481-490

[13]McQueen H A, Mc Bride D, Miele G, Bird A P, Clinton M.2001. Dosage compensation in birds. Current Biology,11,253-257

[14]Münsterberg A, Lovell-Badge R. 1991. Expression of themouse anti-Müllerian hormone gene suggests a role inboth male and female sex differentiation. Development,113, 613-624

[15]Nachtigal M W, Hirokawa Y, Enyeart-Van Houten D L,Flanagan J N, Hammer G D, Ingraham HA. 1998.Wilms’tumor 1 and Dax-1 modulate the orphan nuclear receptorSF-1 in sex-specific gene expression

[16]Cell, 93, 445-454

[17]Nishikimi H, Kansaku N, Saito N, Usami M, Ohno Y,Shimada K. 2000. Sex differentiation and mRNAexpression of P450c17, P450arom and AMH in gonadsof the chicken. Molecular Reproduction andDevelopment, 55, 20-30

[18]Orlando E F, Guillette Jr L J. 2007. Sexual dimorphicresponses in wildlife exposed to endocrine disruptingchemicals. Environmental Research, 104, 163-173

[19]Raymond C S, Kettlewell J R, Hirsch B, Bardwell V J,Zarkower D. 1999. Expression of Dmrt1 in the genitalridge of mouse and chicken embryos suggests a role invertebrate sexual development. Developmental Biology,215, 208-220

[20]Reed K J, SinclairAH. 2002. FET-1: a novelW-linked, femalespecific gene up-regulated in the embryonic chickenovary Mechanical Engineering, 119, S87-S90.

[21]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 andsteroidogenic factor 1 regulates transcription of thehuman anti-müllerian hormone gene. Molecular andCellular Biology, 18, 6653-6665

[22]Scheib D 1983. Effects and role of estrogens in aviangonadal differentiation. Differentiation, 23, 87-92

[23]Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T.2000. Sex-specific expression of an evolutionarilyconserved male regulatory gene, DMRT1, in birds.Cytogenetics and Cell Genetics, 89, 252-257

[24]Smith CA, KatzM, SinclairAH. 2003. DMRT1 is upregulatedin the gonads during female-to-male sex reversal in ZWchicken embryos. Biology of Reproduction, 68, 560-570

[25]Smith CA,Matthijs J S,Andrew H S. 1999a. Gene expressionduring gonadogenesis in the chicken embryo. Gene,234, 395-402

[26]Smith C A, Smith M J, Sinclair A H. 1999b. Expression ofchicken steroidogenic factor-1 during gonadal sexdif ferentiation General and Comparati v eEndocrinology, 113, 187-196

[27]Vaillant S, Magre S, Dorizzi M, Pieau C, Richard-Mercier N.2001. Expression of AMH, SF1, and SOX9 in gonads ofgenetic female chickens during sex reversal induced byan aromatase inhibitor. Developmental Dynamics, 222,228-237

[28]WallisM C,Waters P D, Graves JA. 2008. Sex determinationin mammals - before and after the evolution of SRY.Cellular and Molecular Life Sciences, 65, 3182.

[29]Zheng J X, Yang N. 2007. mRNA expression of genes relatedto avian sex determination during female-to-male sexreversal in ZW chicken embryos. Yi Chuan, 29, 81-86

[30](in Chinese)Zhou M, Maeda T, Xu S Q. 2008. Effect of diethylstilbestrolon feminization of chicken fertile eggs. Bulletin ofScience and Technology, 24, 177-182. (in Chinese)
[1] Tengfei Wang, Changyong Fan, Yufei Xiao, Shan Lü, Guangyang Jiang, Mengyun Zou, Yingjie Wang, Qiao Guo, Zhenghao Che, Xiuli Peng. Protection of chickens from Mycoplasma gallisepticum through the MAPK/ERK/JNK pathway by a compound of ten Chinese medicine formulas[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2356-2370.
[2] Guangzheng Liu, Wenjie Ren, Kai Jin, Dan Zheng, Qisheng Zuo, Yani Zhang, Guohong Chen, Bichun Li, Yingjie Niu. PGC-mediated conservation strategies for germplasm resources of Rugao Yellow chicken and Shouguang chicken in China[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2327-2341.
[3] Jie Zhao, Sa Xiao, Wei Yao, Xudong Chang, Xinglong Wang, Zengqi Yang, Wenbin Wang. Velogenic Newcastle disease virus invades chicken brain by infecting brain microvascular endothelial cells to increase blood-brain barrier permeability[J]. >Journal of Integrative Agriculture, 2025, 24(2): 712-723.
[4] Yuanmei Wang, Jingwei Yuan, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen. Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken[J]. >Journal of Integrative Agriculture, 2025, 24(2): 697-711.
[5] Yanxing Wang, Haigang Ji, Liyang He, Yufang Niu, Yushi Zhang, Yang Liu, Yadong Tian, Xiaojun Liu, Hong Li, Xiangtao Kang, Yanling Gao, Zhuanjian Li. Establishment and analysis of a chicken skeletal muscle satellite cell line using TERT[J]. >Journal of Integrative Agriculture, 2025, 24(11): 4370-4378.
[6] Wenya Li, Haoxiang Ma, Yanxing Wang, Yushi Zhang, Yang Liu, Ruili Han, Hong Li, Hanfang Cai, Xiaojun Liu, Xiangtao Kang, Ruirui Jiang, Zhuanjian Li. The VGLL2 gene participates in muscle development in Gushi chickens[J]. >Journal of Integrative Agriculture, 2025, 24(1): 246-260.
[7] Lei Shi, Yanyan Sun, Yunlei Li, Hao Bai, Jingwei Yuan, Hui Ma, Yuanmei Wang, Panlin Wang, Aixin Ni, Linlin Jiang, Pingzhuang Ge, Shixiong Bian, Yunhe Zong, Jinmeng Zhao, Adamu M. Isa, Hailai H. Tesfay, Jilan Chen. Asymmetric expression of CA2 and CA13 linked to calcification in the bilateral mandibular condyles cause crossed beaks in chickens[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2379-2390.
[8] Ying Ding, Qiong Zhi, Qisheng Zuo, Kai Jin, Wei Han, Bichun Li.

Transcriptome-based analysis of key signaling pathways affecting the formation of primordial germ cell in chickens [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1644-1657.

[9] Lingzhai Meng, Mengmeng Yu, Suyan Wang, Yuntong Chen, Yuanling Bao, Peng Liu, Xiaoyan Feng, Tana He, Ru Guo, Tao Zhang, Mingxue Hu, Changjun Liu, Xiaole Qi, Kai Li, Li Gao, Yanping Zhang, Hongyu Cui, Yulong Gao.

A novel live attenuated vaccine candidate protects chickens against subtype B avian metapneumovirus [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1658-1670.

[10] Qin Ma, Zizhen Fan, Ping Wang, Siya Ma, Jian Wen, Fengqin Cao, Xianwu Lin, Rihui Yan.

Silencing transformer and transformer-2 in Zeugodacus cucurbitae causes defective sex determination with inviability of most pseudomales [J]. >Journal of Integrative Agriculture, 2024, 23(3): 938-947.

[11] Youli Wang, Huajin Zhou, Jing Chen, Yuqin Wu, Yuming Guo, Bo Wang, Jianmin Yuan. Retinol is involved in the intestinal regeneration and strengthens the intestinal barrier during refeeding in broiler chickens[J]. >Journal of Integrative Agriculture, 2024, 23(11): 3843-3859.
[12] WANG Jie, LEI Qiu-xia, CAO Ding-guo, ZHOU Yan, HAN Hai-xia, LIU Wei, LI Da-peng, LI Fu-wei, LIU Jie. Whole genome SNPs among 8 chicken breeds enable identification of genetic signatures that underlie breed features[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2200-2212.
[13] ZHAO Ruo-nan, CHEN Si-yuan, TONG Cui-hong, HAO Jie, LI Pei-si, XIE Long-fei, XIAO Dan-yu, ZENG Zhen-ling, XIONG Wen-guang. Insights into the effects of pulsed antimicrobials on the chicken resistome and microbiota from fecal metagenomes[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1857-1869.
[14] WANG Yong-li, HUANG Chao, YU Yang, CAI Ri-chun, SU Yong-chun, CHEN Zhi-wu, ZHENG Maiqing, CUI Huan-xian.

Dietary aflatoxin B1 induces abnormal deposition of melanin in the corium layer of the chicken shank possibly via promoting the expression of melanin synthesis-related genes [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1847-1856.

[15] SHAN Yan-ju, JI Gai-ge, ZHANG Ming, LIU Yi-fan, TU Yun-jie, JU Xiao-jun, SHU Jing-ting, ZOU Jian-min. Use of transcriptome sequencing to explore the effect of CSRP3 on chicken myoblasts[J]. >Journal of Integrative Agriculture, 2023, 22(4): 1159-1171.
No Suggested Reading articles found!