The transcription factor Sox30 is involved in Nile tilapia spermatogenesis

Ling Wei; Yaohao Tang; Xianhai Zeng; Yueqin Li; Song Zhang; Li Deng; Lingsong Wang; Deshou Wang

doi:10.1016/j.jgg.2021.11.003

Volume 49 Issue 7

Jul. 2022

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Article Navigation > Journal of Genetics and Genomics > 2022 > 49(7): 666-676

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The transcription factor Sox30 is involved in Nile tilapia spermatogenesis

doi: 10.1016/j.jgg.2021.11.003

Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, China

Funds:

This study was supported by grants from the National Natural Science Foundation of China (31772831 and 31302170, 31861123001) and the National Key Research and Development Program of China (2018YFD0900202).

Received Date: 2021-07-22
Accepted Date: 2021-11-07
Rev Recd Date: 2021-11-04
Publish Date: 2021-11-18

Abstract

Abstract

Spermatogenesis is a complex process in which spermatogonial stem cells differentiate and develop into mature spermatozoa. The transcriptional regulatory network involved in fish spermatogenesis remains poorly understood. Here, we demonstrate in Nile tilapia that the Sox transcription factor family member Sox30 is specifically expressed in the testes and mainly localizes to spermatocytes and spermatids. CRISPR/Cas9-mediated sox30 mutation results in abnormal spermiogenesis, reduction of sperm motility, and male subfertility. Comparative transcriptome analysis shows that sox30 mutation alters the expression of genes involved in spermatogenesis. Further chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq), ChIP-PCR, and luciferase reporter assays revealed that Sox30 positively regulates the transcription of ift140 and ptprb, two genes involved in spermiogenesis, by directly binding to their promoters. Our data, taken together, indicate that Sox30 plays an essential role in Nile tilapia spermatogenesis by directly regulating the transcription of the spermiogenesis-related genes ift140 and ptprb.
- Nile tilapia,
- Sox30,
- Spermatogenesis,
- Transcriptional regulation

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References(46)

References

Angelozzi, M., Lefebvre, V., 2019. SOXopathies:Growing family of developmental disorders due to SOX mutations. Trends Genet. 35, 658-671

Bai, S., Fu, K., Yin, H., Cui, Y., Yue, Q., Li, W., Cheng, L., Tan, H., Liu, X., Guo, Y., Zhang, Y., Xie, J., He, W., Wang, Y., Feng, H., Xin, C., Zhang, J., Lin, M., Shen, B., Sun, Z., Guo, X., Zheng, K., Ye, L., 2018. Sox30 initiates transcription of haploid genes during late meiosis and spermiogenesis in mouse testes. Development 145, dev164855

Cavaco, J.E., Bogerd, J., Goos, H., Schulz, R.W., 2001. Testosterone inhibits 11-ketotestosterone-induced spermatogenesis in African catfish (Clarias gariepinus). Biol. Reprod. 65, 1807-1812

Cavaco, J.E., Vilrokx, C., Trudeau, V.L., Schulz, R.W., Goos, H.J., 1998. Sex steroids and the initiation of puberty in male African catfish (Clarias gariepinus). Am. J. Physiol. 275, R1793-1802

Chocu, S., Calvel, P., Rolland, A.D., Pineau, C., 2012. Spermatogenesis in mammals:proteomic insights. Syst. Biol. Reprod. Med. 58, 179-190

Chu, L., Li, J., Liu, Y., Cheng, C.H., 2015. Gonadotropin signaling in zebrafish ovary and testis development:Insights from gene knockout study. Mol. Endocrinol. 29, 1743-1758

Dai, X., Cheng, X., Huang, J., Gao, Y., Wang, D., Feng, Z., Zhai, G., Lou, Q., He, J., Wang, Z., Yin, Z., 2021. Rbm46, a novel germ cell specific factor, modulates meiotic progression and spermatogenesis. Biol. Reprod. 104, 1139-1153

de Kretser, D.M., Loveland, K.L., Meinhardt, A., Simorangkir, D., Wreford, N., 1998. Spermatogenesis. Hum. Reprod. 13 Suppl 1, 1-8

Feng, C.A., Spiller, C., Merriner, D.J., O'Bryan, M.K., Bowles, J., Koopman, P., 2017. SOX30 is required for male fertility in mice. Sci. Rep. 7, 17619

Gonzalez-Fernandez, L., Ortega-Ferrusola, C., Macias-Garcia, B., Salido, G.M., Pena, F.J., Tapia, J.A., 2009. Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biol. Reprod. 80, 1239-1252

Gopalakrishnan, B., Shaha, C., 1998. Inhibition of sperm glutathione S-transferase leads to functional impairment due to membrane damage. FEBS. Lett. 422, 296-300

Han, F., Wang, Z., Wu, F., Liu, Z., Huang, B., Wang, D., 2010. Characterization, phylogeny, alternative splicing and expression of Sox30 gene. BMC Mol. Biol. 11, 98

Hess, R.A., Renato de Franca, L., 2008. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp. Med. Biol. 636, 1-15

Jiang, T., Hou, C.C., She, Z.Y., Yang, W.X., 2013. The SOX gene family:function and regulation in testis determination and male fertility maintenance. Mol. Biol. Rep. 40, 2187-2194

Lehti, M.S., Sironen, A., 2016. Formation and function of the manchette and flagellum during spermatogenesis. Reproduction 151, R43-54

Li, M., Liu, X., Dai, S., Xiao, H., Qi, S., Li, Y., Zheng, Q., Jie, M., Cheng, C.H.K., Wang, D., 2020. Regulation of spermatogenesis and reproductive capacity by Igf3 in tilapia. Cell Mol. Life Sci. 77, 4921-4938

Li, M., Yang, H., Zhao, J., Fang, L., Shi, H., Li, M., Sun, Y., Zhang, X., Jiang, D., Zhou, L., Wang, D., 2014. Efficient and heritable gene targeting in tilapia by CRISPR/Cas9. Genetics 197, 591-599

Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-△△C_T Method. Methods 25, 402-408

Marques, L.S., Fossati, A.A., Leal, M.S., Rodrigues, R.B., Bombardelli, R.A., Streit, D.P., Jr., 2018. Viability assessment of primary growth oocytes following ovarian tissue vitrification of neotropical teleost pacu (Piaractus mesopotamicus). Cryobiology 82, 118-123

Melo, M.C., van Dijk, P., Andersson, E., Nilsen, T.O., Fjelldal, P.G., Male, R., Nijenhuis, W., Bogerd, J., de Franca, L.R., Taranger, G.L., Schulz, R.W., 2015. Androgens directly stimulate spermatogonial differentiation in juvenile Atlantic salmon (Salmo salar). Gen. Comp. Endocrinol. 211, 52-61

Mitchison, H.M., Schmidts, M., Loges, N.T., Freshour, J., Dritsoula, A., Hirst, R.A., O'Callaghan, C., Blau, H., Al Dabbagh, M., Olbrich, H., Beales, P.L., Yagi, T., Mussaffi, H., Chung, E.M., Omran, H., Mitchell, D.R., 2012. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat. Genet. 44, 381-389

Miura, T., Yamauchi, K., Takahashi, H., Nagahama, Y., 1991. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc. Natl. Acad. Sci. U S A 88, 5774-5778

Nakamura, S., Watakabe, I., Nishimura, T., Toyoda, A., Taniguchi, Y., Tanaka, M., 2012. Analysis of medaka sox9 orthologue reveals a conserved role in germ cell maintenance. PLoS One 7, e29982

Nantel, F., Monaco, L., Foulkes, N.S., Masquilier, D., LeMeur, M., Henriksen, K., Dierich, A., Parvinen, M., Sassone-Corsi, P., 1996. Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380, 159-162

Nobrega, R.H., Batlouni, S.R., Franca, L.R., 2009. An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiol. Biochem. 35, 197-206

Oakes, J.A., Barnard, L., Storbeck, K.H., Cunliffe, V.T., Krone, N.P., 2020. 11beta-Hydroxylase loss disrupts steroidogenesis and reproductive function in zebrafish. J. Endocrinol. 247, 197-212

Osaki, E., Nishina, Y., Inazawa, J., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Ohsugi, M., Tezuka, T., Yoshida, M., Semba, K., 1999. Identification of a novel Sry-related gene and its germ cell-specific expression. Nucleic Acids Res. 27, 2503-2510

Pudney, J., 1995. Spermatogenesis in nonmammalian vertebrates. Microsc. Res. Tech. 32, 459-497

Qu, W., Yuan, S., Quan, C., Huang, Q., Zhou, Q., Yap, Y., Shi, L., Zhang, D., Guest, T., Li, W., Yee, S.P., Zhang, L., Cazin, C., Hess, R.A., Ray, P.F., Kherraf, Z.E., Zhang, Z., 2020. The essential role of intraflagellar transport protein IFT81 in male mice spermiogenesis and fertility. Am. J. Physiol. Cell Physiol. 318, C1092-C1106

San Agustin, J.T., Pazour, G.J., Witman, G.B., 2015. Intraflagellar transport is essential for mammalian spermiogenesis but is absent in mature sperm. Mol. Biol. Cell 26, 4358-4372

Schulz, R.W., de Franca, L.R., Lareyre, J.J., Le Gac, F., Chiarini-Garcia, H., Nobrega, R.H., Miura, T., 2010. Spermatogenesis in fish. Gen. Comp. Endocrinol. 165, 390-411

Steger, K., Klonisch, T., Gavenis, K., Behr, R., Schaller, V., Drabent, B., Doenecke, D., Nieschlag, E., Bergmann, M., Weinbauer, G.F., 1999. Round spermatids show normal testis-specific H1t but reduced cAMP-responsive element modulator and transition protein 1 expression in men with round-spermatid maturation arrest. J. Androl. 20, 747-754

Tang, Y., Li, X., Xiao, H., Li, M., Li, Y., Wang, D., Wei, L., 2019. Transcription of the Sox30 gene is positively regulated by Dmrt1 in Nile tilapia. Int. J. Mol. Sci. 20, 5487

Wang, S., Wang, X., Ma, L., Lin, X., Zhang, D., Li, Z., Wu, Y., Zheng, C., Feng, X., Liao, S., Feng, Y., Chen, J., Hu, X., Wang, M., Han, C., 2016. Retinoic acid is sufficient for the in vitro induction of mouse spermatocytes. Stem Cell Reports 7, 80-94

Wei, L., Li, X., Li, M., Tang, Y., Wei, J., Wang, D., 2019. Dmrt1 directly regulates the transcription of the testis-biased Sox9b gene in Nile tilapia (Oreochromis niloticus). Gene 687, 109-115

Wei, L., Yang, C., Tao, W., Wang, D., 2016. Genome-wide identification and transcriptome-based expression profiling of the Sox gene family in the Nile tilapia (Oreochromis niloticus). Int. J. Mol. Sci. 17, 270

Xie, H., Kang, Y., Wang, S., Zheng, P., Chen, Z., Roy, S., Zhao, C., 2020. E2f5 is a versatile transcriptional activator required for spermatogenesis and multiciliated cell differentiation in zebrafish. PLoS Genet. 16, e1008655

Zhang, D., Xie, D., Lin, X., Ma, L., Chen, J., Zhang, D., Wang, Y., Duo, S., Feng, Y., Zheng, C., Jiang, B., Ning, Y., Han, C., 2018a. The transcription factor SOX30 is a key regulator of mouse spermiogenesis. Development 145, dev164723

Zhang, Q., Ye, D., Wang, H., Wang, Y., Hu, W., Sun, Y., 2020. Zebrafish cyp11c1 knockout reveals the roles of 11-ketotestosterone and cortisol in sexual development and reproduction. Endocrinology 161, bqaa048

Zhang, T., Song, W., Li, Z., Qian, W., Wei, L., Yang, Y., Wang, W., Zhou, X., Meng, M., Peng, J., Xia, Q., Perrimon, N., Cheng, D., 2018b. Kruppel homolog 1 represses insect ecdysone biosynthesis by directly inhibiting the transcription of steroidogenic enzymes. Proc. Natl. Acad. Sci. U S A 115, 3960-3965

Zhang, X., Wang, H., Li, M., Cheng, Y., Jiang, D., Sun, L., Tao, W., Zhou, L., Wang, Z., Wang, D., 2014. Isolation of doublesex- and mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia. Biol. Reprod. 91, 136

Zhang, Y., Liu, H., Li, W., Zhang, Z., Shang, X., Zhang, D., Li, Y., Zhang, S., Liu, J., Hess, R.A., Pazour, G.J., Zhang, Z., 2017. Intraflagellar transporter protein (IFT27), an IFT25 binding partner, is essential for male fertility and spermiogenesis in mice. Dev. Biol. 432, 125-139

Zhang, Y., Liu, H., Li, W., Zhang, Z., Zhang, S., Teves, M.E., Stevens, C., Foster, J.A., Campbell, G.E., Windle, J.J., Hess, R.A., Pazour, G.J., Zhang, Z., 2018c. Intraflagellar transporter protein 140 (IFT140), a component of IFT-A complex, is essential for male fertility and spermiogenesis in mice. Cytoskeleton (Hoboken) 75, 70-84

Zhang, Z., Li, W., Zhang, Y., Zhang, L., Teves, M.E., Liu, H., Strauss, J.F., 3rd, Pazour, G.J., Foster, J.A., Hess, R.A., Zhang, Z., 2016. Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice. Mol. Biol. Cell 27, 3705-3716

Zhang, Z., Zhu, B., Ge, W., 2015. Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption. Mol. Endocrinol. 29, 76-98

Zheng, Q., Xiao, H., Shi, H., Wang, T., Sun, L., Tao, W., Kocher, T.D., Li, M., Wang, D., 2020. Loss of Cyp11c1 causes delayed spermatogenesis due to the absence of 11-ketotestosterone. J. Endocrinol. 244, 487-499

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