Study on the role of \(\textit{TDRD1}\) variants in male infertility among 310 Vietnamese individuals

La Duc Duy; Nguyen Minh Nguyet; Huynh Thi Thu Hue; Nguyen Thuy Duong

doi:10.15625/2615-9023/18123

Author affiliations

Authors

La Duc Duy Institute of Genome Research, VAST, Vietnam
Nguyen Minh Nguyet Institute of Genome Research, VAST, Vietnam
Huynh Thi Thu Hue Institute of Genome Research, VAST, Vietnam
Nguyen Thuy Duong Institute of Genome Research, Vietnam Academy of Science and Technology

DOI:

https://doi.org/10.15625/2615-9023/18123

Keywords:

male infertility, PCR-RFLP, rs541192490, rs77559927, TDRD1, Vietnam

Abstract

Infertility is a global reproductive health burden affected by various genetic factors, including spermatogenic defects. The instability of the germ cells’ genome caused by the unregulated replication of transposable elements is one of the causes of spermatogenic impairment. Tudor domain-containing 1 (TDRD1) expressed only in germ cells plays a significant role in the piRNA (PIWI-interacting RNA) pathway to maintain genome integrity via suppressing transposon elements during spermatogenesis. Despite the protein’s role in male germline development, TDRD1 has not been studied intensively. In this study, we established the relationship between male infertility and single nucleotide polymorphisms (SNPs) of TDRD1 (rs541192490, rs77559927) among 310 Vietnamese men (160 infertile patients and 150 healthy controls). Genotypes of single nucleotide polymorphisms of the TDRD1 gene (SNPs) were identified using the PCR-RFLP method. The results showed that TDRD1 SNPs were not associated with male infertility in all three test models (additive, dominant, and recessive) (p-value > 0.05). Haplotype analysis of the two SNPs also showed similar findings. This study would contribute to the knowledge of TDRD1’s association with male infertility in the Vietnamese population.

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References

Anawalt B. D., 2013. Approach to male infertility and induction of spermatogenesis. J. Clin. Endocrinol. Metab., 98: 3532–42. https://doi.org/ 10.1210/jc.2012-2400

Arafat M., Har-Vardi I., Harlev A., Levitas E., Zeadna A., Abofoul-Azab M., Dyomin V., Sheffield V.C., Lunenfeld E., Huleihel M., Parvari R., 2017. Mutation in TDRD9 causes non-obstructive azoospermia in infertile men. J. Med. Genet., 54: 633–639. https://doi.org/10.1136/jmedgenet-2017-104514

Aragon T. J., 2020. Epitools: Epidemiology Tools. https://cran.r-project.org/package= epitools.

Aravin A., Gaidatzis D., Pfeffer S., Lagos-Quintana M., Landgraf P., Iovino N., Morris P., Brownstein M. J., Kuramochi-Miyagawa S., Nakano T., Chien M., Russo J. J., Ju J., Sheridan R., Sander C., Zavolan M., Tuschl T., 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 442: 203–7. https://doi.org/10.1038/nature04916

Aravin A. A., Sachidanandam R., Bourc’his D., Schaefer C., Pezic D., Toth K. F., Bestor T., Hannon G. J., 2008. A piRNA Pathway Primed by Individual Transposons Is Linked to De Novo DNA Methylation in Mice. Mol. Cell, 31:

–99. https://doi.org/10.1016/j.molcel.2008.09.003

Babakhanzadeh E., Khodadadian A., Rostami S., Alipourfard I., Aghaei M., Nazari M., Hosseinnia M., Mehrjardi M. Y. V., Jamshidi Y., Ghasemi N., 2020. Testicular expression of TDRD1, TDRD5, TDRD9 and TDRD12 in azoospermia. BMC Med. Genet: 21. https://doi.org/10.1186/ S12881-020-0970-0

Chuma S., Hosokawa M., Kitamura K., Kasai S., Fujioka M., Hiyoshi M., Takamune K., Noce T., Nakatsuji N., 2006. Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc. Natl. Acad. Sci. U. S. A., 103: 15894–9. https://doi.org/10.1073/pnas.0601878103

Cooke H. J., Saunders P. T. K., 2002. Mouse models of male infertility. Nat. Rev. Genet., 3: 790–801. https://doi.org/ 10.1038/nrg911

Gou L. T., Kang J. Y., Dai P., Wang X., Li F., Zhao S., Zhang M., Hua M. M., Lu Y., Zhu Y., Li Z., Chen H., Wu L. G., Li D., Fu X. D., Li J., Shi H. J., Liu M. F., 2017. Ubiquitination-Deficient Mutations in Human Piwi Cause Male Infertility by Impairing Histone-to-Protamine Exchange during Spermiogenesis. Cell, 169:

–1104. https://doi.org/10.1016/ j.cell.2017.04.034

Graffelman J., 2015. Exploring diallelic genetic markers: The HardyWeinberg package. J. Stat. Softw., 64: 1–23. https://doi.org/10.18637/jss.v064.i03

Gu A., Ji G., Shi X., Long Y., Xia Y., Song L., Wang S., Wang X., 2010. Genetic variants in Piwi-interacting RNA pathway genes confer susceptibility to spermatogenic failure in a Chinese population. Hum. Reprod., 25: 2955–61. https://doi.org/10.1093/humrep/deq274

Hirsh A., 2003. Male subfertility. BMJ, 327: 669–72. https://doi.org/10.1136/ bmj.327.7416.669

Kamaliyan Z., Pouriamanesh S., Soosanabadi M., Gholami M., Mirfakhraie R., 2018. Investigation of piwi-interacting RNA pathway genes role in idiopathic non-obstructive azoospermia. Sci. Rep: 8. https://doi.org/10.1038/S41598-017-17518-4

Kim Y., Choi S. J., Choi C., 2017. An efficient PCR-RFLP method for the rapid identification of Korean pyropia species. Molecules, 22: 2182. https://doi.org/ 10.3390/molecules22122182

Klattenhoff C., Theurkauf W., 2008. Biogenesis and germline functions of piRNAs. Development, 135: 3–9. https://doi.org/10.1242/dev.006486

Kohlrausch F. B., Berteli T. S., Wang F., Navarro P. A., Keefe D. L., 2022. Control of LINE-1 Expression Maintains Genome Integrity in Germline and Early Embryo Development. Reprod. Sci., 29: 328–340. https://doi.org/10.1007/s43032-021-00461-1

Kosova G., Scott N. M., Niederberger C., Prins G. S., Ober C., 2012. Genome-wide association study identifies candidate genes for male fertility traits in humans. Am. J. Hum. Genet., 90: 950–61. https://doi.org/10.1016/j.ajhg.2012.04.016

Krausz C., Escamilla A. R., Chianese C., 2015. Genetics of male infertility: From research to clinic. Reproduction, 150: R159–R174. https://doi.org/10.1530/REP-15-0261

Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., Fitzhugh W., Funke R., Gage D., Harris K., Heaford A., Howland J., Kann L., Lehoczky J., Levine R., McEwan P., McKernan K., Meldrim J., Mesirov J.P., Miranda C., Morris W., Naylor J., Raymond C., Rosetti M., Santos R., Sheridan A., Sougnez C., Stange-Thomann N., Stojanovic N., Subramanian A., Wyman D., Rogers J., Sulston J., Ainscough R., Beck S., Bentley D., Burton J., Clee C., Carter N., Coulson A., Deadman R., Deloukas P., Dunham A., Dunham I., Durbin R., French L., Grafham D., Gregory S., Hubbard T., Humphray S., Hunt A., Jones M., Lloyd C., McMurray A., Matthews L., Mercer S., Milne S., Mullikin J. C., Mungall A., Plumb R., Ross M., Shownkeen R., Sims S., Waterston R. H., Wilson R. K., Hillier L. W., McPherson J. D., Marra M. A., Mardis E. R., Fulton L. A., Chinwalla A. T., Pepin K. H., Gish W. R., Chissoe S. L., Wendl M. C., Delehaunty K. D., Miner T. L., Delehaunty A., Kramer J. B., Cook L. L., Fulton R. S., Johnson D. L., Minx P. J., Clifton S. W., Hawkins T., Branscomb E., Predki P., Richardson P., Wenning S., Slezak T., Doggett N., Cheng J. F., Olsen A., Lucas S., Elkin C., Uberbacher E., Frazier M., Gibbs R. A., Muzny D. M., Scherer S. E., Bouck J. B., Sodergren E. J., Worley K. C., Rives C. M., Gorrell J. H., Metzker M. L., Naylor S. L., Kucherlapati R. S., Nelson D. L., Weinstock G. M., Sakaki Y., Fujiyama A., Hattori M., Yada T., Toyoda A., Itoh T., Kawagoe C., Watanabe H., Totoki Y., Taylor T., Weissenbach J., Heilig R., Saurin W., Artiguenave F., Brottier P., Bruls T., Pelletier E., Robert C., Wincker P., Rosenthal A., Platzer M., Nyakatura G., Taudien S., Rump A., Smith D. R., Doucette-Stamm L., Rubenfield M., Weinstock K., Hong M. L., Dubois J., Yang H., Yu J., Wang J., Huang G., Gu J., Hood L., Rowen L., Madan A., Qin S., Davis R. W., Federspiel N. A., Abola A. P., Proctor M. J., Roe B. A., Chen F., Pan H., Ramser J., Lehrach H., Reinhardt R., McCombie W. R., De La Bastide M., Dedhia N., Blöcker H., Hornischer K., Nordsiek G., Agarwala R., Aravind L., Bailey J. A., Bateman A., Batzoglou S., Birney E., Bork P., Brown D. G., Burge C. B., Cerutti L., Chen H. C., Church D., Clamp M., Copley R. R., Doerks T., Eddy S. R., Eichler E. E., Furey T. S., Galagan J., Gilbert J. G. R., Harmon C., Hayashizaki Y., Haussler D., Hermjakob H., Hokamp K., Jang W., Johnson L. S., Jones T.A., Kasif S., Kaspryzk A., Kennedy S., Kent W.J., Kitts P., Koonin E. V., Korf I., Kulp D., Lancet D., Lowe T.M., McLysaght A., Mikkelsen T., Moran J. V., Mulder N., Pollara V.J., Ponting C. P., Schuler G., Schultz J., Slater G., Smit A. F. A., Stupka E., Szustakowki J., Thierry-Mieg D., Thierry-Mieg J., Wagner L., Wallis J., Wheeler R., Williams A., Wolf Y. I., Wolfe K. H., Yang S. P., Yeh R. F., Collins F., Guyer M. S., Peterson J., Felsenfeld A., Wetterstrand K. A., Myers R. M., Schmutz J., Dickson M., Grimwood J., Cox D. R., Olson M. V., Kaul R., Raymond C., Shimizu N., Kawasaki K., Minoshima S., Evans G. A., Athanasiou M., Schultz R., Patrinos A., Morgan M. J., 2001. Initial sequencing and analysis of the human genome. Nature, 409:

–921. https://doi.org/10.1038/35057062

Lau N. C., Seto A. G., Kim J., Kuramochi-Miyagawa S., Nakano T., Bartel D. P., Kingston R. E., 2006. Characterization of the piRNA complex from rat testes. Science, 313: 363–7. https://doi.org/10.1126/science.1130164

O’Bryan M. K., De Kretser D., Ivell R., Skakkebæk N. E., Almstrup K., Leffers H., 2006. Mouse models for genes involved in impaired spermatogenesis. International Journal of Andrology, 29: 76–89. https://doi.org/10.1111/j.1365-2605.2005.00614.x

Pandey R. R., Tokuzawa Y., Yang Z., Hayashi E., Ichisaka T., Kajita S., Asano Y., Kunieda T., Sachidanandam R., Chuma S., Yamanaka S., Pillai R.S., 2013. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc. Natl. Acad. Sci. U. S. A., 110: 16492–7. https://doi.org/10.1073/pnas.1316316110

Pillai R. S., Chuma S., 2012. piRNAs and their involvement in male germline development in mice. Dev. Growth Differ., 54: 78–92. https://doi.org/ 10.1111/J.1440-169X.2011.01320.X

R Core Team, 2020. R: A language and environment for statistical computing. Available at https://www.r-project.org

Reuter M., Chuma S., Tanaka T., Franz T., Stark A., Pillai R. S., 2009. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol., 16: 639–46. https://doi.org/10.1038/nsmb.1615

Sharlip I. D., Jarow J. P., Belker A. M., Lipshultz L. I., Sigman M., Thomas A. J., Schlegel P. N., Howards S. S., Nehra A., Damewood M. D., Overstreet J. W., Sadovsky R., 2002. Best practice policies for male infertility. Fertil. Steril., 77:

–82. https://doi.org/10.1016/S0015-0282(02)03105-9

Shoji M., Tanaka T., Hosokawa M., Reuter M., Stark A., Kato Y., Kondoh G., Okawa K., Chujo T., Suzuki T., Hata K., Martin S. L., Noce T., Kuramochi-Miyagawa S., Nakano T., Sasaki H., Pillai R. S., Nakatsuji N., Chuma S., 2009. The TDRD9-MIWI2 Complex Is Essential for piRNA-Mediated Retrotransposon Silencing in the Mouse Male Germline. Dev. Cell, 17: 775–87. https://doi.org/ 10.1016/j.devcel.2009.10.012

Slotkin R. K., Martienssen R., 2007. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet., 8: 272–85. https://doi.org/10.1038/nrg2072

Yabuta Y., Ohta H., Abe T., Kurimoto K., Chuma S., Saitou M., 2011. TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J. Cell Biol., 192: 781–95. https://doi.org/10.1083/jcb.201009043

Yadav R. P., Kotaja N., 2014. Small RNAs in spermatogenesis. Mol. Cell. Endocrinol., 382: 498–508. https://doi.org/10.1016/ j.mce.2013.04.015

Yan W., 2009. Male infertility caused by spermiogenic defects: Lessons from gene knockouts. Mol. Cell. Endocrinol., 306: 24. https://doi.org/10.1016/J.MCE.2009.03.003

Zhu X. Bin, Lu J. Q., Zhi E. L., Zhu Y., Zou S. S., Zhu Z. J., Zhang F., Li Z., 2016. Association of a TDRD1 variant with spermatogenic failure susceptibility in the Han Chinese. J. Assist. Reprod. Genet., 33: 1099. https://doi.org/10.1007/s10815-016-0738-9