DOI QR코드

DOI QR Code

Tudor Domain Containing Protein TDRD12 Expresses at the Acrosome of Spermatids in Mouse Testis

  • Kim, Min (Department of Biomedical Science, CHA University) ;
  • Ki, Byeong Seong (Department of Biomedical Science, CHA University) ;
  • Hong, Kwonho (Department of Nanobiomedical Science & BK21 PLUS NBM Global Research Center for Regenerative Medicine, Dankook University) ;
  • Park, Se-pill (Department of Biotechnology, College of Applied Life Science, Jeju National University) ;
  • Ko, Jung-Jae (Department of Biomedical Science, CHA University) ;
  • Choi, Youngsok (Department of Biomedical Science, CHA University)
  • Received : 2015.05.16
  • Accepted : 2015.09.26
  • Published : 2016.07.01

Abstract

Tdrd12 is one of tudor domain containing (Tdrd) family members. However, the expression pattern of Tdrd12 has not been well studied. To compare the expression levels of Tdrd12 in various tissues, real time-polymerase chain reaction was performed using total RNAs from liver, small intestine, heart, brain, kidney, lung, spleen, stomach, uterus, ovary, and testis. Tdrd12 mRNA was highly expressed in testis. Antibody against mouse TDRD12 were generated using amino acid residues SQRPNEKPLRLTEKKDC of TDRD12 to investigate TDRD12 localization in testis. Immunostaining assay shows that TDRD12 is mainly localized at the spermatid in the seminiferous tubules of adult testes. During postnatal development, TDRD12 is differentially expressed. TDRD12 was detected in early spermatocytes at 2 weeks and TDRD12 was localized at acrosome of the round spermatids. TDRD12 expression was not co-localized with TDRD1 which is an important component of piRNA pathway in germ cells. Our results indicate that TDRD12 may play an important role in spermatids and function as a regulator of spermatogenesis in dependent of TDRD1.

Keywords

References

  1. Aravin, A. A., G. W. van der Heijden, J. Castaneda, V. V. Vagin, G. J. Hannon, and A. Bortvin. 2009. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 5:e1000764. https://doi.org/10.1371/journal.pgen.1000764
  2. Bak, C. W., T. K. Yoon, and Y. Choi. 2011. Functions of PIWI proteins in spermatogenesis. Clin. Exp. Reprod. Med. 38:61-67. https://doi.org/10.5653/cerm.2011.38.2.61
  3. Bao, J., L. Wang, J. Lei, Y. Hu, Y. Liu, H. Shen, W. Yan, and C. Xu. 2012. STK31(TDRD8) is dynamically regulated throughout mouse spermatogenesis and interacts with MIWI protein. Histochem. Cell Biol. 137:377-389. https://doi.org/10.1007/s00418-011-0897-9
  4. Bortvin, A. 2013. PIWI-interacting RNAs (piRNAs) - a mouse testis perspective. Biochemistry (Mosc) 78:592-602. https://doi.org/10.1134/S0006297913060059
  5. Callebaut, I. and J. P. Mornon. 1997. The human EBNA-2 coactivator p100: multidomain organization and relationship to the staphylococcal nuclease fold and to the tudor protein involved in Drosophila melanogaster development. Biochem. J. 321:125-132. https://doi.org/10.1042/bj3210125
  6. Caudy, A. A., R. F. Ketting, S. M. Hammond, A. M. Denli, A. M. Bathoorn, B. B. Tops, J. M. Silva, M. M. Myers, G. J. Hannon, and R. H. Plasterk. 2003. A micrococcal nuclease homologue in RNAi effector complexes. Nature 425:411-414. https://doi.org/10.1038/nature01956
  7. Chen, C., J. Jin, D. A. James, M. A. Adams-Cioaba, J. G. Park, Y. Guo, E. Tenaglia, C. Xu, G. Gish, J. Min, and T. Pawson. 2009. Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc. Natl. Acad. Sci. USA 106:20336-20341. https://doi.org/10.1073/pnas.0911640106
  8. Chuma, S., M. Hiyoshi, A. Yamamoto, M. Hosokawa, K. Takamune, and N. Nakatsuji. 2003. Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech. Dev. 120:979-990. https://doi.org/10.1016/S0925-4773(03)00181-3
  9. Chuma, S., M. Hosokawa, K. Kitamura, S. Kasai, M. Fujioka, M. Hiyoshi, K. Takamune, T. Noce, and N. Nakatsuji. 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. USA 103:15894-15899. https://doi.org/10.1073/pnas.0601878103
  10. Gao, X., X. Zhao, Y. Zhu, J. He, J. Shao, C. Su, Y. Zhang, W. Zhang, J. Saarikettu, O. Silvennoinen, Z. Yao, and J. Yang. 2012. Tudor staphylococcal nuclease (Tudor-SN) participates in small ribonucleoprotein (snRNP) assembly via interacting with symmetrically dimethylated Sm proteins. J. Biol. Chem. 287:18130-18141. https://doi.org/10.1074/jbc.M111.311852
  11. Garcia-Lopez, J., D. Hourcade Jde, and J. Del Mazo. 2013. Reprogramming of microRNAs by adenosine-to-inosine editing and the selective elimination of edited microRNA precursors in mouse oocytes and preimplantation embryos. Nucl. Acids Res. 41:5483-5493. https://doi.org/10.1093/nar/gkt247
  12. Handler, D., D. Olivieri, M. Novatchkova, F. S. Gruber, K. Meixner, K. Mechtler, A. Stark, R. Sachidanandam, and J. Brennecke. 2011. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 30:3977-3993. https://doi.org/10.1038/emboj.2011.308
  13. Kallajoki, M., I. Virtanen, and J. Suominen. 1986. The fate of acrosomal staining during the acrosome reaction of human spermatozoa as revealed by a monoclonal antibody and PNA-lectin. Int. J. Androl. 9:181-194. https://doi.org/10.1111/j.1365-2605.1986.tb00881.x
  14. Kotaja, N. and P. Sassone-Corsi. 2007. The chromatoid body: a germ-cell-specific RNA-processing centre. Nat. Rev. Mol. Cell Biol. 8:85-90.
  15. Lachke, S. A., F. S. Alkuraya, S. C. Kneeland, T. Ohn, A. Aboukhalil, G. R. Howell, I. Saadi, R. Cavallesco, Y. Yue, A. C. Tsai, K. S. Nair, M. I. Cosma, R. S. Smith, E. Hodges, S. M. Alfadhli, A. Al-Hajeri, H. E. Shamseldin, A. Behbehani, G. J. Hannon, M. L. Bulyk, A. V. Drack, P. J. Anderson, S. W. John, and R. L. Maas. 2011. Mutations in the RNA granule component TDRD7 cause cataract and glaucoma. Science 331:1571-1576. https://doi.org/10.1126/science.1195970
  16. Leverson, J. D., P. J. Koskinen, F. C. Orrico, E. M. Rainio, K. J. Jalkanen, A. B. Dash, R. N. Eisenman, and S. A. Ness. 1998. Pim-1 kinase and p100 cooperate to enhance c-Myb activity. Mol. Cell 2:417-425. https://doi.org/10.1016/S1097-2765(00)80141-0
  17. Li, C. L., W. Z. Yang, Y. P. Chen, and H. S. Yuan. 2008. Structural and functional insights into human Tudor-SN, a key component linking RNA interference and editing. Nucl. Acids Res. 36:3579-3589. https://doi.org/10.1093/nar/gkn236
  18. Luteijn, M. J. and R. F. Ketting. 2013. PIWI-interacting RNAs: From generation to transgenerational epigenetics. Nat. Rev. Genet. 14:523-534.
  19. Matzuk, M. M. and D. J. Lamb. 2008. The biology of infertility: Research advances and clinical challenges. Nat. Med. 14:1197-1213. https://doi.org/10.1038/nm.f.1895
  20. Meikar, O., M. Da Ros, H. Korhonen, and N. Kotaja. 2011. Chromatoid body and small RNAs in male germ cells. Reproduction 142:195-209. https://doi.org/10.1530/REP-11-0057
  21. Pan, J., M. Goodheart, S. Chuma, N. Nakatsuji, D. C. Page, and P. J. Wang. 2005. RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132:4029-4039. https://doi.org/10.1242/dev.02003
  22. Pandey, R. R., Y. Tokuzawa, Z. Yang, E. Hayashi, T. Ichisaka, S. Kajita, Y. Asano, T. Kunieda, R. Sachidanandam, S. Chuma, S. Yamanaka, and R. S. Pillai. 2013. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc. Natl. Acad. Sci. USA 110:16492-16497. https://doi.org/10.1073/pnas.1316316110
  23. Paukku, K., N. Kalkkinen, O. Silvennoinen, K. K. Kontula, and J. Y. Lehtonen. 2008. p100 increases AT1R expression through interaction with AT1R 3'-UTR. Nucl. Acids Res. 36:4474-4487. https://doi.org/10.1093/nar/gkn411
  24. Reuter, M., S. Chuma, T. Tanaka, T. Franz, A. Stark, and R. S. Pillai. 2009. Loss of the Mili-interacting Tudor domaincontaining protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol. 16:639-646. https://doi.org/10.1038/nsmb.1615
  25. Reynolds, N., B. Collier, K. Maratou, V. Bingham, R. M. Speed, M. Taggart, C. A. Semple, N. K. Gray, and H. J. Cooke. 2005. Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum. Mol. Genet. 14:3899-3909. https://doi.org/10.1093/hmg/ddi414
  26. Saxe, J. P., M. Chen, H. Zhao, and H. Lin. 2013. Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. EMBO J. 32:1869-1885. https://doi.org/10.1038/emboj.2013.121
  27. Shoji, M., T. Tanaka, M. Hosokawa, M. Reuter, A. Stark, Y. Kato, G. Kondoh, K. Okawa, T. Chujo, T. Suzuki, K. Hata, S. L. Martin, T. Noce, S. Kuramochi-Miyagawa, T. Nakano, H. Sasaki, R. S. Pillai, N. Nakatsuji, and S. Chuma. 2009. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 17:775-787. https://doi.org/10.1016/j.devcel.2009.10.012
  28. Smith, J. M., J. Bowles, M. Wilson, R. D. Teasdale, and P. Koopman. 2004. Expression of the tudor-related gene Tdrd5 during development of the male germline in mice. Gene Expr. Patterns 4:701-705. https://doi.org/10.1016/j.modgep.2004.04.002
  29. Tanaka, T., M. Hosokawa, V. V. Vagin, M. Reuter, E. Hayashi, A. L. Mochizuki, K. Kitamura, H. Yamanaka, G. Kondoh, K. Okawa, S. Kuramochi-Miyagawa, T. Nakano, R. Sachidanandam, G. J. Hannon, R. S. Pillai, N. Nakatsuji, and S. Chuma. 2011. Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis. Proc. Natl. Acad. Sci. USA 108:10579-10584. https://doi.org/10.1073/pnas.1015447108
  30. van der Heijden, G. W., J. Castaneda, and A. Bortvin. 2010. Bodies of evidence - compartmentalization of the piRNA pathway in mouse fetal prospermatogonia. Curr. Opin. Cell Biol. 22:752-757. https://doi.org/10.1016/j.ceb.2010.08.014
  31. Vasileva, A., D. Tiedau, A. Firooznia, T. Muller-Reichert, and R. Jessberger. 2009. Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr. Biol. 19:630-639. https://doi.org/10.1016/j.cub.2009.02.047
  32. Wang, P. J., J. R. McCarrey, F. Yang, and D. C. Page. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27:422-426. https://doi.org/10.1038/86927
  33. Yabuta, Y., H. Ohta, T. Abe, K. Kurimoto, S. Chuma, and M. Saitou. 2011. TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J. Cell Biol. 192:781-795. https://doi.org/10.1083/jcb.201009043
  34. Yang, J., S. Aittomaki, M. Pesu, K. Carter, J. Saarinen, N. Kalkkinen, E. Kieff, and O. Silvennoinen. 2002. Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. EMBO J. 21:4950-4958. https://doi.org/10.1093/emboj/cdf463
  35. Ying, M. and D. Chen. 2012. Tudor domain-containing proteins of Drosophila melanogaster. Dev. Growth Differ. 54:32-43. https://doi.org/10.1111/j.1440-169X.2011.01308.x

Cited by

  1. Tdrd12 Is Essential for Germ Cell Development and Maintenance in Zebrafish vol.18, pp.6, 2017, https://doi.org/10.3390/ijms18061127
  2. Biased Duplications and Loss of Members in Tdrd Family in Teleost Fish vol.328, pp.8, 2017, https://doi.org/10.1002/jez.b.22757
  3. Structure and function of eTudor domain containing TDRD proteins vol.54, pp.2, 2016, https://doi.org/10.1080/10409238.2019.1603199
  4. The Role of the PRMT5-SND1 Axis in Hepatocellular Carcinoma vol.5, pp.1, 2016, https://doi.org/10.3390/epigenomes5010002