Hostname: page-component-669899f699-ggqkh Total loading time: 0 Render date: 2025-04-26T04:09:10.371Z Has data issue: false hasContentIssue false
  • English
  • Français

Age-related and photoperiodic variation of the DAZ gene family in the testis of the Syrian hamster (Mesocricetus auratus)

Published online by Cambridge University Press:  25 March 2018

Candela Rocío González ,
Luciana Moverer ,
Ricardo Saúl Calandra ,
Silvia Inés González-Calvar  and
Alfredo Daniel Vitullo
Candela Rocío González*
Affiliation:
Hidalgo 775, 1405 Buenos Aires, Argentina.
Luciana Moverer
Affiliation:
Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y Diagnóstico, Universidad Maimónides; Hidalgo 775, 1405 Buenos Aires; Argentina.
Ricardo Saúl Calandra
Affiliation:
Laboratorio de Endocrinología Molecular de la Reproducción, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Vuelta de Obligado 2490, 1428 Buenos Aires, Argentina.
Silvia Inés González-Calvar
Affiliation:
Laboratorio de Endocrinología Molecular de la Reproducción, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Vuelta de Obligado 2490, 1428 Buenos Aires, Argentina.
Alfredo Daniel Vitullo
Affiliation:
Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y Diagnóstico, Universidad Maimónides; Hidalgo 775, 1405 Buenos Aires; Argentina.
*
All correspondence to: Candela Rocío González. Hidalgo 775, 1405 Buenos Aires, Argentina. E-mail: gonzalez.candela@maimonides.edu
Get access Rights & Permissions [Opens in a new window]

Summary

The Deleted in AZoospermia (DAZ) gene family regulates the development, maturation and maintenance of germ cells and spermatogenesis in mammals. The DAZ family consists of two autosomal genes, Boule and Dazl (Daz-like), and the Daz gene on chromosome Y. The aim of this study was to analyze the localization of DAZL and BOULE during testicular ontogeny of the seasonal-breeding Syrian hamster, Mesocricetus auratus. We also evaluated the testicular expression of DAZ family genes under short- or long-photoperiod conditions. In the pre-pubertal and adult testis, DAZL protein was found mainly in spermatogonia. BOULE was found in the spermatogonia from 20 days of age and during the pre-pubertal and adult period it was also detected in spermatocytes and round spermatids. DAZL and BOULE expression in spermatogonia was strictly nuclear only in 20-day-old hamsters. We also detected the novel mRNA and protein expression of BOULE in Leydig cells. In adult hamsters, Dazl expression was increased in regressed testis compared with non-regressed testis and DAZL protein expression was restricted to primary spermatocytes in regressed testis. These results show that DAZL and BOULE are expressed in spermatogonia at early stages in the Syrian hamster, then both proteins translocate to the cytoplasm when meiosis starts. In the adult regressed testis, the absence of DAZL in spermatogonia might be related to the decrease in germ cell number, suggesting that DAZ gene family expression is involved in changes in seminiferous epithelium during photoregression.

Keywords

BOULEDAZLPhotoperiodSyrian hamsterTestis
Type
Research Article
Information
Zygote , Volume 26 , Issue 2 , April 2018 , pp. 127 - 134
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Bartke, A. (1985). Male hamster reproductive endocrinology. In The Hamster: Reproduction and Behavior (ed. Siegel, H.I.), pp. 73–98. New York, USA: Plenum Press.CrossRefGoogle Scholar
Bartke, A. & Russell, L.D. (1988). Morphometric studies on hamster testes in gonadally active and inactive states: light microscope findings. Biol. Reprod. 39, 1225–37.Google Scholar
Bartke, A., Sinha Hikim, A.P. & Russell, L.D. (1999). Leydig cell structure and function in seasonal breeders. In The Leydig Cell (eds Payne, A.H., Hardy, M.P. & Russell, L.D.), pp. 431–50. St. Louis, MO, USA: Cache River Press.Google Scholar
Cheng, Y.S., Kuo, P.L., Teng, Y.N., Kuo, T.Y., Chung, C.L., Lin, Y.H., Liao, R.W., Nan Lin, J.S. & Lin, Y.M. (2006). Association of spermatogenic failure with decreased CDC25A expression in infertile men. Hum. Reprod. 21, 2346–52.CrossRefGoogle ScholarPubMed
Foresta, C., Moro, E. & Ferlin, A. (2001). Y chromosome microdeletions and alterations of spermatogenesis. Endocr. Rev. 22, 226–39.Google ScholarPubMed
Frungieri, M.B., González-Calvar, S.I., Rubio, M., Ozu, M., Lustig, L. & Calandra, R.S. (1999). Serotonin in golden hamster testes: testicular levels, immunolocalization and role during sexual development and photoperiodic regression–recrudescence transition. Neuroendocrinology 69, 299–308.CrossRefGoogle ScholarPubMed
Frungieri, M.B., Mayerhofer, A., Zitta, K., Pignataro, O.P., Calandra, R.S. & González-Calvar, S.I. (2005). Direct effect of melatonin on Syrian hamster testes: mel1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone (CRH) system. Endocrinology 146, 1541–52.CrossRefGoogle Scholar
González, C.R., Dorfman, V.B. & Vitullo, A.D. (2015). IGF1 regulation of Boule and Cdc25a transcripts through a testosterone-independent pathway in adult mice spermatogenesis. Reprod. Biol. 15, 48–55.CrossRefGoogle Scholar
González, C.R., Alvarez Sedó, C., Nodar, F., Papier, S. & Vitullo, A.D. (2016). Simultaneous analysis of DAZ family members and CDC25A: a predicting study for successful TESE. Asian J. Androl. 18, 1–2.Google Scholar
Gromoll, J., Weinbauer, G.F., Skaletsky, H., Schlatt, S., Rocchietti-March, M., Page, D.C. & Nieschlag, E. (1999). The Old World monkey DAZ (Deleted in Azoospermia) gene yields insights into the evolution of the DAZ gene cluster on the human Y chromosome. Hum. Mol. Genet. 8, 2017–24.CrossRefGoogle ScholarPubMed
Jiao, X., Trifillis, P. & Kiledjian, M. (2002). Identification of target messenger RNA substrates for the murine deleted in azoospermia-like RNA-binding protein. Biol. Reprod. 66, 475–85.CrossRefGoogle ScholarPubMed
Karashima, T., Sugimoto, A. & Yamamoto, M. (2000). Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127, 1069–79.CrossRefGoogle Scholar
Kostova, E., Yeung, C.H., Luetjens, C.M., Brune, M., Nieschlag, E. & Gromoll, J. (2007). Association of three isoforms of the meiotic BOULE gene with spermatogenic failure in infertile men. Mol. Hum. Reprod. 13, 85–93.CrossRefGoogle ScholarPubMed
Kotaja, N. & Sassone-Corsi, P. (2007). The chromatoid body: a germ-cell-specific RNA-processing centre. Nat. Rev. Mol. Cell. Biol. 8, 85–90.CrossRefGoogle ScholarPubMed
Levy, H., Deane, H.W. & Rubin, B.L. (1959). Visualization of steroid 3β-ol-dehydrogenase activity in tissues of intact and hypophysectomized rats. Endocrinology 65, 932–43.CrossRefGoogle Scholar
Luetjens, C.M., Xu, E.Y., Reijo, R.A., Kamischke, A., Nieschlag, E. & Gromoll, J. (2004). Association of meiotic arrest with lack of BOULE protein expression in infertile men. J. Clin. Endocrinol. Metab. 89, 1926–33.CrossRefGoogle ScholarPubMed
Maines, J.Z. & Wasserman, S.A. (1999). Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule. Nat. Cell. Biol. 1, 171–4.CrossRefGoogle ScholarPubMed
Mason, A.O., Duffy, S., Zhao, S., Ubuka, T., Bentley, G.E., Tsutsui, K., Silver, R. & Kriegsfeld, L.J. (2010). Photoperiod and reproductive condition are associated with changes in RF amide-related peptide (RFRP) expression in Syrian hamsters (Mesocricetus auratus). J. Biol. Rhythms 25, 176–85.CrossRefGoogle Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real time RT-PCR. Nucl. Acids Res. 29, e45.CrossRefGoogle ScholarPubMed
Reijo, R.A., Dorfman, D.M., Slee, R., Renshaw, A.A., Loughlin, K.R., Cooke, H. & Page, D.C. (2000). DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol. Reprod. 63, 1490–6.CrossRefGoogle ScholarPubMed
Ruggiu, M., Saunders, P.T. & Cooke, H.J. (2000). Dynamic subcellular distribution of the DAZL protein is confined to primate male germ cells. J. Androl. 21, 470–7.CrossRefGoogle ScholarPubMed
Saunders, P.T.K., Turner, J.M.A., Ruggiu, M., Taggart, M., Burgoyne, P.S., Elliott, D. & Cooke, H.J. (2003). Absence of mDazl produces a final block on germ cell development at meiosis. Reproduction 126, 589–97.CrossRefGoogle ScholarPubMed
Saxena, R., Brown, L.G., Hawkins, T., Alagappan, R.K., Skaletsky, H. & Reeve, M.P. (1996). The DAZ gene cluster on the human Y chromosome arise from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat. Genet. 14, 292–9.CrossRefGoogle Scholar
Simonneaux, V., Ansel, L., Revel, F.G., Klosen, P., Pévet, P., Mikkelsen, J.D. (2009). Kisspeptin and the seasonal control of reproduction in hamsters. Peptides 30, 146–53.CrossRefGoogle ScholarPubMed
Smorag, L., Xu, X., Engel, W. & Pantakani, D.V. (2014). The roles of DAZL in RNA biology and development. Wiley Interdiscip. Rev. RNA. 5, 527–35.CrossRefGoogle ScholarPubMed
Van Gompel, J.W. & Xu, E.Y. (2010). A novel requirement in mammalian spermatid differentiation for the DAZ-family protein Boule. Hum. Mol. Genet. 19, 2360–9.CrossRefGoogle ScholarPubMed
Van Gompel, M.J. & Xu, E.Y. (2011). The roles of the DAZ family in spermatogenesis: more than just translation? Spermatogenesis 1, 36–46.CrossRefGoogle Scholar
Venables, J.P., Ruggiu, M. & Cooke, H.J. (2001). The RNA-binding specificity of the mouse DAZL protein. Nucl. Acids Res. 29, 2479–83.CrossRefGoogle ScholarPubMed
Xu, E.Y., Moore, F.L. & Pera, R.A. (2001). A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc. Natl. Acad. Sci. USA 98, 7414–9.CrossRefGoogle ScholarPubMed
Yen, P.H. (2004). Putative biological functions of the DAZ family. Int. J. Androl. 27, 125–9.CrossRefGoogle ScholarPubMed