Skip to main content
Log in

Nascent polypeptide-associated complex as tissue-specific cofactor during germinal cell differentiation in Drosophila testes

  • Molecular Cell Biology
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

During the process of spermatogenesis, the proliferation of spermatogonia (stem cell descendants) is replaced by their differentiation in growing spermatocytes responsible for the preparation to meiosis, which is accompanied by a cardinal change in transcriptional programs. We have demonstrated that, in drosophila, this process is accompanied by a splash of the expression of β-subunit of nascent polypeptide-associated complex (NAC) associated by ribosomes. Nascent polypeptide-associated complex is known as a chaperone involved in co-translational protein folding. This is the first case of the detection of tissue-specific co-translational NAC cofactor in multicellular eukaryotes. It is proposed that spermatocyte specific NAC is involved in the modulation of the expression of the proteins that provide the functioning of subsequent stages of spermatogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wiedmann B., Sakai H., Davis T.A., Wiedmann M. 1994. A protein complex required for signal-sequencespecific sorting and translocation. Nature. 370 (6489), 434–440.

    Article  CAS  PubMed  Google Scholar 

  2. Rospert S., Dubaquie Y., Gautschi M. 2002. Nascentpolypeptide- associated complex. Cell. Mol. Life Sci. 59 (10), 1632–1639.

    Article  CAS  PubMed  Google Scholar 

  3. Pechmann S., Willmund F., Frydman J. 2013. The ribosome as a hub for protein quality control. Mol. Cell. 49 (3), 411–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Deng J.M., Behringer R.R. 1995. An insertional mutation in the BTF3 transcription factor gene leads to an early postimplantation lethality in mice. Transgenic Res. 4 (4), 264–269.

    Article  CAS  PubMed  Google Scholar 

  5. Markesich D.C., Gajewski K.M., Nazimiec M.E., Beckingham K. 2000. Bicaudal encodes the Drosophila beta NAC homolog, a component of the ribosomal translational machinery. Development. 127 (3), 559–572.

    CAS  PubMed  Google Scholar 

  6. Bloss T.A., Witze E.S., Rothman J.H. 2003. Suppression of CED-3-independent apoptosis by mitochondrial betaNAC in Caenorhabditis elegans. Nature. 424 (6952), 1066–1071.

    Article  CAS  PubMed  Google Scholar 

  7. Del Alamo M., Hogan D.J., Pechmann S., Albanese V., Brown P.O., Frydman J. 2011. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 9 (7), e1001100.

    Article  Google Scholar 

  8. Lesnik C., Cohen Y., Atir-Lande A., Schuldiner M., Arava Y. 2014. OM14 is a mitochondrial receptor for cytosolic ribosomes that supports co-translational import into mitochondria. Nat. Commun. 5, 5711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Guo B., Huang J., Wu W., Feng D., Wang X., Chen Y., Zhang H. 2014. The nascent polypeptide-associated complex is essential for autophagic flux. Autophagy. 10 (10), 1738–1748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Creagh E.M., Brumatti G., Sheridan C., Duriez P.J., Taylor R.C., Cullen S.P., Adrain C., Martin S.J. 2009. Bicaudal is a conserved substrate for Drosophila and mammalian caspases and is essential for cell survival. PLoS ONE. 4 (3), e5055.

    Article  Google Scholar 

  11. Arsenovic P.T., Maldonado A.T., Colleluori V.D., Bloss T.A. 2012. Depletion of the C. elegans NAC engages the unfolded protein response, resulting in increased chaperone expression and apoptosis. PLoS ONE. 7 (9), e44038.

    Article  Google Scholar 

  12. Karan R., Subudhi P.K. 2012. Overexpression of a nascent polypeptide associated complex gene (Sabeta- NAC) of Spartina alterniflora improves tolerance to salinity and drought in transgenic Arabidopsis. Biochem. Biophys. Res. Commun. 424 (4), 747–752.

    Article  CAS  PubMed  Google Scholar 

  13. Kirstein-Miles J., Scior A., Deuerling E., Morimoto R.I. 2013. The nascent polypeptide-associated complex is a key regulator of proteostasis. EMBO J. 32 (10), 1451–1468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hotokezaka Y., Katayama I., Van Leyen K., Nakamura T. 2015. GSK-3beta-dependent downregulation of gammataxilin and alphaNAC merge to regulate ER stress responses. Cell Death Dis. 6, e1719.

    Article  Google Scholar 

  15. Gamerdinger M., Hanebuth M.A., Frickey T., Deuerling E. 2015. The principle of antagonism ensures pro-tein targeting specificity at the endoplasmic reticulum. Science. 348 (6231), 201–207.

    Article  CAS  PubMed  Google Scholar 

  16. Nyathi Y., Pool M.R. 2015. Analysis of the interplay of protein biogenesis factors at the ribosome exit site reveals new role for NAC. J. Cell. Biol. 210 (2), 287–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Usakin L.A., Kogan G.L., Kalmykova A.I., Gvozdev V.A. 2005. An alien promoter capture as a primary step of the evolution of testes-expressed repeats in the Drosophila melanogaster genome. Mol. Biol. Evol. 22 (7), 1555–1560.

    Article  CAS  PubMed  Google Scholar 

  18. Kogan G.L., Usakin L.A., Ryazansky S.S., Gvozdev V.A. 2012. Expansion and evolution of the X-linked testis specific multigene families in the melanogaster species subgroup. PLoS ONE. 7 (5), e37738.

    Article  Google Scholar 

  19. Usakin L.A., Gvozdev V.A., Kogan L.L. 2009. Molecular variation of the testes-specific ßNACtes genes in the Drosophila melanogaster genome. Mol. Biol. (Moscow). 43 (3), 367–373.

    Article  CAS  Google Scholar 

  20. Vibranovski M.D., Lopes H.F., Karr T.L., Long M. 2009. Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testisexpressed genes. PLoS Genet. 5 (11), e1000731.

    Article  Google Scholar 

  21. Chen X., Lu C., Morillo Prado J.R., Eun S.H., Fuller M.T. 2011. Sequential changes at differentiation gene promoters as they become active in a stem cell lineage. Development. 138 (12), 2441–2450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. White-Cooper H. 2010. Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction. 139 (1), 11–21.

    Article  CAS  PubMed  Google Scholar 

  23. Barreau C., Benson E., Gudmannsdottir E., Newton F., White-Cooper H. 2008. Post-meiotic transcription in Drosophila testes. Development. 135 (11), 1897–1902.

    Article  CAS  PubMed  Google Scholar 

  24. Blumer N., Schreiter K., Hempel L., Santel A., Hollmann M., Schafer M.A., Renkawitz-Pohl R. 2002. A new translational repression element and unusual transcriptional control regulate expression of don juan during Drosophila spermatogenesis. Mech. Dev. 110 (1–2), 97–112.

    Article  CAS  PubMed  Google Scholar 

  25. Gilbert W.V. 2011. Functional specialization of ribosomes? Trends Biochem. Sci. 36 (3), 127–132.

    CAS  Google Scholar 

  26. Shi Z., Barna M. 2015. Translating the genome in time and space: Specialized ribosomes, RNA regulons, and RNA-binding proteins. Annu. Rev. Cell Dev. Biol. 31, 31–54.

    Article  CAS  PubMed  Google Scholar 

  27. Kibanov M.V., Kotov A.A., Olenina L.V. 2013. Multicolor fluorescence imaging of whole-mount Drosophila testes for studying spermatogenesis. Anal. Biochem. 436(1), 55–64.

    Article  CAS  PubMed  Google Scholar 

  28. Xing Y., Li W.X. 2015. Heterochromatin components in germline stem cell maintenance. Sci. Rep. 5, 17463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ott A.K., Locher L., Koch M., Deuerling E. 2015. Functional dissection of the nascent polypeptide-associated complex in Saccharomyces cerevisiae. PLoS ONE. 10 (11), e0143457.

    Article  Google Scholar 

  30. Sanchez C.G., Teixeira F.K., Czech B., Preall J.B., Zamparini A.L., Seifert J.R., Malone C.D., Hannon G.J., Lehmann R. 2016. Regulation of ribosome biogenesis and protein synthesis controls germline stem cell differentiation. Cell Stem Cell. 18 (2), 276–290.

    Article  CAS  PubMed  Google Scholar 

  31. Kondrashov N., Pusic A., Stumpf C.R., Shimizu K., Hsieh A.C., Xue S., Ishijima J., Shiroishi T., Barna M. 2011. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell. 145 (3), 383–397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. A. Gvozdev.

Additional information

Original Russian Text © G.L. Kogan, N.V. Akulenko, Yu.A. Abramov, O.A. Sokolova, E.A. Fefelova, V.A. Gvozdev, 2017, published in Molekulyarnaya Biologiya, 2017, Vol. 51, No. 4, pp. 677–682.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kogan, G.L., Akulenko, N.V., Abramov, Y.A. et al. Nascent polypeptide-associated complex as tissue-specific cofactor during germinal cell differentiation in Drosophila testes. Mol Biol 51, 596–601 (2017). https://doi.org/10.1134/S0026893317040112

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893317040112

Keywords

Navigation