Skip to main content
Log in

The Telomere-Binding Protein Taz1p as a Target for Modification by a SUMO-1 Homologue in Fission Yeast

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

In fission yeast (Schizosaccharomyces pombe) the homologue of the mammalian SUMO-1 ubiquitin-like modifier is encoded by the pmt3 gene. A two-hybrid screen using the telomere-binding protein Taz1p as bait identified Pmt3p as an interacting factor. In vitro experiments using purified components of the fission yeast Pmt3p modification system demonstrated that Taz1p could be modified directly by Pmt3p. The amino acid sequence of Taz1p contains a close match to the consensus modification site for SUMO-1, and a PEST sequence similar to those found in established SUMO-1 targets. Although previous experiments have identified an increase in telomere length as one consequence of the pmt3− genotype, we could not detect Pmt3p modification of Taz1p in protein extracts made from exponentially growing haploid cells or any effect of Pmt3p on the localization of GFP-Taz1p at discrete foci in the haploid cell nucleus.

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

  • Bahler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., Steever, A. B., Wach, A., Philippsen, P., and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943–951.

    PubMed  CAS  Google Scholar 

  • Baumann, P., and Cech, T. R. (1998). Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171–1175.

    Google Scholar 

  • Boddy, M. N., Howe, K., Etkin, L. D., Solomon, E., and Freemont, P. S. (1998). PIC1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene 13:971–982.

    Google Scholar 

  • Chikashige, Y., Ding, D. Q., Funabiki, H., Haraguchi, T., Mashiko, S., Yanagida, M., and Hiraoka, Y. (1998). Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273.

    Google Scholar 

  • Chikashige, Y., and Hiraoka, Y. (1998). Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr. Biol. 11:1618–1623.

    Google Scholar 

  • Cooper, J. P., Nimmo, E. R., Allshire, R. C., and Cech, T. R. (1998). Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 385:744–747.

    Google Scholar 

  • Cooper, J. P., Watanabe, Y., and Nurse, P. (1998). Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392:828–831.

    PubMed  CAS  Google Scholar 

  • Desterro, J. M. P., Rodriguez, M. S., and Hay, R. T. (1998). SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell. 2:233–239.

    PubMed  CAS  Google Scholar 

  • Ferreira, M. G., and Cooper, J. P. (1998). The fission yeast Taz1 protein protects chromosomes from Ku-dependent end-to-end fusions. Mol. Cell 7:55–63.

    Google Scholar 

  • Funabiki, H., Hagan, I., Uzawa, S., and Yanagida, M. (1998). Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121:961–976.

    Google Scholar 

  • Gottschling, D. E., Aparicio, O. M., Billington, B. L., and Zakian, V. A. (1998). Position effect at S. cerevisiae telomeres: Reversible repression of pol II transcription. Cell 63:751–762.

    Google Scholar 

  • Hardy, C. F. J., Sussel, L., and Shore, D. (1998). A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 6:801–814.

    Google Scholar 

  • Ho, J. C. Y., Warr, N. J., Shimizu, H., and Watts, F. Z. (1998). SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52. Nucl. Acids Res. 29:4179–4186.

    Google Scholar 

  • Kanoh, J., and Ishikawa, F. (1998). spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr. Biol. 11:1624–1630.

    Google Scholar 

  • Kawabe, Y., Seki, M., Seki, T., Wang, W. S., Imamura, O., Furuichi, Y., Saitoh, H., and Enomoto, T. (1998). Covalent modification of the Werner’s syndrome gene product with the ubiquitin-related protein, SUMO-1. J. Biol. Chem. 275:20963–20966.

    Google Scholar 

  • Kim, Y. H., Choi, C. Y., and Kim, Y. (1998). Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc. Natl. Acad. Sci. U.S.A 96:12350–12355.

    Google Scholar 

  • Laroche, T., Martin, S. G., Gotta, M., Gorham, H. C., Pryde, F. E., Louis, E. J., and Gasser, S. M. (1998). Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8:653–656.

    PubMed  CAS  Google Scholar 

  • Lundblad, V., and Szostak, J. W. (1998) A mutant wih a defect in telomere elongation leads to senescence in yeast. Cell 57:633–643.

    Google Scholar 

  • Mahajan, R., Delphin, C., Guan, T., Gerace, L., and Melchior, F. (1998). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88:97–107.

    Google Scholar 

  • Melchior, F. (1998). SUMO-Nonclassical ubiquitin. Ann. Rev. Cell Dev. Biol. 16:591–626.

    Google Scholar 

  • Meluh, P. B., and Koshland, D. (1998). Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol. Biol. Cell. 6:793–807.

    Google Scholar 

  • Miller, K. M., and Cooper, J. P. (1998). The telomere protein Taz1 is required to prevent and repair genomic DNA breaks. Mol. Cell 11:303–313.

    Google Scholar 

  • Minty, A., Dumont, X., Kaghad, M., and Caput, D. (1998). Covalent modification of p73α by SUMO-1. J. Biol. Chem. 275:36316–36323.

    Google Scholar 

  • Moreno, S., Klar, A., and Nurse, P. (1998). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823.

    Google Scholar 

  • Nakamura, T. M., Morin, G. B., Chapman, K. B., Weinrich, S. L., Andrews, W. H., Lingner, J., Harley, C. B., and Cech, T. R. (1998). Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955–959.

    Google Scholar 

  • Nimmo, E. R., Pidoux, A. L., Perry, P. E., and Allshire, R. C. (1998). Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392:825–828.

    PubMed  CAS  Google Scholar 

  • Niwa, O., Shimanuki, M., and Miki, F. (1998). Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19:3831–3840.

    Google Scholar 

  • Okura, T., Gong, L., Kamitani, T., Wada, T., Okura, I., Wei, C. F., Chang, H. M., and Yeh, E. T. (1998). Protection against Fas/APO-1 and tumour necrosis factor mediated cell death by a novel protein, sentrin. J. Immunol. 157:4277–4281.

    Google Scholar 

  • Printen, J. A., and Sprague, G. F. (1998). Protein–protein interactions in the yeast pheromone response pathway-Ste5p interacts with all members of the MAP kinase cascade. Genetics 138:609–619.

    Google Scholar 

  • Rangasamy, D., and Wilson, V. G. (1998). Bovine papillomavirus E1 protein is smoylated by the host cell Ubc9 protein. J. Biol. Chem. 275:30487–30495.

    Google Scholar 

  • Rechsteiner, M., and Rogers, S. W. (1998). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267–271.

    Google Scholar 

  • Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K., and Chen, D. J. (1996a). Associations of UBE21 with RAD52, UBL1, p53 and RAD51 proteins in a yeast two-hybrid system. Genomics 37:183–186.

    CAS  Google Scholar 

  • Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K., and Chen, D. J. (1996b). UBL1, a human ubiquitin-like protein associated with human RAD51/RAD52 proteins. Genomics 36:271–279.

    CAS  Google Scholar 

  • Sherman, F. (1998). Getting started with yeast. Methods Enzymol. 194:3–21.

    Article  Google Scholar 

  • Spink, K. G., Evans, R. J., and Chambers, A. (1998). Sequence-specific binding of Taz1p dimers to fission yeast telomeric DNA. Nucl. Acids Res. 28:527–533.

    Google Scholar 

  • Tanaka, K., Nishide, J., Okazaki, K., Kato, H., Niwa, O., Nakagawa, T., Matsuda, H., Kawamukai, M., and Murakami, Y. (1998). Characterization of a fission yeast SUMO-1 homologue, Pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol. Cell. Biol. 19:8660–8672.

    Google Scholar 

  • Vassetzky, N. S., Gaden, F., Brun, C., Gasser, S. M., and Gilson, E. (1998). Taz1p and Teb1p, two telobox proteins in Schizosaccharomyces pombe, recognize different telomere-related DNA sequences. Nucl. Acids Res. 27:4687–4694.

    Google Scholar 

  • Vidal, M., Brachmann, R. K., Fattaey, A., Harlow, E., and Boeke, J. D. (1998). Reverse two-hybrid and one-hybrid systems to detect dissociation of protein–protein and DNA–protein interactions. Proc. Natl. Acad. Sci. U.S.A 93:10315–10320.

    Google Scholar 

  • Wotton, D., and Shore, D. (1998). A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 11:748–760.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Chambers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spink, K., Ho, J.C.Y., Tanaka, K. et al. The Telomere-Binding Protein Taz1p as a Target for Modification by a SUMO-1 Homologue in Fission Yeast. Biochem Genet 43, 103–117 (2005). https://doi.org/10.1007/s10528-005-1503-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-005-1503-4

Keywords:

Navigation