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.
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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.
Baumann, P., and Cech, T. R. (1998). Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171–1175.
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.
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.
Chikashige, Y., and Hiraoka, Y. (1998). Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr. Biol. 11:1618–1623.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lundblad, V., and Szostak, J. W. (1998) A mutant wih a defect in telomere elongation leads to senescence in yeast. Cell 57:633–643.
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.
Melchior, F. (1998). SUMO-Nonclassical ubiquitin. Ann. Rev. Cell Dev. Biol. 16:591–626.
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.
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.
Minty, A., Dumont, X., Kaghad, M., and Caput, D. (1998). Covalent modification of p73α by SUMO-1. J. Biol. Chem. 275:36316–36323.
Moreno, S., Klar, A., and Nurse, P. (1998). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823.
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.
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.
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.
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.
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.
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.
Rechsteiner, M., and Rogers, S. W. (1998). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267–271.
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.
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.
Sherman, F. (1998). Getting started with yeast. Methods Enzymol. 194:3–21.
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.
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.
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.
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.
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.
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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
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DOI: https://doi.org/10.1007/s10528-005-1503-4