Phosphorylation by casein kinase 2 facilitates Psh1 proteinassisted degradation of Cse4 protein

Journal of Biological Chemistry

Volumn 289, Issue 42, 2014, Pages 29297-29309

  Hewawasam, Geetha S ^a   Mattingly, Mark ^a   Venkatesh, Swaminathan ^a   Zhang, Ying ^a   Florens, Laurence ^a   Workman, Jerry L ^a   Gerton, Jennifer L ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CASEIN; ENZYMES; PROTEINS;

BUDDING YEASTS; CASEIN KINASE 2; HISTONE H3; MISLOCALIZATION; MUTANT STRAIN; PHOSPHORYLATION SITES; UBIQUITIN LIGASES;

PHOSPHORYLATION;

ALANINE; CASEIN KINASE II; HISTONE H3; PROTEIN CSE4; PROTEIN PSH1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CSE4 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; ELONGATION FACTOR; NONHISTONE PROTEIN; PROTEASOME; PSH1 PROTEIN, S CEREVISIAE; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; ENZYME ACTIVITY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; YEAST CELL; CATALYSIS; CENTROMERE; ENZYMOLOGY; GENE DELETION; METABOLISM; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

CASEIN KINASE II; CATALYSIS; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; GENE DELETION; KINETOCHORES; PEPTIDE ELONGATION FACTORS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84908032078     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.580589     Document Type: Article

References (39)

1. Furuyama, S., and Biggins, S. (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc. Natl. Acad. Sci. U. S. A. 104, 14706-14711
2. Hyman, A. A., and Sorger, P. K. (1995) Structure and function of kinetochores in budding yeast. Annu. Rev. Cell Dev. Biol. 11, 471-495
3. Cheeseman, I. M., Drubin, D. G., and Barnes, G. (2002) Simple centromere, complex kinetochore: linking spindle microtubules and centromeric DNA in budding yeast. J. Cell Biol. 157, 199-203
4. Collins, K. A., Camahort, R., Seidel, C., Gerton, J. L., and Biggins, S. (2007) The overexpression of a Saccharomyces cerevisiae centromeric histone H3 variant mutant protein leads to a defect in kinetochore biorientation. Genetics 175, 513-525
5. Au, W. C., Crisp, M. J., DeLuca, S. Z., Rando, O. J., and Basrai, M. A. (2008) Altered dosage and mislocalization of histone H3 and Cse4p lead to chromosome loss in Saccharomyces cerevisiae. Genetics 179, 263-275
6. Van Hooser, A. A., Ouspenski, I. I., Gregson, H. C., Starr, D. A., Yen, T. J., Goldberg, M. L., Yokomori, K., Earnshaw, W. C., Sullivan, K. F., and Brinkley, B. R. (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114, 3529-3542
7. Amato, A., Schillaci, T., Lentini, L., and Di Leonardo, A. (2009) CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol. Cancer 8, 119
8. Tomonaga, T., Matsushita, K., Yamaguchi, S., Oohashi, T., Shimada, H., Ochiai, T., Yoda, K., and Nomura, F. (2003) Overexpression and mistargeting of centromere protein-A inhuman primary colorectal cancer. Cancer Res. 63, 3511-3516
9. Collins, K. A., Furuyama, S., and Biggins, S. (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 14, 1968-1972
10. Moreno-Moreno, O., Torras-Llort, M., and Azorín, F. (2006) Proteolysis restricts localizationof CID, the centromere-specific histone H3variant of Drosophila, to centromeres. Nucleic Acids Res. 34, 6247-6255
11. Hewawasam, G., Shivaraju, M., Mattingly, M., Venkatesh, S., Martin-Brown, S., Florens, L., Workman, J. L., and Gerton, J. L. (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol. Cell 40, 444-454
12. Ranjitkar, P., Press, M. O., Yi, X., Baker, R., MacCoss, M. J., and Biggins, S. (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell 40, 455-464
13. Moreno-Moreno, O., Medina-Giró, S., Torras-Llort, M., and Azorín, F. (2011) TheFbox protein partner of paired regulates stability of Drosophila centromeric histone H3, CenH3 (CID). Curr. Biol. 21, 1488-1493
14. Hunter, T. (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738
15. Block, K., Boyer, T. G., and Yew, P. R. (2001) Phosphorylation of the human ubiquitin-conjugating enzyme, CDC34, by casein kinase 2. J. Biol. Chem. 276, 41049-41058
16. Coccetti, P., Tripodi, F., Tedeschi, G., Nonnis, S., Marin, O., Fantinato, S., Cirulli, C., Vanoni, M., and Alberghina, L. (2008) The CK2 phosphorylation of catalytic domain of Cdc34 modulates its activity at the G1 to S transition in Saccharomyces cerevisiae. Cell Cycle 7, 1391-1401
17. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., Wilm, M., and Séraphin, B. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229
18. Akiyoshi, B., Sarangapani, K. K., Powers, A. F., Nelson, C. R., Reichow, S. L., Arellano-Santoyo, H., Gonen, T., Ranish, J. A., Asbury, C. L., and Biggins, S. (2010) Tension directly stabilizes reconstituted kinetochoremicrotubule attachments. Nature 468, 576-579
19. Meggio, F., and Pinna, L. A. (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17, 349-368
20. Glover, C. V., 3rd (1998) On the physiological role of casein kinase II in Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 59, 95-133
21. Liu, C., Apodaca, J., Davis, L. E., and Rao, H. (2007) Proteasome inhibition in wild-type yeast Saccharomyces cerevisiae cells. BioTechniques 42, 158, 160, 162
22. Ohkuni, K., Abdulle, R., and Kitagawa, K. (2014) Degradation of centromeric histone H3 variant Cse4 requires the Fpr3 peptidyl-prolyl cis-trans isomerase. Genetics 196, 1041-1045
23. Wilson, L. K., Dhillon, N., Thorner, J., and Martin, G. S. (1997) Casein kinase II catalyzes tyrosine phosphorylation of the yeast nucleolar immunophilin Fpr3. J. Biol. Chem. 272, 12961-12967
24. Pardo, P. S., Murray, P. F., Walz, K., Franco, L., and Passeron, S. (1998) In vivo and in vitro phosphorylation of the a7/PRS1 subunit of Saccharomyces cerevisiae 20 S proteasome: in vitro phosphorylation by protein kinase CK2 is absolutely dependent on polylysine. Arch. Biochem. Biophys. 349, 397-401
25. Ludemann, R., Lerea, K. M., and Etlinger, J. D. (1993) Copurification of casein kinase II with 20 S proteasomes and phosphorylation of a 30-kDa proteasome subunit. J. Biol. Chem. 268, 17413-17417
26. Kim, I. S., Lee, M., Park, J. H., Jeon, R., Baek, S. H., and Kim, K. I. (2014) βTrCP-mediated ubiquitylation regulates protein stability of Mis18β in a cell cycle-dependent manner. Biochem. Biophys. Res. Commun. 443, 62-67
27. Willems, A. R., Schwab, M., and Tyers, M. (2004) A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim. Biophys. Acta 1695, 133-170
28. Sadowski, M., Mawson, A., Baker, R., and Sarcevic, B. (2007) Cdc34 C-terminal tail phosphorylation regulates Skp1/cullin/F-box (SCF)-mediated ubiquitination and cell cycle progression. Biochem. J. 405, 569-581
29. Shivaraju, M., Camahort, R., Mattingly, M., and Gerton, J. L. (2011) Scm3 is a centromeric nucleosome assembly factor. J. Biol. Chem. 286, 12016-12023
30. Camahort, R., Li, B., Florens, L., Swanson, S. K., Washburn, M. P., and Gerton, J. L. (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26, 853-865
31. Lacoste, N., Woolfe, A., Tachiwana, H., Garea, A. V., Barth, T., Cantaloube, S., Kurumizaka, H., Imhof, A., and Almouzni, G. (2014) Mislocalization of the centromeric histone variant CenH3/CENP-A inhuman cells depends on the chaperone DAXX. Mol. Cell 53, 631-644
32. Mishra, P. K., Ottmann, A. R., and Basrai, M. A. (2013) Structural integrity of centromeric chromatin and faithful chromosome segregation requires Pat1. Genetics 195, 369-379
33. Haase, J., Mishra, P. K., Stephens, A., Haggerty, R., Quammen, C., Taylor, R. M., 2nd, Yeh, E., Basrai, M. A., and Bloom, K. (2013) A 3D map of the yeast kinetochore reveals the presence of core and accessory centromerespecific histone. Curr. Biol. 23, 1939-1944
34. Krogan, N. J., Kim, M., Ahn, S. H., Zhong, G., Kobor, M. S., Cagney, G., Emili, A., Shilatifard, A., Buratowski, S., and Greenblatt, J. F. (2002) RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22, 6979-6992
35. Peng, Y., Wong, C. C., Nakajima, Y., Tyers, R. G., Sarkeshik, A. S., Yates, J., 3rd, Drubin, D. G., and Barnes, G. (2011) Overlapping kinetochore targets of CK2 and Aurora B kinases in mitotic regulation. Mol. Biol. Cell 22, 2680-2689
36. Lampson, M. A., and Cheeseman, I. M. (2011) Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 21, 133-140
37. London, N., Ceto, S., Ranish, J. A., and Biggins, S. (2012) Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr. Biol. 22, 900-906
38. Zybailov, B., Mosley, A. L., Sardiu, M. E., Coleman, M. K., Florens, L., and Washburn, M. P. (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339-2347
39. Belle, A., Tanay, A., Bitincka, L., Shamir, R., and O'Shea, E. K. (2006) Quantification of protein half-lives in the budding yeast proteome. Proc. Natl. Acad. Sci. U. S. A. 103, 13004-13009