Genetic analysis of the kinetochore DASH complex reveals an antagonistic relationship with the Ras/protein kinase A pathway and a novel subunit required for Ask1 association

Molecular and Cellular Biology

Volumn 25, Issue 2, 2005, Pages 767-778

  Li, Ju Mei ^a,b   Li, Yumei ^b   Elledge, Stephen J ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHODIESTERASE; PHOSPHODIESTERASE 2; PROTEIN ASK 1; PROTEIN ASK 2; PROTEIN ASK 3; PROTEIN DAM 1; PROTEIN DUO 1; PROTEIN HSK 2; PROTEIN HSK 3; PROTEIN SPC 19; PROTEIN SPC 34; PROTEIN SUBUNIT; RAS 2 PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CENTROMERE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE INTERACTION; GENE LOCATION; GENETIC ANALYSIS; IN VIVO STUDY; MITOSIS INHIBITION; MITOSIS SPINDLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; TEMPERATURE SENSITIVITY;

AMINO ACID SEQUENCE; CELL CYCLE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PHENOTYPE; PROTEIN SUBUNITS; RAS PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TEMPERATURE;

ANIMALIA;

EID: 11844306595     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.2.767-778.2005     Document Type: Article

References (52)

1. Adams, I. R., and J. V. Kilmartin. 2000. Spindle pole bodies duplication: a model for centrosome duplication? Trends Cell Biol. 10:329-335.
2. Amon, A. 1999. The spindle checkpoint. Curr. Opin. Genet. Dev. 9:69-75.
3. Aparicio, O. M., D. M. Weinstein, and S. P. Bell. 1997. Components and dynamics of DNA replication complexes in 5. cerevisiae: restriction of MCM proteins and Cdc45p during S phase. Cell 91:59-69.
4. Biggins, S., and C. E. Walczak. 2003. Captivating capture: how microtubules attach to kinetochores. Curr. Biol. 13:R449-R460.
5. Bischoff, J. R., and G. D. Plowman. 1999. The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis. Trends Cell Biol. 9:454-459.
6. Bolte, M., P. Dieckhoff, C. Krause, G. H. Braus, and S. Irniger. 2003. Synergistic inhibition of APC/C by glucose and activated Ras proteins can be mediated by each of the Tpk1-3 proteins in Saccharomyces cerevisiae. Microbiology 149:1205-1216.
7. Breviario, D., A. G. Hinnebusch, and R. Dhar. 1988. Multiple regulatory mechanisms control the expression of the RAS1 and RAS2 genes of Saccharomyces cerevisiae. EMBO J. 7:1805-1813.
8. Cheeseman, I. M., S. Anderson, M. Jwa, E. M. Green, J. Kang, J. R. Yates III, S. M. Chan, D. Grubin, and G. Barnes. 2002. Phospho-regulation of kinetochore-microtubule attachments by the aurora kinase Ipl1p. Cell 111: 163-172.
9. Cheeseman, I. M., C. Brew, M. Wolyniak, A. Desai, S. Anderson, N. Muster, J. R. Yates, T. C. Huffaker, D. G. Drubin, and G. Barnes. 2001. Implication of a novel multiprotein Dam1p complex in outer kinetochore function. J. Cell Biol. 155:1137-1145.
10. Ciosk, R., W. Zachariae, C. Michaelis, A. Shevchenko, M. Mann, and K. Nasmyth. 1998. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93:1067-1076.
11. Cleveland, D. W., Y. Mao, and K. F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407-421.
12. Connelly, C., and P. Hieter. 1996. Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86:275-285.
13. Enquist-Newman, M., I. M. Cheeseman, D. Van Goor, D. G. Drubin, P. B. Meluh, and G. Barnes. 2001. Dad1p, third component of the Duo1p/Dam1p complex involved in kinetochore function and mitotic spindle integrity. Mol. Biol. Cell 12:2601-2613.
14. Farr, K. A., and M. A. Hoyt. 1998. Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint. Mol. Cell. Biol. 18:2738-2747.
15. Hardwick, K. G., and A. W. Murray. 1995. Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol. 131:709-720.
16. Hardwick, K. G., E. Weiss, F. C. Luca, M. Winey, and A. W. Murray. 1996. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273:953-956.
17. Heo, S. J., K. Tatebayashi, and H. Ikeda. 1999. The budding yeast cohesin gene SCC1/MCD1/RHC21 genetically interacts with PKA, CDK and APC. Curr. Genet. 36:329-338.
18. Hofmann, C., I. M. Cheeseman, B. L. Goode, K. L. McDonald, G. Barnes, and D. G. Drubin. 1998. Saccharomyces cerevisiae Duo1p and Dam1p, novel proteins involved in mitotic spindle function. J. Cell Biol. 143:1029-1040.
19. Hoyt, M. A., and J. R. Geiser. 1996. Genetic analysis of the mitotic spindle. Annu. Rev. Genet. 30:7-33.
20. Hoyt, M. A., L. Totis, and B. T. Roberts. 1991. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66:507-517.
21. Ikeuchi, A., Y. Sasaki, Y. Kawarasaki, and T. Yamane. 2003. Exhaustive identification of interaction domains using a high-throughput method based on two-hybrid screening and PCR-convergence: molecular dissection of a kinetochore subunit Spc34p. Nucleic Acids Res. 31:6953-6962.
22. Irniger, S., M. Baumer, and G. H. Braus. 2000. Glucose and ras activity influence the ubiquitin ligases APC/C and SCF in Saccharomyces cerevisiae. Genetics 154:1509-1521.
23. Janke, C., J. Ortiz, T. U. Tanaka, J. Lechner, and E. Schiebel. 2002. Four new subunits of the Dam1-Duo1 complex reveal novel functions in sister kinetochore biorientation. EMBO J. 21:181-193.
24. Jones, M. H., J. B. Bachant, A. R. Castillo, T. H. Giddings, and M. Winey. 1999, Yeast Dam1p is required to maintain spindle integrity during mitosis and interacts with the Mps1p kinase. Mol. Biol. Cell 10:2377-2391.
25. Jones, M. H., X. He, T. H. Giddings, and M. Winey. 2001. Yeast Dam1p has a role at the kinetochore in assembly of the mitotic spindle. Proc. Natl. Acad. Sci. USA 98:13675-13680.
26. Kataoka, T., S. Powers, C. McGill, O. Fasano, J. Strathern, J. Broach, and M. Wigler. 1984. Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37:437-445.
27. Kim, J. H., J. S. Kang, and C. S. Chan. 1999. Sli15 associates with the ipl1 protein kinase to promote proper chromosome segregation in Saccharomyces cerevisiae. J. Cell Biol. 145:1381-1394.
28. Li, R., and A. W. Murray. 1991. Feedback control of mitosis in budding yeast. Cell 66:519-537.
29. Li, Y., J. Bachant, A. Alcasabas, Y. Wang, J. Qin, and S. J. Elledge. 2002. The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev. 16:183-197.
30. Li, Y., and S. J. Elledge. 2003. The DASH complex component Ask1 is a cell cycle-regulated Cdk substrate in Saccharomyces cerevisiae. Cell Cycle 2:78-83.
31. Longtime, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
32. McAinsh, A. D., J. D. Tytell, and P. K. Sorger. 2003. Structure, function, and regulation of budding yeast kinetochores. Annu. Rev. Cell Dev. Biol. 19: 519-539.
33. Meluh, P. B., and D. Koshland. 1997. Budding yeast centromere composition and assembly as revealed by in vitro cross-linking. Genes Dev. 11:3401-3412.
34. Musacchio, A., and K. G. Bardwick. 2002. The spindle checkpoint: structural insights into dynamic signaling. Nat. Rev. Mol. Cell Biol. 3:731-741.
35. Pangilinan, F., and F. Spencer. 1996. Abnormal kinetochore structure activates the spindle assembly checkpoint in budding yeast. Mol. Biol. Cell 7:1195-1208.
36. Pinsky, B. A., S. Y. Tatsutani, K. A. Collins, and S. Biggins. 2003. An Mtw1 complex promotes kinetochore biorientation that is monitored by the Ipl1/Aurora protein kinase. Dev. Cell 5:735-745.
37. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Seraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
38. Scharfenberger, M., J. Ortiz, N. Grau, C. Janke, E. Schiebel, and J. Lechner. 2003. Nsl1p is essential for the establishment of bipolarity and the localization of the Dam-Duo complex. EMBO J. 22:6584-6597.
39. Schneper, L., A. Krauss, R. Miyamoto, S. Fang, and J. R. Broach. 2004. The Ras/protein kinase A pathway acts in parallel with the Mob2/Cbk1 pathway to effect cell cycle progression and proper bud site selection. Eukaryot. Cell 3:108-120.
40. Searle, J. S., K. L. Schollaert, B. J. Wilkins, and Y. Sanchez. 2004. The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat. Cell Biol. 6:138-145.
41. Shang, C., T. R. Hazbun, I. M. Cheeseman, J. Aranda, S. Fields, D. G. Drubin, and G. Barnes. 2003. Kinetochore protein interactions and their regulation by the Aurora kinase Ipl1p. Mol. Biol. Cell 14:3342-3355.
42. Tanaka, T. U. 2002. Bi-orienting chromosomes on the mitotic spindle. Curr. Opin. Cell Biol. 14:365-371.
43. Tanaka, T. U., N. Rachidi, C. Janke, G. Pereira, M. Galova, E. Schiebel, M. J. Stark, and K. Nasmyth. 2002. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 8:317-329.
44. Toda, T., I. Uno, T. Ishikawa, S. Powers, T. Kataoka, D. Broek, S. Cameron, J. Broach, K. Matsumoto, and M. Wigler. 1985. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27-36.
45. Tokiwa, G., M. Tyers, T. Volpe, and B. Futcher. 1994. Inhibition of G1 cyclin activity by the Ras/cAMP pathway in yeast. Nature 371:342-345.
46. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
47. Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G. F. Berriz, R. L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D. S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J. N. Levinson, H. Lu, P. Menard, C. Munyana, A. B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A. M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S. L. Wong, L. V. Zhang, H. Zhu, C. G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F. P. Roth, G. W. Brown, B. Andrews, H. Bussey, and C. Boone. 2004. Global mapping of the yeast genetic interaction network. Science 303:808-813.
48. Uhlmann, F., F. Lottspeich, and K. Nasmyth. 1999. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Sccl. Nature 400:37-42.
49. Wang, H., and S. J. Elledge. 1999. DRC1, DNA replication and checkpoint protein 1, functions with DPB11 to control DNA replication and the S-phase checkpoint in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 96:3824-3829.
50. Wang, Y., and D. J. Burke. 1995. Checkpoint genes required to delay cell division in response to nocodazole respond to impaired kinetochore function in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6838-6844.
51. Winey, M., and E. T. O'Toole. 2001. The spindle cycle in budding yeast. Nat. Cell Biol. 3:23-27.
52. Zou, L., and B. Stillman. 2000. Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol. Cell. Biol. 20:3089-3096.