The Cik1/Kar3 motor complex is required for the proper kinetochore- microtubule interaction after stressful DNA replication

Genetics

Volumn 187, Issue 2, 2011, Pages 397-407

  Liu, Hong ^a,c   Jin, Fengzhi ^b   Liang, Fengshan ^b   Tian, Xuemei ^b   Wang, Yanchang ^a,b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HYDROXYUREA; PROTEIN CIK1; PROTEIN KAR3; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; BACTERIAL STRAIN; CELL MUTANT; CENTROMERE; CHROMOSOME; CONCENTRATION (PARAMETERS); DNA REPLICATION; DNA SYNTHESIS; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENOME; MICROTUBULE; MOTOR PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS;

ANAPHASE; DNA REPLICATION; HYDROXYUREA; INTRACELLULAR SPACE; KINETOCHORES; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTATION; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 79951546976     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.125468     Document Type: Article

References (42)

1. ALCASABAS, A. A., A. J. OSBORN, J. BACHANT, F. HU, P. J. WERLER et al., 2001 Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3: 958-965.
2. ALLINGHAM, J. S., L. R. SPROUL, I. RAYMENT and S. P. GILBERT, 2007 Vik1 modulates microtubule-Kar3 interactions through a motor domain that lacks an active site. Cell 128: 1161-1172.
3. BARRETT, J. G., B. D. MANNING and M. SNYDER, 2000 The Kar3p kinesin-related protein forms a novel heterodimeric structure with its associated protein Cik1p. Mol. Biol. Cell 11: 2373-2385.
4. BRAUN, M., D. R. DRUMMOND, R. A. CROSS and A. D. MCAINSH, 2009 The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATP-dependent sorting mechanism. Nat. Cell Biol. 11: 724-730.
5. CHU, H. M., M. YUN, D. E. ANDERSON, H. SAGE, H. W. PARK et al., 2005 Kar3 interaction with Cik1 alters motor structure and function. EMBO J. 24: 3214-3223.
6. COHEN-FIX, O., J. M. PETERS, M. W. KIRSCHNER and D. KOSHLAND, 1996 Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10: 3081-3093.
7. D'AMOURS, D., F. STEGMEIER and A. AMON, 2004 Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117: 455-469.
8. ENDOW, S. A., S. J. KANG, L. L. SATTERWHITE, M. D. ROSE, V. P. SKEEN et al., 1994 Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J. 13: 2708-2713.
9. FINK, G., L. HAJDO, K. J. SKOWRONEK, C. REUTHER, A. A. KASPRZAK et al., 2009 The mitotic kinesin-14 Ncd drives directional microtubule-microtubule sliding. Nat. Cell Biol. 11: 717-723.
10. GACHET, Y., C. REYES, T. COURTHEOUX, S. GOLDSTONE, G. GAY et al., 2008 Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring dam1 and klp2. Mol. Biol. Cell 19: 1646-1662.
11. GARDNER, M. K., D. C. BOUCK, L. V. PALIULIS, J. B. MEEHL, E. T. O'TOOLE et al., 2008a Chromosome congression by Kinesin-5 motor-mediated disassembly of longer kinetochore microtubules. Cell 135: 894-906.
12. GARDNER, M. K., J. HAASE, K. MYTHREYE, J. N. MOLK, M. ANDERSON et al., 2008b The microtubule-based motor Kar3 and plus end-binding protein Bim1 provide structural support for the anaphase spindle. J. Cell Biol. 180: 91-100.
13. GOSHIMA, G., and M. YANAGIDA, 2000 Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell 100: 619-633.
14. HE, X., S. ASTHANA and P. K. SORGER, 2000 Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101: 763-775.
15. 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.
16. KHMELINSKII, A., C. LAWRENCE, J. ROOSTALU and E. SCHIEBEL, 2007 Cdc14-regulated midzone assembly controls anaphase B. J. Cell Biol. 177: 981-993.
17. KING, J. M., T. S. HAYS and R. B. NICKLAS, 2000 Dynein is a transient kinetochore component whose binding is regulated by microtubule attachment, not tension. J. Cell Biol. 151: 739-748.
18. LI, Y., J. BACHANT, A. A. ALCASABAS, Y. WANG, J. QIN et al., 2002 The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev. 16: 183-197.
19. LIU, H., and Y. WANG, 2006 The function and regulation of budding yeast Swe1 in response to interrupted DNA synthesis. Mol. Biol. Cell 17: 2746-2756.
20. LIU, H., F. LIANG, F. JIN and Y. WANG, 2008 The coordination of centro-mere replication, spindle formation, and kinetochore-microtubule interaction in budding yeast. PLoS Genet. 4: e1000262.
21. LONGTINE, M. S., A. MCKENZIE, 3RD, D. J. DEMARINI, N. G. SHAH, A. WACH et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
22. MADDOX, P. S., J. K. STEMPLE, L. SATTERWHITE, E. D. SALMON and K. BLOOM, 2003 The minus end-directed motor Kar3 is required for coupling dynamic microtubule plus ends to the cortical shmoo tip in budding yeast. Curr. Biol. 13: 1423-1428.
23. MANNING, B. D., J. G. BARRETT, J. A. WALLACE, H. GRANOK and M. SNYDER, 1999 Differential regulation of the Kar3p kinesin-related protein by two associated proteins, Cik1p and Vik1p. J. Cell Biol. 144: 1219-1233.
24. MELUH, P. B., and M. D. ROSE, 1990 KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60: 1029-1041.
25. MICHAELIS, C., R. CIOSK and K. NASMYTH, 1997 Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45.
26. MOLK, J. N., E. D. SALMON and K. BLOOM, 2006 Nuclear congression is driven by cytoplasmic microtubule plus end interactions in S. cerevisiae. J. Cell Biol. 172: 27-39.
27. ORTIZ, J., C. FUNK, A. SCHAFER and J. LECHNER, 2009 Stu1 inversely regulates kinetochore capture and spindle stability. Genes Dev. 23: 2778-2791.
28. PAGE, B. D., and M. SNYDER, 1992 CIK1: a developmentally regulated spindle pole body-associated protein important for microtubule functions in Saccharomyces cerevisiae. Genes Dev. 6: 1414-1429.
29. PAGE, B. D., L. L. SATTERWHITE, M. D. ROSE and M. SNYDER, 1994 Localization of the Kar3 kinesin heavy chain-related protein requires the Cik1 interacting protein. J. Cell Biol. 124: 507-519.
30. 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.
31. RIEDER, C. L., and S. P. ALEXANDER, 1990 Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells. J. Cell Biol. 110: 81-95.
32. SANCHEZ, Y., B. A. DESANY, W. J. JONES, Q. LIU, B. WANG et al., 1996 Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
33. SAUNDERS, W. S., D. KOSHLAND, D. ESHEL, I. R. GIBBONS and M. A. HOYT, 1995 Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128: 617-624.
34. SIKORSKI, R. S., and P. HIETER, 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
35. SPROUL, L. R., D. J. ANDERSON, A. T. MACKEY, W. S. SAUNDERS and S. P. GILBERT, 2005 Cik1 targets the minus-end kinesin depo-lymerase Kar3 to microtubule plus ends. Curr. Biol. 15: 1420-1427.
36. TANAKA, T., J. FUCHS, J. LOIDL and K. NASMYTH, 2000 Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat. Cell Biol. 2: 492-499.
37. TANAKA, K., N. MUKAE, H. DEWAR, M. VAN BREUGEL, E. K. JAMES et al., 2005 Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434: 987-994.
38. TANAKA, K., E. KITAMURA, Y. KITAMURA and T. U. TANAKA, 2007 Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J. Cell Biol. 178: 269-281.
39. TANG, X., and Y.WANG, 2006 Pds1/Esp1-dependent and -independent sister chromatid separation in mutants defective for protein phosphatase 2A. Proc. Natl. Acad. Sci. USA 103: 16290-16295.
40. VARMA, D., P. MONZO, S. A. STEHMAN and R. B. VALLEE, 2008 Direct role of dynein motor in stable kinetochore-microtubule attachment, orientation, and alignment. J. Cell Biol. 182: 1045-1054.
41. 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.
42. ZHANG, T., H. H. LIM, C. S. CHENG and U. SURANA, 2006 Deficiency of centromere-associated protein Slk19 causes premature nuclear migration and loss of centromeric elasticity. J. Cell Sci. 119: 519-531.