Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference

Molecular Biology of the Cell

Volumn 16, Issue 7, 2005, Pages 3187-3199

  Zhu, Changjun ^a   Zhao, Jian ^a,d   Bibikova, Marina ^b   Leverson, Joel D ^c   Bossy Wetzel, Ella ^a   Fan, Jian Bing ^b   Abraham, Robert T ^a   Jiang, Wei ^a  

^a BURNHAM INSTITUTE   (United States)

^b ILLUMINA INC   (United States)

^c ABBOTT LABORATORIES   (United States)

^d SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MOLECULAR MOTOR; PROTEIN EG5; PROTEIN KID; PROTEIN KIF18; PROTEIN KIF2A; PROTEIN KIF4A; PROTEIN KIF4B; PROTEIN KIFC1; PROTEIN MCAK; PROTEIN MKLP1; PROTEIN MKLP2; RIBONUCLEASE III; RNA; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CELL DIVISION; CHROMOSOME CONDENSATION; CONTROLLED STUDY; CYTOKINESIS; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; RNA INTERFERENCE;

3' UNTRANSLATED REGIONS; ANAPHASE; BIOCHEMISTRY; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; CYTOKINESIS; DYNEIN ATPASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GENE LIBRARY; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; KINESIN; KINETOCHORES; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PHENOTYPE; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; TIME FACTORS; TRANSFECTION;

ESCHERICHIA COLI;

EID: 21844473254     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-02-0167     Document Type: Article

References (70)

1. Abaza, A., Soleilhac, J. M., Westendorf, J., Piel, M., Crevel, I., Roux, A., and Pirollet, F. (2003). M phase phosphoprotein 1 is a human plus-end-directed kinesin-related protein required for cytokinesis. J. Biol. Chem. 278, 27844-27852.
2. Andrews, P. D., Ovechkina, Y., Morrice, N., Wagenbach, M., Duncan, K., Wordeman, L., and Swedlow, J. R. (2004). Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 6, 233-268.
3. Antonio, C., Ferby, I., Wilhelm, H., Jones, M., Karsenti, E., Nebreda, A. R., and Vernos, I. (2000). Xkid, a chromokinesin required for chromosome alignment on the metaphase plate. Cell 102, 425-435.
4. Blangy, A., Lane, H. A., d'Herin, P., Harper, M., Kress, M., and Nigg, E. A. (1995). Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83, 1159-1169.
5. Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W. C., and Wheatley, S. P. (2003). Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J. Cell Sci. 116, 2987-2998.
6. Cassimeris, L., and Morabito, J. (2004). TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol. Biol. Cell 15, 1580-1590.
7. Chan, G. K., Jablonski, S. A., Sudakin, V., Hittle, J. C., and Yen, T. J. (1999). Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC. J. Cell Biol. 146, 941-954.
8. Chan, G. K., Schaar, B. T., and Yen, T. J. (1998). Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1. J. Cell Biol. 143, 49-63.
9. Chen, M. C., Zhou, Y., and Detrich, H. W., 3rd. (2002). Zebrafish mitotic kinesin-like protein 1 (Mklp1) functions in embryonic cytokinesis. Physiol. Genorn. 8, 51-66.
10. Cleveland, D. W., Mao, Y., and Sullivan, K. F. (2003). Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421.
11. Cottingham, F. R., and Hoyt, M. A. (1997). Mitotic spindle positioning in Saccharomyces cercevisiae is accomplished by antagonistically acting microtubule motor proteins. J. Cell Biol. 138, 1041-1053.
12. Desai, A., Verma, S., Mitchison, T. J., and Walczak, C. E. (1999). Kin I kinesins are microtubule-destabilizing enzymes. Cell 96, 69-78.
13. Echard, A., Jollivet, F., Martinez, O., Lacapere, J. J., Rousselet, A., Janoueix-Lerosey, I., and Goud, B. (1998). Interaction of a Golgi-associated kinesin-like protein with Rab6. Science 279, 580-585.
14. Echeverri, C. J., Paschal, B. M., Vaughan, K. T., and Vallee, R. B. (1996). Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132, 617-633.
15. Fontijn, R. D., Goud, B., Echard, A., Jollivet, F., van Marie, J., Pannekoek, H., and Horrevoets, A. J. (2001). The human kinesin-like protein RB6K is under tight cell cycle control and is essential for cytokinesis. Mol. Cell. Biol. 27, 2944-2955.
16. Funabiki, H., and Murray, A. W. (2000). The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 102, 411-424.
17. Gaetz, J., and Kapoor, T. M. (2004). Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J. Cell Biol. 166, 465-471.
18. Gandhi, R., Bonaccorsi, S., Wentworth, D., Doxsey, S., Gatti, M., and Pereira, A. (2004). The Drosophila kinesin-like protein KLP67A is essential for mitotic and male meiotic spindle assembly. Mol. Biol. Cell 15, 121-131.
19. Ganem, N. J., and Compton, D. A. (2004). The KinI kinesin Kif2a is required for bipolar spindle assembly through a functional relationship with MCAK. J. Cell Biol. 166, 473-478.
20. Garcia, M. A., Koonrugsa, N., and Toda, T. (2002). Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast. EMBO J. 21, 6015-6024.
21. Gorbsky, G. J. (2004). Mitosis: MCAK under the aura of Aurora B. Curr. Biol. 14, R346-R348.
22. Goshima, G., and Vale, R. D. (2003). The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162, 1003-1016.
23. Gruneberg, U., Neef, R., Honda, R., Nigg, E. A., and Barr, F. A. (2004). Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKIp2. J. Cell Biol. 166, 167-172.
24. Hildebrandt, E. R., and Hoyt, M. A. (2000). Mitotic motors in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1496, 99-116.
25. Hill, E., Clarke, M., and Barr, F. A. (2000). The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis. EMBO J. 19, 5711-5719.
26. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S. V., Burchard, J., Mao, M., Li, B., Cavet, G., and Linsley, P. S. (2003). Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635-637.
27. Jiang, W., Jimenez, G., Wells, N. J., Hope, T. J., Wahl, G. M., Hunter, T., and Fukunaga, R. (1998). PRC1, a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell 2, 877-885.
28. Kapoor, T. M., and Compton, D. A. (2002). Searching for the middle ground: mechanisms of chromosome alignment during mitosis. J. Cell Biol. 157, 551-556.
29. Kapoor, T. M., Mayer, T. U., Coughlin, M. L., and Mitchison, T. J. (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150, 975-988.
30. Kapoor, T. M., and Mitchison, T. J. (2001). Eg5 is static in bipolar spindles relative to tubulin: evidence for a static spindle matrix. J. Cell Biol. 154, 1125-1133.
31. Kittler, R. et al. (2004). An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division. Nature 432, 1036-1040.
32. Kline-Smith, S. L., Khodjakov, A., Hergert, P., and Walczak, C. E. (2004). Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments. Mol. Biol. Cell 15, 1146-1159.
33. Kurasawa, Y., Earnshaw, W. C., Mochizuki, Y., Dohmae, N., and Todokoro, K. (2004). Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 23, 3237-3248.
34. Kwon, M., Morales-Mulia, S., Brust-Mascher, I., Rogers, G. C., Sharp, D. J., and Scholey, J. M. (2004). The chromokinesin, KLP3A, dives mitotic spindle pole separation during prometaphase and anaphase and facilitates chromatid motility. Mol. Biol. Cell 15, 219-233.
35. Lan, W., Zhang, X., Kline-Smith, S. L., Rosasco, S. E., Barrett-Wilt, G. A., Shabanowitz, J., Hunt, D. F., Walczak, C. E., and Stukenberg, P. T. (2004). Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr. Biol. 14, 273-286.
36. Lawrence, C. J. et al. (2004). A standardized kinesin nomenclature. J. Cell Biol. 167, 19-22.
37. Lee, Y. M., and Kim, W. (2004). Kinesin superfamily protein member 4 (KIF4) is localized to midzone and midbody in dividing cells. Exp. Mol. Med. 36, 93-97.
38. Levesque, A. A., and Compton, D. A. (2001). The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J. Cell Biol. 154, 1135-1146.
39. Mandelkow, E., and Mandelkow, E. M. (2002). Kinesin motors and disease. Trends Cell Biol. 12, 585-591.
40. Maney, T., Hunter, A. W., Wagenbach, M., and Wordeman, L. (1998). Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. J. Cell Biol. 142, 787-801.
41. Mao, Y., Abrieu, A., and Cleveland, D. W. (2003). Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/ inactivation of BubR1. Cell 114, 87-98.
42. Matuliene, J., and Kuriyama, R. (2004). Role of the midbody matrix in cytokinesis: RNAi and genetic rescue analysis of the mammalian motor protein CHO1. Mol. Biol. Cell 15, 3083-3094.
43. Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L., and Mitchison, T. J. (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenorype-based screen. Science 286, 971-974.
44. Mazumdar, M., Sundareshan, S., and Misteli, T. (2004). Human chromokinesin KIF4A functions in chromosome condensation and segregation. J. Cell Biol. 166, 613-620.
45. McEwen, B. F., Chan, G. K., Zubrowski, B., Savoian, M. S., Sauer, M. T., and Yen, T. J. (2001). CENP-E is essential for reliable bioriented spindle attachment, but chromosome alignment can be achieved via redundant mechanisms in mammalian cells. Mol. Biol. Cell 12, 2776-2789.
46. Miki, H., Setou, M., Kaneshiro, K., and Hirokawa, N. (2001). All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. USA 98, 7004-7011.
47. Mishima, M., Kaitna, S., and Glotzer, M. (2002). Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54.
48. Mishima, M., Pavicic, V., Gruneberg, U., Nigg, E. A., and Glotzer, M. (2004). Cell cycle regulation of central spindle assembly. Nature 430, 908-913.
49. Molina, I., Baars, S., Brill, J. A., Hales, K. G., Fuller, M. T., and Ripoll, P. (1997). A chromatin-associated kinesin-related protein required for normal mitotic chromosome segregation in Drosophila. J. Cell Biol. 139, 1361-1371.
50. Mountain, V., Simerly, C., Howard, L., Ando, A., Schatten, G., and Compton, D. A. (1999). The kinesin-related protein, HSET, opposes the activity of Eg5 and cross-links microtubules in the mammalian mitotic spindle. J. Cell Biol. 147, 351-366.
51. Neef, R., Preisinger, C., Sutcliffe, J., Kopajtich, R., Nigg, E. A., Mayer, T. U., and Barr, F. A. (2003). Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162, 863-875.
52. Ohi, R., Sapra, T., Howard, J., and Mitchison, T. J. (2004). Differentiation of cytoplasmic and meiotic spindle assembly MCAK functions by Aurora B-dependent phosphorylation. Mol. Biol. Cell 15, 2895-2906.
53. Ohkura, H., Torok, T., Tick, G., Hoheisel, J., Kiss, I., and Glover, D. M. (1997). Mutation of a gene for a Drosophila kinesin-like protein, Klp38B, leads to failure of cytokinesis. J. Cell Sci. 110(Pt 8), 945-954.
54. Putkey, F. R., Cramer, T., Morphew, M. K., Silk, A. D., Johnson, R. S., McIntosh, J. R., and Cleveland, D. W. (2002). Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Dev. Cell 3, 351-365.
55. Rischitor, P. E., Konzack, S., and Fischer, R. (2004). The Kip3-like kinesin KipB moves along microtubules and determines spindle position during synchronized mitoses in Aspergillus nidulans hyphae. Eukaryot. Cell 3, 632-645.
56. Sakowicz, R. et al. (2004). Antitumor activity of a kinesin inhibitor. Cancer Res. 64, 3276-3280.
57. Savoian, M. S., Gatt, M. K., Riparbelli, M. G., Callaini, G., and Glover, D. M. (2004). Drosophila Klp67A is required for proper chromosome congression and segregation during meiosis 1. J. Cell Sci. 117, 3669-3677.
58. Schaar, B. T., Chan, G. K., Maddox, P., Salmon, E. D., and Yen, T. J. (1997). CENP-E function at kinetochores is essential for chromosome alignment. J. Cell Biol. 139, 1373-1382.
59. Shannon, K. B., and Salmon, E. D. (2002). Chromosome dynamics: new light on Aurora B kinase function. Curr. Biol. 12, R458-R460.
60. Snove, O., Jr., and Holen, T. (2004). Many commonly used siRNAs risk off-target activity. Biochem. Biophys. Res. Commun. 319, 256-263.
61. Tanudji, M., Shoemaker, J., L'Italien, L., Russell, L., Chin, G., and Schebye, X. M. (2004). Gene silencing of CENP-E by small interfering RNA in HeLa cells leads to missegregation of chromosomes after a mitotic delay. Mol. Biol. Cell 15, 3771-3781.
62. Vale, R. D. (2003). The molecular motor toolbox for intracellular transport. Cell 112, 467-480.
63. Walczak, C. E., Mitchison, T. J., and Desai, A. (1996). XKCM1, a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84, 37-47.
64. Walczak, C. E., Vernos, I., Mitchison, T. J., Karsenti, E., and Heald, R. (1998). A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr. Biol. 8, 903-913.
65. Waters, J. C., Skibbens, R. V., and Salmon, E. D. (1996). Oscillating mitotic newt lung cell kinetochores are, on average, under tension and rarely push. J. Cell Sci. 109(Pt 12), 2823-2831.
66. Weaver, B. A., Bonday, Z. Q., Putkey, F. R., Kops, G. J., Silk, A. D., and Cleveland, D. W. (2003). Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J. Cell Biol. 162, 551-563.
67. West, R. R., Malmstrom, T., and McIntosh, J. R. (2002). Kinesins klp5(+) and klp6(+) are required for normal chromosome movement in mitosis. J. Cell Sci. 115, 931-940.
68. Yang, D., Buchholz, F., Huang, Z., Goga, A., Chen, C. Y., Brodsky, F. M., and Bishop, J. M. (2002). Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 99, 9942-9947.
69. Zhu, C., Bossy-Wetzel, E., and Jiang, W. (2005). Recruitment of MKLP1 to the spindle midzone/midbody by INCENP is essential for midbody formation and completion of cytokinesis in human cells. Biochem. J. (in press).
70. Zhu, C., and Jiang, W. (2005). Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc. Natl. Acad. Sci. USA 102, 343-348.