The Drosophila Kinesin-like Protein KLP67A Is Essential for Mitotic and Male Meiotic Spindle Assembly

Molecular Biology of the Cell

Volumn 15, Issue 1, 2004, Pages 121-131

  Gandhi, Rita ^a   Bonaccorsi, Silvia ^b   Wentworth, Diana ^a   Doxsey, Stephen ^a   Gatti, Maurizio ^c   Pereira, Andrea ^b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; KINESIN LIKE PROTEIN 67A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIVISION; CELL MUTANT; CENTROSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; DROSOPHILA; FEMALE; MALE; MEIOSIS; METAPHASE; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE;

ANIMALS; CENTROSOME; CHROMOSOME SEGREGATION; DROSOPHILA; DROSOPHILA PROTEINS; GENES, FUNGAL; MALE; MEIOSIS; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; RNA, SMALL INTERFERING; SPERMATOCYTES; TUBULIN;

ANIMALIA; ARACHNIDA; HEXAPODA;

EID: 0347990574     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-05-0342     Document Type: Article

References (55)

1. Adams, R.R., Tavares, A.A., Salzberg, A., Bellen, H.J., and Glover, D.M. (1998). pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12, 1483-1494.
2. Basto, R., Gomes, R., and Karess, R.E. (2000). Rough Deal and Zw10 are required for the metaphase checkpoint in Drosophila. Nat. Cell Biol. 2, 939-943.
3. Bonaccorsi, S., Giansanti M.G., and Gatti, M. (1998). Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J. Cell Biol. 142, 751-761.
4. Cassimeris, L. (1999). Accessory protein regulation of microtubule dynamics throughout the cell cycle. Curr. Opin. Cell Biol. 11, 134-141.
5. Cenci, G., Bonaccorsi, S., Pisano, C., Verni, F., and Gatti, M. (1994). Chromatin and microtubule organization during premeiotic meiotic, and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J. Cell Sci. 107, 3521-3534.
6. Cottingham, F.R., Gheber, L., Miller, D.L., and Hoyt, M.A. (1999). Novel roles for Saccharomyces cerevisiae mitotic spindle motors. J. Cell Biol. 147, 335-349.
7. Cottingham, F.R., and Hoyt, M.A. (1997). Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins. J. Cell Biol. 138, 1041-1053.
8. Deak, P., et al. (1997). P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics 147, 1697-1722.
9. Desai, A., and Mitchison, T.J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
10. DeZwaan, T.M., Ellingson, E., Pellman, D., and Roof, D.M. (1997). Kinesin related KIP3 of Saccharomyces cerevisiae is required for a distinct step in nuclear migration. J. Cell Biol. 138, 1023-1040.
11. Eggert, H., Bergemann, K., and Saumweber, H. (1998). Molecular screening for P-element insertions in a large genomic region of Drosophila melanogaster using polymerase chain reaction mediated by the vectorette. Genetics 149, 1427-1434.
12. Endow, S. A. and Kim, A. J. (2000). The kinesin tree. http://www.blocks.fh-crc.org/%7Ekinesin/
13. Fuller, M.T. (1993). Spermatogenesis. In: The Development of Drosophila melanogaster, vol. I., ed. M. Bate and A.M. Arias, Plainview, NY: Cold Spring Harbor Laboratory Press, 71-147.
14. Gatti, M., Giansanti, M.G., and Bonaccorsi, S. (2000). Relationships between the central spindle and the contractile ring during cytokinesis in animal cells. Microsc. Res. Tech. 49, 202-208.
15. Gonzalez, C., Casal, J., and Ripoll, P. (1989). Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. Genet. Res. 54, 205-212.
16. Gunsalus, K., Bonaccorsi, S., Williams, E., Verni, F., Gatti, M., and Goldberg, M. (1995). Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131, 1243-1259.
17. Heck, M.M.S., Pereira, A., Pesavento, P., Yannoni, Y., Spradling, A.C., and Goldstein, L.S.B. (1993). The kinesin-like protein KLP61F is essential for mitosis in Drosophila. J. Cell Biol. 123, 665-679.
18. Holy, T.E., and Leibler, S. (1994). Dynamic instability of microtubules as an efficient way to search in space. Proc. Nat. Acad. Sci. USA 91, 5682-5685.
19. Hunter, A.W., Caplow, M., Coy, D.L., Hancock, W.O., Diez, S., Wordeman, L., and Howard, J. (2003). The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol. Cell 11, 445-457.
20. Kirschner, M., and Mitchison, T. (1986). Beyond self-assembly: from microtubules to morphogenesis. Cell 45, 329-342.
21. Kline-Smith, S.L., and Walczak, C.E. (2002). The microtubule-destabilizing kinesin XKCM1 regulates microtubule dynamic instability in cells. Mol. Biol. Cell 13, 2718-2731.
22. Korinek, W.S., Copeland, M.J., Chaudhuri, A., and Chant, J. (2000). Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science 287, 2257-2259.
23. Lee, L., Tirnauer, J.S., Li, J., Schuyler, S.C., Liu, J.Y., and Pellman, D. (2000). Positioning of the microtubule spindle by a cortical-microtubule capture mechanism. Science 287, 2260-2262.
24. Leicht, B.L., and Bonner, J.J. (1988). Genetic analysis of chromosomal region 67A-D of Drosophila melanogaster. Genetics 119, 579-593.
25. Li, K., and Kaufman, T.C. (1996). The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85, 585-596.
26. 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.
27. Mastronarde, D.N., McDonald, K.L., Ding, R., and McIntosh, J.R. (1993). Interpolar spindle microtubules in PTK cells. J. Cell Biol. 123, 1475-1489.
28. Miki, H., Setou, M., Kaneshiro, K., and Hirokawa, N. (2001). All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Nat. Acad. Sci. USA 98, 7004-7011.
29. Mitchison, T.J., Evans, L., Schulze, E., and Kirschner, M. (1986). Sites of microtubule assembly and disassembly in the mitotic spindle. Cell 45, 515-527.
30. Nangaku, M., Sato-Yoshitake, R., Okada, Y., Noda, Y., Takemura, R., Yamazaki, H., and Hirokawa, N. (1994). KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79, 1209-1220.
31. Pereira, A.J., Dalby, B., Stewart, R.J., Doxsey, S.J., and Goldstein, L.S.B. (1997). Mitochondrial association of a plus end-directed microtubule motor expressed during mitosis in Drosophila. J. Cell Biol. 136, 1081-1090.
32. Rebollo, E., and Gonzalez, C. (2000). Visualizing the spindle checkpoint in Drosophila spermatocytes. EMBO Rep. 1, 65-70.
33. Riparbelli, M.G., Callaini, G., Glover, D.M., and Avides Mdo, C. (2002). A requirement for the Abnormal Spindle protein to organize microtubules of the central spindle for cytokinesis in Drosophila. J. Cell Sci. 115, 913-922.
34. Robinson, J.T., Wojcik, E.J., Sanders, M.A., McGrail, M., and Hays, T.S. (1999). Cytoplasmic dynein is required for nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146, 597-608.
35. Rorth, P. (1996). A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Genetics 93, 12418-12422.
36. Salmon, E.D., Leslie, R.J., Saxton, W.M., Karrow, M.L., and McIntosh, J.R. (1984). Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J. Cell Biol. 99, 2165-2174.
37. Sampaio, P., Rebollo, E., Varmark, H., Sunkel, C.E., and Gonzalez, C. (2001). Organized microtubule arrays in gamma-tubulin-depleted Drosophila spermatocytes. Curr. Biol. 11, 1788-1793.
38. Saxton, W.M., Stemple, D.L., Leslie, R.J., Salmon, E.D., Zavortink, M., and McIntosh, J.R. (1984). Tubulin dynamics in cultured mammalian cells. J. Cell Biol. 99, 2175-2186.
39. Schuyler, S.C., and Pellman, D. (2001). Search, capture and signal: games microtubules and centrosomes play. J. Cell Sci. 114, 247-255.
40. Severin, F., Habermann, B., Huffaker, T., and Hyman, T. (2001). Stu2 promotes mitotic spindle elongation in anaphase. J. Cell Biol. 153, 435-442.
41. Sharp, D.J., Brown, H.M., Kwon, M., Rogers, G.C., Holland, G., and Scholey, J.M. (1999a). Functional coordination of three mitotic motors in Drosophila embryos. Mol. Biol. Cell 11, 241-253.
42. Sharp, D.J., McDonald, K.L., Brown, H.M., Matthies, H.J., Walczak, C., Vale, R.D., Mitchison, T.J., and Scholey, J.M. (1999b). The bipolar kinesin, KLP61F, cross-links microtubules within interpolar microtubule bundles of Drosophila embryonic mitotic spindles. J. Cell Biol. 144, 125-138.
43. Sharp, D.J., Yu, K.R., Sisson, J.C., Sullivan, W., and Scholey, J.M. (1999c). Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1, 51-54.
44. Sibon, O.C., Stevenson, V.A., and Theurkauf, W.E. (1997). DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388, 93-97.
45. Spradling, A.C., Stern, D., Kiss, I., Roote, J., Laverty, T., and Rubin, G.M. (1995). Gene disruptions using P transposable elements. Proc. Natl. Acad. Sci. USA 92, 10824-10830.
46. Stevenson, V.A., Kramer, J., Kuhn, J., and Theurkauf, W.E. (2001). Centrosomes and the Scrambled protein coordinate microtubule-independent actin reorganization. Nat. Cell Biol. 3, 68-75.
47. Straight, A.F., Sedat, J.W., and Murray, A.W. (1998). Time-lapse microscopy reveals unique roles for kinesins during anaphase in budding yeast. J. Cell Biol. 143, 687-694.
48. Tanaka, Y., Kanai, Y., Okada, Y., Nonaka, S., Takeda, S., Harada, A., and Hirokawa, N. (1998). Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93, 1147-1158.
49. Theurkauf, W.E., and Heck, M.M. (1999). Identification and characterization of mitotic mutations in Drosophila. Methods Cell Biol. 61, 317-346.
50. Verde, F., Dogterom, M., Stelzer, E., Karsenti, E., and Leibler, S. (1992). Control of microtubule dynamics and length by cyclin-A and cyclin-B dependent kinases in Xenopus egg extracts. J. Cell Biol. 118, 1097-1108.
51. Wakefield, J.G., Bonaccorsi, S., and Gatti, M. (2001). The Drosophila protein Asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell Biol. 153, 637-648.
52. Walczak, C.E., Gan, E.C., Desai, A., Mitchison, T.J., and Kline-Smith, S.L. (2002). The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly. Curr. Biol. 12, 1885-1889.
53. Walczak, C.E., Mitchison, T.J., and Desai, A. (1996). XKCM 1, A Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84, 37-47.
54. + are required for normal chromosome movement in mitosis. J. Cell Sci. 115, 931-940.
55. West, R.R., Malmstrom, T., Troxell, C.L., and McIntosh, J.R. (2001). Two related kinesins, klp5+ and klp6+, foster microtubule disassembly and are required for meiosis in fission yeast. Mol. Biol. Cell 12, 3919-32.