Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Mar 5;93(5):1735–1742. doi: 10.1073/pnas.93.5.1735

Going mobile: microtubule motors and chromosome segregation.

N R Barton 1, L S Goldstein 1
PMCID: PMC39850  PMID: 8700828

Abstract

Proper chromosome segregation in eukaryotes depends upon the mitotic and meiotic spindles, which assemble at the time of cell division and then disassemble upon its completion. These spindles are composed in large part of microtubules, which either generate force by controlled polymerization and depolymerization or transduce force generated by molecular microtubule motors. In this review, we discuss recent insights into chromosome segregation mechanisms gained from the analyses of force generation during meiosis and mitosis. These analyses have demonstrated that members of the kinesin superfamily and the dynein family are essential in all organisms for proper chromosome and spindle behavior. It is also apparent that forces generated by microtubule polymerization and depolymerization are capable of generating forces sufficient for chromosome movement in vitro; whether they do so in vivo is as yet unclear. An important realization that has emerged is that some spindle activities can be accomplished by more than one motor so that functional redundancy is evident. In addition, some meiotic or mitotic movements apparently occur through the cooperative action of independent semiredundant processes. Finally, the molecular characterization of kinesin-related proteins has revealed that variations both in primary sequence and in associations with other proteins can produce motor complexes that may use a variety of mechanisms to transduce force in association with microtubules. Much remains to be learned about the regulation of these activities and the coordination of opposing and cooperative events involved in chromosome segregation; this set of problems represents one of the most important future frontiers of research.

Full text

PDF
1735

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Afshar K., Barton N. R., Hawley R. S., Goldstein L. S. DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell. 1995 Apr 7;81(1):129–138. doi: 10.1016/0092-8674(95)90377-1. [DOI] [PubMed] [Google Scholar]
  2. Aizawa H., Sekine Y., Takemura R., Zhang Z., Nangaku M., Hirokawa N. Kinesin family in murine central nervous system. J Cell Biol. 1992 Dec;119(5):1287–1296. doi: 10.1083/jcb.119.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Asai D. J., Beckwith S. M., Kandl K. A., Keating H. H., Tjandra H., Forney J. D. The dynein genes of Paramecium tetraurelia. Sequences adjacent to the catalytic P-loop identify cytoplasmic and axonemal heavy chain isoforms. J Cell Sci. 1994 Apr;107(Pt 4):839–847. doi: 10.1242/jcs.107.4.839. [DOI] [PubMed] [Google Scholar]
  4. Brown K. D., Coulson R. M., Yen T. J., Cleveland D. W. Cyclin-like accumulation and loss of the putative kinetochore motor CENP-E results from coupling continuous synthesis with specific degradation at the end of mitosis. J Cell Biol. 1994 Jun;125(6):1303–1312. doi: 10.1083/jcb.125.6.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown M., Garvik B., Hartwell L., Kadyk L., Seeley T., Weinert T. Fidelity of mitotic chromosome transmission. Cold Spring Harb Symp Quant Biol. 1991;56:359–365. doi: 10.1101/sqb.1991.056.01.043. [DOI] [PubMed] [Google Scholar]
  6. Campbell M. S., Gorbsky G. J. Microinjection of mitotic cells with the 3F3/2 anti-phosphoepitope antibody delays the onset of anaphase. J Cell Biol. 1995 Jun;129(5):1195–1204. doi: 10.1083/jcb.129.5.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carpenter A. T. A meiotic mutant defective in distributive disjunction in Drosophila melanogaster. Genetics. 1973 Mar;73(3):393–428. doi: 10.1093/genetics/73.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carpenter A. T. Chiasma function. Cell. 1994 Jul 1;77(7):957–962. doi: 10.1016/0092-8674(94)90434-0. [DOI] [PubMed] [Google Scholar]
  9. Carpenter A. T. Distributive segregation: motors in the polar wind? Cell. 1991 Mar 8;64(5):885–890. doi: 10.1016/0092-8674(91)90313-n. [DOI] [PubMed] [Google Scholar]
  10. Cassimeris L. U., Walker R. A., Pryer N. K., Salmon E. D. Dynamic instability of microtubules. Bioessays. 1987 Oct;7(4):149–154. doi: 10.1002/bies.950070403. [DOI] [PubMed] [Google Scholar]
  11. Cassimeris L., Rieder C. L., Salmon E. D. Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression. J Cell Sci. 1994 Jan;107(Pt 1):285–297. doi: 10.1242/jcs.107.1.285. [DOI] [PubMed] [Google Scholar]
  12. Chandra R., Salmon E. D., Erickson H. P., Lockhart A., Endow S. A. Structural and functional domains of the Drosophila ncd microtubule motor protein. J Biol Chem. 1993 Apr 25;268(12):9005–9013. [PubMed] [Google Scholar]
  13. Cole D. G., Cande W. Z., Baskin R. J., Skoufias D. A., Hogan C. J., Scholey J. M. Isolation of a sea urchin egg kinesin-related protein using peptide antibodies. J Cell Sci. 1992 Feb;101(Pt 2):291–301. doi: 10.1242/jcs.101.2.291. [DOI] [PubMed] [Google Scholar]
  14. Cole D. G., Chinn S. W., Wedaman K. P., Hall K., Vuong T., Scholey J. M. Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature. 1993 Nov 18;366(6452):268–270. doi: 10.1038/366268a0. [DOI] [PubMed] [Google Scholar]
  15. Cole D. G., Saxton W. M., Sheehan K. B., Scholey J. M. A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos. J Biol Chem. 1994 Sep 16;269(37):22913–22916. [PMC free article] [PubMed] [Google Scholar]
  16. Cole D. G., Scholey J. M. Structural variations among the kinesins. Trends Cell Biol. 1995 Jul;5(7):259–262. doi: 10.1016/s0962-8924(00)89028-5. [DOI] [PubMed] [Google Scholar]
  17. Coue M., Lombillo V. A., McIntosh J. R. Microtubule depolymerization promotes particle and chromosome movement in vitro. J Cell Biol. 1991 Mar;112(6):1165–1175. doi: 10.1083/jcb.112.6.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Davis D. G. Chromosome Behavior under the Influence of Claret-Nondisjunctional in DROSOPHILA MELANOGASTER. Genetics. 1969 Mar;61(3):577–594. doi: 10.1093/genetics/61.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Endow S. A., Chandra R., Komma D. J., Yamamoto A. H., Salmon E. D. Mutants of the Drosophila ncd microtubule motor protein cause centrosomal and spindle pole defects in mitosis. J Cell Sci. 1994 Apr;107(Pt 4):859–867. doi: 10.1242/jcs.107.4.859. [DOI] [PubMed] [Google Scholar]
  20. Endow S. A. Chromosome distribution, molecular motors and the claret protein. Trends Genet. 1993 Feb;9(2):52–55. doi: 10.1016/0168-9525(93)90187-M. [DOI] [PubMed] [Google Scholar]
  21. Endow S. A., Kang S. J., Satterwhite L. L., Rose M. D., Skeen V. P., Salmon E. D. Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J. 1994 Jun 1;13(11):2708–2713. doi: 10.1002/j.1460-2075.1994.tb06561.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Endow S. A., Titus M. A. Genetic approaches to molecular motors. Annu Rev Cell Biol. 1992;8:29–66. doi: 10.1146/annurev.cb.08.110192.000333. [DOI] [PubMed] [Google Scholar]
  23. Enos A. P., Morris N. R. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell. 1990 Mar 23;60(6):1019–1027. doi: 10.1016/0092-8674(90)90350-n. [DOI] [PubMed] [Google Scholar]
  24. Eshel D., Urrestarazu L. A., Vissers S., Jauniaux J. C., van Vliet-Reedijk J. C., Planta R. J., Gibbons I. R. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11172–11176. doi: 10.1073/pnas.90.23.11172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fuller M. T., Wilson P. G. Force and counterforce in the mitotic spindle. Cell. 1992 Nov 13;71(4):547–550. doi: 10.1016/0092-8674(92)90587-3. [DOI] [PubMed] [Google Scholar]
  26. Gibbons B. H., Asai D. J., Tang W. J., Hays T. S., Gibbons I. R. Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol Biol Cell. 1994 Jan;5(1):57–70. doi: 10.1091/mbc.5.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gibbons I. R. Dynein ATPases as microtubule motors. J Biol Chem. 1988 Nov 5;263(31):15837–15840. [PubMed] [Google Scholar]
  28. Gibbons I. R., Gibbons B. H., Mocz G., Asai D. J. Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain. Nature. 1991 Aug 15;352(6336):640–643. doi: 10.1038/352640a0. [DOI] [PubMed] [Google Scholar]
  29. Gibbons I. R., Rowe A. J. Dynein: A Protein with Adenosine Triphosphatase Activity from Cilia. Science. 1965 Jul 23;149(3682):424–426. doi: 10.1126/science.149.3682.424. [DOI] [PubMed] [Google Scholar]
  30. Goldstein L. S. The kinesin superfamily: tails of functional redundancy. Trends Cell Biol. 1991 Oct;1(4):93–98. doi: 10.1016/0962-8924(91)90036-9. [DOI] [PubMed] [Google Scholar]
  31. Goldstein L. S., Vale R. D. Motor proteins. A brave new world for dynein. Nature. 1991 Aug 15;352(6336):569–570. doi: 10.1038/352569a0. [DOI] [PubMed] [Google Scholar]
  32. Goldstein L. S. With apologies to scheherazade: tails of 1001 kinesin motors. Annu Rev Genet. 1993;27:319–351. doi: 10.1146/annurev.ge.27.120193.001535. [DOI] [PubMed] [Google Scholar]
  33. Gorbsky G. J. Kinetochores, microtubules and the metaphase checkpoint. Trends Cell Biol. 1995 Apr;5(4):143–148. doi: 10.1016/s0962-8924(00)88968-0. [DOI] [PubMed] [Google Scholar]
  34. Hagan I., Yanagida M. Kinesin-related cut7 protein associates with mitotic and meiotic spindles in fission yeast. Nature. 1992 Mar 5;356(6364):74–76. doi: 10.1038/356074a0. [DOI] [PubMed] [Google Scholar]
  35. Hagan I., Yanagida M. Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature. 1990 Oct 11;347(6293):563–566. doi: 10.1038/347563a0. [DOI] [PubMed] [Google Scholar]
  36. Hatsumi M., Endow S. A. Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis. J Cell Sci. 1992 Mar;101(Pt 3):547–559. doi: 10.1242/jcs.101.3.547. [DOI] [PubMed] [Google Scholar]
  37. Heck M. M., Pereira A., Pesavento P., Yannoni Y., Spradling A. C., Goldstein L. S. The kinesin-like protein KLP61F is essential for mitosis in Drosophila. J Cell Biol. 1993 Nov;123(3):665–679. doi: 10.1083/jcb.123.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hogan C. J., Wein H., Wordeman L., Scholey J. M., Sawin K. E., Cande W. Z. Inhibition of anaphase spindle elongation in vitro by a peptide antibody that recognizes kinesin motor domain. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6611–6615. doi: 10.1073/pnas.90.14.6611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Houliston E., Le Guellec R., Kress M., Philippe M., Le Guellec K. The kinesin-related protein Eg5 associates with both interphase and spindle microtubules during Xenopus early development. Dev Biol. 1994 Jul;164(1):147–159. doi: 10.1006/dbio.1994.1187. [DOI] [PubMed] [Google Scholar]
  40. Hoyt M. A. Cellular roles of kinesin and related proteins. Curr Opin Cell Biol. 1994 Feb;6(1):63–68. doi: 10.1016/0955-0674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  41. Hoyt M. A., He L., Loo K. K., Saunders W. S. Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol. 1992 Jul;118(1):109–120. doi: 10.1083/jcb.118.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Hoyt M. A., He L., Totis L., Saunders W. S. Loss of function of Saccharomyces cerevisiae kinesin-related CIN8 and KIP1 is suppressed by KAR3 motor domain mutations. Genetics. 1993 Sep;135(1):35–44. doi: 10.1093/genetics/135.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Hyman A. A., Middleton K., Centola M., Mitchison T. J., Carbon J. Microtubule-motor activity of a yeast centromere-binding protein complex. Nature. 1992 Oct 8;359(6395):533–536. doi: 10.1038/359533a0. [DOI] [PubMed] [Google Scholar]
  44. Inoué S., Sato H. Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J Gen Physiol. 1967 Jul;50(6 Suppl):259–292. [PMC free article] [PubMed] [Google Scholar]
  45. Jang J. K., Messina L., Erdman M. B., Arbel T., Hawley R. S. Induction of metaphase arrest in Drosophila oocytes by chiasma-based kinetochore tension. Science. 1995 Jun 30;268(5219):1917–1919. doi: 10.1126/science.7604267. [DOI] [PubMed] [Google Scholar]
  46. Karsenti E. Mitotic spindle morphogenesis in animal cells. Semin Cell Biol. 1991 Aug;2(4):251–260. [PubMed] [Google Scholar]
  47. Kilmartin J. V. Genetic and biochemical approaches to spindle function and chromosome segregation in eukaryotic microorganisms. Curr Opin Cell Biol. 1994 Feb;6(1):50–54. doi: 10.1016/0955-0674(94)90115-5. [DOI] [PubMed] [Google Scholar]
  48. Kondo S., Sato-Yoshitake R., Noda Y., Aizawa H., Nakata T., Matsuura Y., Hirokawa N. KIF3A is a new microtubule-based anterograde motor in the nerve axon. J Cell Biol. 1994 Jun;125(5):1095–1107. doi: 10.1083/jcb.125.5.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Koonce M. P., Grissom P. M., McIntosh J. R. Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein. J Cell Biol. 1992 Dec;119(6):1597–1604. doi: 10.1083/jcb.119.6.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Koshland D. E., Mitchison T. J., Kirschner M. W. Polewards chromosome movement driven by microtubule depolymerization in vitro. Nature. 1988 Feb 11;331(6156):499–504. doi: 10.1038/331499a0. [DOI] [PubMed] [Google Scholar]
  51. Kuriyama R., Kofron M., Essner R., Kato T., Dragas-Granoic S., Omoto C. K., Khodjakov A. Characterization of a minus end-directed kinesin-like motor protein from cultured mammalian cells. J Cell Biol. 1995 May;129(4):1049–1059. doi: 10.1083/jcb.129.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Li M., McGrail M., Serr M., Hays T. S. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J Cell Biol. 1994 Sep;126(6):1475–1494. doi: 10.1083/jcb.126.6.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Li X., Nicklas R. B. Mitotic forces control a cell-cycle checkpoint. Nature. 1995 Feb 16;373(6515):630–632. doi: 10.1038/373630a0. [DOI] [PubMed] [Google Scholar]
  54. Li Y. Y., Yeh E., Hays T., Bloom K. Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10096–10100. doi: 10.1073/pnas.90.21.10096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Liao H., Li G., Yen T. J. Mitotic regulation of microtubule cross-linking activity of CENP-E kinetochore protein. Science. 1994 Jul 15;265(5170):394–398. doi: 10.1126/science.8023161. [DOI] [PubMed] [Google Scholar]
  56. Lombillo V. A., Nislow C., Yen T. J., Gelfand V. I., McIntosh J. R. Antibodies to the kinesin motor domain and CENP-E inhibit microtubule depolymerization-dependent motion of chromosomes in vitro. J Cell Biol. 1995 Jan;128(1-2):107–115. doi: 10.1083/jcb.128.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Lye R. J., Porter M. E., Scholey J. M., McIntosh J. R. Identification of a microtubule-based cytoplasmic motor in the nematode C. elegans. Cell. 1987 Oct 23;51(2):309–318. doi: 10.1016/0092-8674(87)90157-7. [DOI] [PubMed] [Google Scholar]
  58. McDonald H. B., Stewart R. J., Goldstein L. S. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor. Cell. 1990 Dec 21;63(6):1159–1165. doi: 10.1016/0092-8674(90)90412-8. [DOI] [PubMed] [Google Scholar]
  59. McIntosh J. R., Pfarr C. M. Mitotic motors. J Cell Biol. 1991 Nov;115(3):577–585. doi: 10.1083/jcb.115.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Meluh P. B., Rose M. D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell. 1990 Mar 23;60(6):1029–1041. doi: 10.1016/0092-8674(90)90351-e. [DOI] [PubMed] [Google Scholar]
  61. Middleton K., Carbon J. KAR3-encoded kinesin is a minus-end-directed motor that functions with centromere binding proteins (CBF3) on an in vitro yeast kinetochore. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7212–7216. doi: 10.1073/pnas.91.15.7212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Mikami A., Paschal B. M., Mazumdar M., Vallee R. B. Molecular cloning of the retrograde transport motor cytoplasmic dynein (MAP 1C). Neuron. 1993 May;10(5):787–796. doi: 10.1016/0896-6273(93)90195-w. [DOI] [PubMed] [Google Scholar]
  63. Mitsui H., Yamaguchi-Shinozaki K., Shinozaki K., Nishikawa K., Takahashi H. Identification of a gene family (kat) encoding kinesin-like proteins in Arabidopsis thaliana and the characterization of secondary structure of KatA. Mol Gen Genet. 1993 Apr;238(3):362–368. doi: 10.1007/BF00291995. [DOI] [PubMed] [Google Scholar]
  64. Murray A. W. Cell cycle. Tense spindles can relax. Nature. 1995 Feb 16;373(6515):560–561. doi: 10.1038/373560a0. [DOI] [PubMed] [Google Scholar]
  65. Nicklas R. B. The forces that move chromosomes in mitosis. Annu Rev Biophys Biophys Chem. 1988;17:431–449. doi: 10.1146/annurev.bb.17.060188.002243. [DOI] [PubMed] [Google Scholar]
  66. Nicklas R. B., Ward S. C. Elements of error correction in mitosis: microtubule capture, release, and tension. J Cell Biol. 1994 Sep;126(5):1241–1253. doi: 10.1083/jcb.126.5.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Nislow C., Lombillo V. A., Kuriyama R., McIntosh J. R. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature. 1992 Oct 8;359(6395):543–547. doi: 10.1038/359543a0. [DOI] [PubMed] [Google Scholar]
  68. Nislow C., Sellitto C., Kuriyama R., McIntosh J. R. A monoclonal antibody to a mitotic microtubule-associated protein blocks mitotic progression. J Cell Biol. 1990 Aug;111(2):511–522. doi: 10.1083/jcb.111.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Noda Y., Sato-Yoshitake R., Kondo S., Nangaku M., Hirokawa N. KIF2 is a new microtubule-based anterograde motor that transports membranous organelles distinct from those carried by kinesin heavy chain or KIF3A/B. J Cell Biol. 1995 Apr;129(1):157–167. doi: 10.1083/jcb.129.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. O'Connell M. J., Meluh P. B., Rose M. D., Morris N. R. Suppression of the bimC4 mitotic spindle defect by deletion of klpA, a gene encoding a KAR3-related kinesin-like protein in Aspergillus nidulans. J Cell Biol. 1993 Jan;120(1):153–162. doi: 10.1083/jcb.120.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Ogawa K. Four ATP-binding sites in the midregion of the beta heavy chain of dynein. Nature. 1991 Aug 15;352(6336):643–645. doi: 10.1038/352643a0. [DOI] [PubMed] [Google Scholar]
  72. Paschal B. M., Shpetner H. S., Vallee R. B. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol. 1987 Sep;105(3):1273–1282. doi: 10.1083/jcb.105.3.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Paschal B. M., Vallee R. B. Retrograde transport by the microtubule-associated protein MAP 1C. Nature. 1987 Nov 12;330(6144):181–183. doi: 10.1038/330181a0. [DOI] [PubMed] [Google Scholar]
  74. Pesavento P. A., Stewart R. J., Goldstein L. S. Characterization of the KLP68D kinesin-like protein in Drosophila: possible roles in axonal transport. J Cell Biol. 1994 Nov;127(4):1041–1048. doi: 10.1083/jcb.127.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Pfarr C. M., Coue M., Grissom P. M., Hays T. S., Porter M. E., McIntosh J. R. Cytoplasmic dynein is localized to kinetochores during mitosis. Nature. 1990 May 17;345(6272):263–265. doi: 10.1038/345263a0. [DOI] [PubMed] [Google Scholar]
  76. Plamann M., Minke P. F., Tinsley J. H., Bruno K. S. Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J Cell Biol. 1994 Oct;127(1):139–149. doi: 10.1083/jcb.127.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Rashid D. J., Wedaman K. P., Scholey J. M. Heterodimerization of the two motor subunits of the heterotrimeric kinesin, KRP85/95. J Mol Biol. 1995 Sep 15;252(2):157–162. doi: 10.1006/jmbi.1995.0484. [DOI] [PubMed] [Google Scholar]
  78. Rasmusson K., Serr M., Gepner J., Gibbons I., Hays T. S. A family of dynein genes in Drosophila melanogaster. Mol Biol Cell. 1994 Jan;5(1):45–55. doi: 10.1091/mbc.5.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Rieder C. L., Salmon E. D. Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J Cell Biol. 1994 Feb;124(3):223–233. doi: 10.1083/jcb.124.3.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Rodionov V. I., Gelfand V. I., Borisy G. G. Kinesin-like molecules involved in spindle formation. J Cell Sci. 1993 Dec;106(Pt 4):1179–1188. doi: 10.1242/jcs.106.4.1179. [DOI] [PubMed] [Google Scholar]
  81. Roof D. M., Meluh P. B., Rose M. D. Kinesin-related proteins required for assembly of the mitotic spindle. J Cell Biol. 1992 Jul;118(1):95–108. doi: 10.1083/jcb.118.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Roof D. M., Meluh P. B., Rose M. D. Multiple kinesin-related proteins in yeast mitosis. Cold Spring Harb Symp Quant Biol. 1991;56:693–703. doi: 10.1101/sqb.1991.056.01.078. [DOI] [PubMed] [Google Scholar]
  83. Saunders W. S., Hoyt M. A. Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell. 1992 Aug 7;70(3):451–458. doi: 10.1016/0092-8674(92)90169-d. [DOI] [PubMed] [Google Scholar]
  84. Saunders W. S., Koshland D., Eshel D., Gibbons I. R., Hoyt M. A. Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J Cell Biol. 1995 Feb;128(4):617–624. doi: 10.1083/jcb.128.4.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Saunders W. S. Mitotic spindle pole separation. Trends Cell Biol. 1993 Dec;3(12):432–437. doi: 10.1016/0962-8924(93)90032-v. [DOI] [PubMed] [Google Scholar]
  86. Sawin K. E., Endow S. A. Meiosis, mitosis and microtubule motors. Bioessays. 1993 Jun;15(6):399–407. doi: 10.1002/bies.950150606. [DOI] [PubMed] [Google Scholar]
  87. Sawin K. E., LeGuellec K., Philippe M., Mitchison T. J. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature. 1992 Oct 8;359(6395):540–543. doi: 10.1038/359540a0. [DOI] [PubMed] [Google Scholar]
  88. Sawin K. E., Mitchison T. J. Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4289–4293. doi: 10.1073/pnas.92.10.4289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Sawin K. E., Mitchison T. J., Wordeman L. G. Evidence for kinesin-related proteins in the mitotic apparatus using peptide antibodies. J Cell Sci. 1992 Feb;101(Pt 2):303–313. doi: 10.1242/jcs.101.2.303. [DOI] [PubMed] [Google Scholar]
  90. Sawin K. E., Scholey J. M. Motor proteins in cell division. Trends Cell Biol. 1991 Nov;1(5):122–129. doi: 10.1016/0962-8924(91)90117-r. [DOI] [PubMed] [Google Scholar]
  91. Saxton W. M., Hicks J., Goldstein L. S., Raff E. C. Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell. 1991 Mar 22;64(6):1093–1102. doi: 10.1016/0092-8674(91)90264-y. [DOI] [PubMed] [Google Scholar]
  92. Schroer T. A. New insights into the interaction of cytoplasmic dynein with the actin-related protein, Arp1. J Cell Biol. 1994 Oct;127(1):1–4. doi: 10.1083/jcb.127.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Schroer T. A. Structure, function and regulation of cytoplasmic dynein. Curr Opin Cell Biol. 1994 Feb;6(1):69–73. doi: 10.1016/0955-0674(94)90118-x. [DOI] [PubMed] [Google Scholar]
  94. Sekine Y., Okada Y., Noda Y., Kondo S., Aizawa H., Takemura R., Hirokawa N. A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J Cell Biol. 1994 Oct;127(1):187–201. doi: 10.1083/jcb.127.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Sellitto C., Kuriyama R. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells. J Cell Biol. 1988 Feb;106(2):431–439. doi: 10.1083/jcb.106.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Shakir M. A., Fukushige T., Yasuda H., Miwa J., Siddiqui S. S. C. elegans osm-3 gene mediating osmotic avoidance behaviour encodes a kinesin-like protein. Neuroreport. 1993 Jul;4(7):891–894. doi: 10.1097/00001756-199307000-00013. [DOI] [PubMed] [Google Scholar]
  97. Shimizu T., Furusawa K., Ohashi S., Toyoshima Y. Y., Okuno M., Malik F., Vale R. D. Nucleotide specificity of the enzymatic and motile activities of dynein, kinesin, and heavy meromyosin. J Cell Biol. 1991 Mar;112(6):1189–1197. doi: 10.1083/jcb.112.6.1189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Steuer E. R., Wordeman L., Schroer T. A., Sheetz M. P. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature. 1990 May 17;345(6272):266–268. doi: 10.1038/345266a0. [DOI] [PubMed] [Google Scholar]
  99. Tabish M., Siddiqui Z. K., Nishikawa K., Siddiqui S. S. Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J Mol Biol. 1995 Mar 31;247(3):377–389. doi: 10.1006/jmbi.1994.0146. [DOI] [PubMed] [Google Scholar]
  100. Theurkauf W. E., Hawley R. S. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol. 1992 Mar;116(5):1167–1180. doi: 10.1083/jcb.116.5.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Thrower D. A., Jordan M. A., Schaar B. T., Yen T. J., Wilson L. Mitotic HeLa cells contain a CENP-E-associated minus end-directed microtubule motor. EMBO J. 1995 Mar 1;14(5):918–926. doi: 10.1002/j.1460-2075.1995.tb07073.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Vaisberg E. A., Koonce M. P., McIntosh J. R. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J Cell Biol. 1993 Nov;123(4):849–858. doi: 10.1083/jcb.123.4.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Vale R. D., Goldstein L. S. One motor, many tails: an expanding repertoire of force-generating enzymes. Cell. 1990 Mar 23;60(6):883–885. doi: 10.1016/0092-8674(90)90334-b. [DOI] [PubMed] [Google Scholar]
  104. Vale R. D. Microtubule motors: many new models off the assembly line. Trends Biochem Sci. 1992 Aug;17(8):300–304. doi: 10.1016/0968-0004(92)90440-k. [DOI] [PubMed] [Google Scholar]
  105. Vale R. D., Reese T. S., Sheetz M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 1985 Aug;42(1):39–50. doi: 10.1016/s0092-8674(85)80099-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Vallee R. Chromosome kinetics. Movement on two fronts. Nature. 1991 May 16;351(6323):187–188. doi: 10.1038/351187a0. [DOI] [PubMed] [Google Scholar]
  107. Vallee R. Cytoplasmic dynein: advances in microtubule-based motility. Trends Cell Biol. 1991 Jul;1(1):25–29. doi: 10.1016/0962-8924(91)90066-i. [DOI] [PubMed] [Google Scholar]
  108. Vallee R. Mitosis: dynein and the kinetochore. Nature. 1990 May 17;345(6272):206–207. doi: 10.1038/345206a0. [DOI] [PubMed] [Google Scholar]
  109. Verde F., Berrez J. M., Antony C., Karsenti E. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J Cell Biol. 1991 Mar;112(6):1177–1187. doi: 10.1083/jcb.112.6.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Vernos I., Karsenti E. Chromosomes take the lead in spindle assembly. Trends Cell Biol. 1995 Aug;5(8):297–301. doi: 10.1016/s0962-8924(00)89045-5. [DOI] [PubMed] [Google Scholar]
  111. Vernos I., Raats J., Hirano T., Heasman J., Karsenti E., Wylie C. Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning. Cell. 1995 Apr 7;81(1):117–127. doi: 10.1016/0092-8674(95)90376-3. [DOI] [PubMed] [Google Scholar]
  112. Wadsworth P. Mitosis: spindle assembly and chromosome motion. Curr Opin Cell Biol. 1993 Feb;5(1):123–128. doi: 10.1016/s0955-0674(05)80017-1. [DOI] [PubMed] [Google Scholar]
  113. Wald H. Cytologic Studies on the Abnormal Development of the Eggs of the Claret Mutant Type of Drosophila Simulans. Genetics. 1936 May;21(3):264–281. doi: 10.1093/genetics/21.3.264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Walker R. A., Salmon E. D., Endow S. A. The Drosophila claret segregation protein is a minus-end directed motor molecule. Nature. 1990 Oct 25;347(6295):780–782. doi: 10.1038/347780a0. [DOI] [PubMed] [Google Scholar]
  115. Walker R. A., Sheetz M. P. Cytoplasmic microtubule-associated motors. Annu Rev Biochem. 1993;62:429–451. doi: 10.1146/annurev.bi.62.070193.002241. [DOI] [PubMed] [Google Scholar]
  116. Walther Z., Vashishtha M., Hall J. L. The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J Cell Biol. 1994 Jul;126(1):175–188. doi: 10.1083/jcb.126.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Wang S. Z., Adler R. Chromokinesin: a DNA-binding, kinesin-like nuclear protein. J Cell Biol. 1995 Mar;128(5):761–768. doi: 10.1083/jcb.128.5.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Williams B. C., Riedy M. F., Williams E. V., Gatti M., Goldberg M. L. The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis. J Cell Biol. 1995 May;129(3):709–723. doi: 10.1083/jcb.129.3.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Wordeman L., Mitchison T. J. Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis. J Cell Biol. 1995 Jan;128(1-2):95–104. doi: 10.1083/jcb.128.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Wright B. D., Terasaki M., Scholey J. M. Roles of kinesin and kinesin-like proteins in sea urchin embryonic cell division: evaluation using antibody microinjection. J Cell Biol. 1993 Nov;123(3):681–689. doi: 10.1083/jcb.123.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Xiang X., Beckwith S. M., Morris N. R. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2100–2104. doi: 10.1073/pnas.91.6.2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Yamazaki H., Nakata T., Okada Y., Hirokawa N. KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J Cell Biol. 1995 Sep;130(6):1387–1399. doi: 10.1083/jcb.130.6.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Yang J. T., Saxton W. M., Stewart R. J., Raff E. C., Goldstein L. S. Evidence that the head of kinesin is sufficient for force generation and motility in vitro. Science. 1990 Jul 6;249(4964):42–47. doi: 10.1126/science.2142332. [DOI] [PubMed] [Google Scholar]
  124. Yeh E., Skibbens R. V., Cheng J. W., Salmon E. D., Bloom K. Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae. J Cell Biol. 1995 Aug;130(3):687–700. doi: 10.1083/jcb.130.3.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Yen T. J., Compton D. A., Wise D., Zinkowski R. P., Brinkley B. R., Earnshaw W. C., Cleveland D. W. CENP-E, a novel human centromere-associated protein required for progression from metaphase to anaphase. EMBO J. 1991 May;10(5):1245–1254. doi: 10.1002/j.1460-2075.1991.tb08066.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Yen T. J., Li G., Schaar B. T., Szilak I., Cleveland D. W. CENP-E is a putative kinetochore motor that accumulates just before mitosis. Nature. 1992 Oct 8;359(6395):536–539. doi: 10.1038/359536a0. [DOI] [PubMed] [Google Scholar]
  127. Zhang P., Hawley R. S. The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the nod locus. Genetics. 1990 May;125(1):115–127. doi: 10.1093/genetics/125.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Zhang P., Knowles B. A., Goldstein L. S., Hawley R. S. A kinesin-like protein required for distributive chromosome segregation in Drosophila. Cell. 1990 Sep 21;62(6):1053–1062. doi: 10.1016/0092-8674(90)90383-p. [DOI] [PubMed] [Google Scholar]
  129. Zhang Z., Tanaka Y., Nonaka S., Aizawa H., Kawasaki H., Nakata T., Hirokawa N. The primary structure of rat brain (cytoplasmic) dynein heavy chain, a cytoplasmic motor enzyme. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7928–7932. doi: 10.1073/pnas.90.17.7928. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES