Opposing motor activities are required for the organization of the mammalian mitotic spindle pole

Journal of Cell Biology

Volumn 135, Issue 2, 1996, Pages 399-414

  Gaglio, Tirso ^a   Saredi, Alejandro ^a   Bingham, James B ^b   Hasbani, M Josh ^b   Gill, Steven R ^b   Schroer, Trina A ^b   Compton, Duane A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; NUCLEAR PROTEIN;

ANIMAL CELL; ARTICLE; CELL LINE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; HUMAN; HUMAN CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NUCLEAR; CELL LINE; CELL-FREE SYSTEM; CERCOPITHECUS AETHIOPS; CHICKENS; DYNEIN ATPASE; HELA CELLS; HUMANS; KINESIN; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; NUCLEOLUS ORGANIZER REGION; RECOMBINANT PROTEINS; XENOPUS PROTEINS;

ANIMALIA; ASTER; MAMMALIA;

EID: 0029862190     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.2.399     Document Type: Article

References (91)

1. Afshar, K., N.R. Barton, R.S. Hawley, and L.S.B. Goldstein. 1995. DNA binding and meiotic chromosomal localization of the Drosophila Nod kinesin-related protein. Cell. 81:129-138.
2. Ando, A., Y.Y. Kikuti, H. Kawata, N. Okamoto, T. Imai, T. Eki, K. Yokoyama, E. Soeda, T. Ikemura, K. Abe, and H. Inoko. 1994. Cloning of a new kinesin-related gene located at the centromeric end of the human MHC region. Immunogenetics. 39:194-200.
3. Barton, N.R., and L.S.B. Goldstein. 1996. Going mobile: microtubule motors and chromosome segregation. Proc. Natl. Acad. Sci. USA. 93:1735-1742.
4. Belmont, L.D., A.A. Hyman, K.E. Sawin, and T.J. Mitchison. 1990. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell. 62:579-589.
5. cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell. 83: 1159-1169.
6. Blose, S.H., D.I. Melzer, and J.R. Feramisco. 1984. 10-nm filaments are induced to collapse in living cells microinjected with a monoclonal and polyclonal antibodies against tubulin. J. Cell Biol. 98:847-858.
7. Burke, B., and L. Gerace. 1986. A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell. 44:639-652.
8. Capecchi, M.R. 1980. High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell. 22:479-488.
9. Clark, S.W., and D.I. Meyer. 1994. ACT3: a putative centractin homologue in S. cerevisiae is required for proper orientation of the mitotic spindle. J. Cell Biol. 127:129-138.
10. Cleveland, D.W. 1995. NuMA involvement in nuclear structure, spindle assembly, and nuclear reformation. Trends Cell Biol. 5:60-64.
11. Compton, D.A., and D.W. Cleveland. 1993. NuMA is required for the proper completion of mitosis. J. Cell Biol. 120:947-957.
12. Compton, D.A., and D.W. Cleveland. 1994. NuMA, a nuclear protein involved in mitosis and nuclear reformation. Curr. Opin. Cell Biol. 6:343-346.
13. cdc2 phosphorylation sites in NuMA impair the assembly of the mitotic spindle and block mitosis. J. Cell Sci. 108:621-633.
14. Compton, D.A., T.J. Yen, and D.W. Cleveland. 1991. Identification of novel centromere/kinetochore-associated proteins using monoclonal antibodies generated against human mitotic chromosome scaffolds. J. Cell Biol. 112: 1083-1097.
15. Compton, D.A., I. Szilak, and D.W. Cleveland. 1992. Primary structure of NuMA, an intranuclear protein that defines a novel pathway for the segregation of proteins at mitosis. J. Cell Biol. 116:1395-1408.
16. Coue, M., V.A. Lombillo, and J.R. McIntosh. 1991. Microtubule depolymerization promotes particle and chromosome movement in vitro. J. Cell Biol. 112: 1165-1175.
17. Desai, A., and T.J. Mitchison. 1995. A new role for motor proteins as couplers to depolymerizing microtubules. J. Cell Biol. 128:1-4.
18. Doxsey, S.J., P. Stein, L. Evans, P.D. Calarco, and M. Kirschner. 1994. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell. 76:639-650.
19. Earnshaw, W.C., and J.E. Tomkiel. 1992. Centromere and kinetochore structure. Curr. Opin. Cell Biol. 4:86-93.
20. Echeverri, C.J., B.M. Paschal, K.T. Vaughan, and R.B. Vallee. 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.
21. Endow, S.A. 1993. Chromosome distribution, molecular motors and the claret protein. Trends Genet. 9:52-55.
22. Endow, S.A., R. Chandra, D.J. Komma, A.H. Yamamoto, and E.D. Salmon. 1994. Mutants of the Drosophila ncd microtubule motor protein cause centrosomal and spindle pole defects in mitosis. J. Cell Sci. 107:859-867.
23. Fuller, M.T., and P.G. Wilson. 1992. Force and counterforce in the mitotic spindle. Cell. 71:547-550.
24. Gaglio, T., A. Saredi, and D.A. Compton. 1995. NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 131:693-708.
25. Gill, S.R., T.A. Schroer, I. Szilak, E.R. Steuer, M.P. Sheetz, and D.W. Cleveland. 1991. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115:1639-1650.
26. Hayden, J.H., S.S. Bowser, and C.L. Rieder. 1990. Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells. J. Cell Biol. 111:1039-1045.
27. Holy, T.E., and S. Leibler. 1994. Dynamic instability of microtubules as an efficient way to search in space. Proc. Natl. Acad. Sci. USA. 91:5682-5685.
28. Holzbaur, E.L.F., and R.B. Vallee. Dyneins: molecular structure and cellular function. Annu. Rev. Cell Biol. 10:339-372.
29. Hoyt, M.A. 1994. Cellular roles of kinesin and related proteins. Curr. Opin. Cell Biol. 6:63-68.
30. Hyman, A.A., and E. Karsenti. 1996. Morphogenetic properties of microtubules and mitotic spindle assembly. Cell. 84:401-410.
31. Hyman, A.A., and T.J. Mitchison. 1991. Two different microtubule-based motor activities with opposite polarities in kinetochores. Nature (Lond.). 351: 206-211.
32. Inoue, S., and E.D. Salmon. 1995. Force generation by microtubule assembly/ disassembly in mitosis and related movements. Mol. Biol. Cell. 6:1619-1640.
33. Kallajoki, M., K. Weber, and M. Osborn. 1991. A 210 kD nuclear matrix protein is a function part of the mitotic spindle: a microinjection study using SPN monoclonal antibodies. EMBO (Eur. Mol. Biol. Organ.) J. 10:3351-3362.
34. Kallajoki, M., K. Weber, and M. Osborn. 1992. Ability to organize microtubules in taxol-treated mitotic PtK2 cells goes with the SPN antigen and not with the centrosome. J. Cell Sci. 102:91-102.
35. Kallajoki, M., J. Harborth, K. Weber, and M. Osborn. 1993. Microinjection of a monoclonal antibody against SPN antigen, now identified by peptide sequences as the NuMA protein, induces micronuclei in PtK2 cells. J. Cell Sci. 104:139-150.
36. Karki, S., and E.L.F. Holzbaur. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806-28811.
37. Koshland, D.E., T.J. Mitchison, and M.W. Kirschner. 1988. Polewards chromosome movement driven by microtubule depolymerization in vitro. Nature (Lond.). 331:499-504.
38. Kuriyama, R., M. Kofron, R. Essner, T. Kato, S. Dragas-Granoic, C.K. Omoto, and A. Khodjakov. 1995. Characterization of a minus end-directed kinesin-related motor protein from cultured mammalian cells. J. Cell Biol. 129:1049-1059.
39. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly at the head of the bacteriophage T4. Nature (Lond.). 227:680-682.
40. Li, X., and R.B. Nicklas. 1995. Mitotic forces control a cell-cycle checkpoint. Nature (Lond). 373:630-632.
41. Lydersen, B.K., and D.E. Pettijohn. 1980. Human specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell. 22:489-499.
42. Maekawa, T., R. Leslie, and R. Kuriyama. 1991. Identification of a minus-end specific microtubule-associated protein located at the mitotic spindle poles in cultured mammalian cells. Eur. J. Cell Biol. 54:255-267.
43. Mastronarde, D.N., K.L. McDonald, R. Ding, and J.R. McIntosh. 1993. Interpolar spindle microtubules in PTK cells. J. Cell Biol. 123:1475-1489.
44. Matthies, H.J.G., H.B. McDonald, L.S.B. Goldstein, and W.E. Theurkauf. 1996. Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein. J. Cell Biol. 134:455-464.
45. McIntosh, J.R., and M.P. Koonce. 1989. Mitosis. Science (Wash. DC). 246:622-628.
46. McKim, K.S., and R.S. Hawley. 1995. Chromosomal control of meiotic cell division. Science (Wash. DC). 270:1595-1601.
47. Mitchison, T.J. 1989a. Mitosis: basic concepts. Curr. Opin. Cell Biol. 1:67-74.
48. Mitchison, T.J. 1989b. Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J. Cell Biol. 109:637-652.
49. Moore, J.D., and S.A. Endow. 1996. Kinesin proteins: a phylum of motors for microtubule-based motility. Bioessays. 18:207-219.
50. Muhua, L., T.S. Karpova, and J.A. Cooper. 1994. A yeast actin-related protein homologous to that found in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell. 19:255-262.
51. Murray, A.W. 1995. Tense spindle can relax. Nature (Lond.). 373:560-561.
52. Nicklas, R.B. 1989. The motor for poleward chromosome movement in anaphase is in or near the kinetochore. J. Cell Biol. 109:2245-2255.
53. Nicklas, R.B., G.M. Lee, C.L. Rieder, and G. Rupp. 1989. Mechanically cut mitotic spindles: clean cuts and stable microtubules. J. Cell Sci. 94:415-423.
54. Nicklas, R.B., S.C. Ward, and G.J. Gorbsky. 1995. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J. Cell Biol. 130:929-939.
55. Pfarr, C.M., M. Cove, P.M. Grissom, T.S. Hayes, M.E. Porter, and J.R. McIntosh. 1991. Cytoplasmic dynein is localized to kinetochores during mitosis. Nature (Lond.). 345:263-265.
56. Plamann, M., P.F. Minke, J.H. Tinsley, and K.S. Bruno. 1994. Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127:139-149.
57. Pluta, A.F., A.M. Makay, A.M. Ainsztein, I.G. Goldberg, and W.C. Earnshaw. 1995. The centromere: hub of chromosomal activities. Science (Wash. DC). 270:1591-1594.
58. Rieder, C.L. 1981. The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma (Berl.). 84:145-158.
59. Rieder, C.L. 1991. Mitosis: towards a molecular understanding of chromosome behavior. Curr. Opin. Cell Biol. 3:59-66.
60. Rieder, C.L., and E.D. Salmon. 1994. Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J. Cell Biol. 124:223-233.
61. Rieder, C.L., S.P. Alexander, and G. Rupp. 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.
62. Rieder, C.L., J.G. Ault, U. Eichenlaub-Ritter, and G. Sluder. 1993. Morphogenesis of the mitotic and meiotic spindle: conclusions obtained from one system are not necessarily applicable to the other. In Chromosome Segregation and Aneuploidy. B.K. Vig and A. Kappas, editors. Springer-Verlag, New York. 183-197.
63. Rieder, C.L., A. Schultz, R. Cole, and G. Sluder. 1994. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol. 127:1301-1310.
64. Saredi, A., L. Howard, and D.A. Compton. 1996. NuMA assembles into an extensive filamentous structure when expressed in the cell cytoplasm. J. Cell Sci. 109:619-630.
65. Saunders, W.S., and M.A. Hoyt. 1992. Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell. 70:451-458.
66. Saunders, W.S., D. Koshland, D. Eshe, 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.
67. Sawin, K.E., and T.J. Mitchison. 1991. Poleward microtubule flux in mitotic spindles assembled in vitro. J. Cell Biol. 112:941-954.
68. Sawin, K.E., K. LeGuellec, M. Philippe, and T.J. Mitchison. 1992a. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature (Lond.). 359:540-543.
69. Sawin, K.E., T.J. Mitchison, and L.G. Wordeman. 1992b. Evidence for kinesin-related proteins in the mitotic apparatus using peptide antibodies. J. Cell Sci. 101:303-313.
70. Schafer, D.A., S.R. Gill, J.A. Cooper, J.E. Heuser, and T.A. Schroer. 1994. Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J. Cell Biol. 126:403-412.
71. Schroer, T.A. 1994a. Structure, function and regulation of cytoplasmic dynein. Curr. Opin. Cell Biol. 6:69-73.
72. Schroer, T.A. 1994b. New insights into the interaction of cytoplasmic dynein with the actin-related protein, Arp1. J. Cell Biol. 127:1-4.
73. Schroer, T.A., and M.P. Sheetz. 1991. Two activators of microtubule-based vesicle transport. J. Cell Biol. 115:1309-1318.
74. Schroer, T.A., J.B. Bingham, and S.R. Gill. 1996. Actin related protein 1 and cytoplasmic dynein-based motility - what's the connection? Trends Cell Biol. 6:212-215.
75. Steuer, E.R., T.A. Schroer, L. Wordeman, and M.P. Sheetz. 1991. Cytoplasmic dynein localizes to mitotic spindles and kinetochores. Nature (Lond.). 345: 265-268.
76. Theurkauf, W.E., and R.S. Hawley. 1992. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-related protein. J. Cell Biol. 116:1167-1180.
77. Glued, the largest subunit of dynactin, is nonessential in Neurospora but required for nuclear distribution. Mol. Biol. Cell. 7:731-742.
78. Tousson, A., C. Zeng, B.R. Brinkley, and M.M. Valdivia. 1991. Centrophilin, a novel mitotic protein in the mammalian cell nucleus. J. Cell Biol. 112:427-440.
79. Vaisberg, E.A., M.P. Koonce, and J.R. McIntosh. 1993. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J. Cell Biol. 112:427-440.
80. Vaisberg, E.A., P.M. Grissom, and J.R. McIntosh. 1996. Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J. Cell Biol. 133:831-842.
81. Vallee, R.B., and M.P. Sheetz. 1996. Targeting of motor proteins. Science (Wash. DC). 271:1539-1544.
82. Glued. J. Cell Biol. 131:1507-1516.
83. Verde F., J.-M. Berrez, C. Antony, and E. Karsenti. 1991. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and ctyoplasmic dynein. J. Cell Biol. 112:1177-1187.
84. Vernos, I., and E. Karsenti. 1995. Chromosomes take the lead in spindle assembly. Trends Cell Biol. 5:297-301.
85. Vernos, I., J. Raats, T. Hirano, J. Heasman, E. Karsenti, and C. Wylie. 1995. Xklp1, a chromosomal Xenopus kinesin-related protein essential for spindle organization and chromosome positioning. Cell. 81:117-127.
86. Walczak, C.E., and T.J. Mitchison. 1996. Kinesin related proteins at mitotic spindle poles: function and regulation. Cell. 85:943-946.
87. Wang, S.-Z., and R. Adler. 1995. Chromokinesin: a DNA-binding, kinesin-related nuclear protein. J. Cell Biol. 128:761-768.
88. Glued component of the dynactin complex binds to both micotubules and the actin related protein centractin (Arp-1). Proc. Natl. Acad. Sci. USA. 92:1634-1638.
89. Waters, J.C., R.W. Cole, and C.L. Rieder. 1993. The force-producing mechanism for centrosome separation during spindle formation in vertebrates is intrinsic to each aster. J. Cell Biol. 122:361-372.
90. Yang, C.H., and M. Snyder. 1992. The nuclear-mitotic apparatus protein (NuMA) is important in the establishment and maintenance of the bipolar mitotic spindle apparatus. Mol. Biol. Cell. 3:1259-1267.
91. Yang, C.H., E.J. Lambie, and M. Snyder. 1992. NuMA: an unusually long coiled-coil related protein in the mammalian cell nucleus. J. Cell Biol. 116: 1303-1317.