Published 17 September 2001. doi:10.1083/jcb.200106093
© The Rockefeller University Press,
0021-9525/2001/9/1135 $5.00
The Journal of Cell Biology, Volume 154, Number 6, September 17, 2001 1135-1146
The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles
Aime A. Levesque and
Duane A. Compton
Department of Biochemistry, Dartmouth Medical School, Hanover, NH 03755
Address correspondence to Duane A. Compton, Department of Biochemistry, Dartmouth Medical School, 7200 Vail, Room 411, Hanover, NH 03755. Tel.: (603) 650-1990. Fax: (603) 650-1128. E-mail: duane.a.compton{at}dartmouth.edu
Chromokinesins have been postulated to provide the polar ejection force needed for chromosome congression during mitosis. We have evaluated that possibility by monitoring chromosome movement in vertebrate-cultured cells using time-lapse differential interference contrast microscopy after microinjection with antibodies specific for the chromokinesin Kid. 17.5% of cells injected with Kid-specific antibodies have one or more chromosomes that remain closely opposed to a spindle pole and fail to enter anaphase. In contrast, 82.5% of injected cells align chromosomes in metaphase, progress to anaphase, and display chromosome velocities not significantly different from control cells. However, injected cells lack chromosome oscillations, and chromosome orientation is atypical because chromosome arms extend toward spindle poles during both congression and metaphase. Furthermore, chromosomes cluster into a mass and fail to oscillate when Kid is perturbed in cells containing monopolar spindles. These data indicate that Kid generates the polar ejection force that pushes chromosome arms away from spindle poles in vertebrate-cultured cells. This force increases the efficiency with which chromosomes make bipolar spindle attachments and regulates kinetochore activities necessary for chromosome oscillation, but is not essential for chromosome congression.
Key Words: chromosome; kinetochore; mitotic spindle; Kid; kinesin

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
Related Article
-
Mitosis without wind
- William A. Wells
J. Cell Biol. 2001 154: 1099.
[Full Text]
[PDF]
This article has been cited by other articles:
-
Paul, R., Wollman, R., Silkworth, W. T., Nardi, I. K., Cimini, D., Mogilner, A.
(2009). Computer simulations predict that chromosome movements and rotations accelerate mitotic spindle assembly without compromising accuracy. Proc. Natl. Acad. Sci. USA
106: 15708-15713
[Abstract]
[Full Text]
-
Maddika, S., Sy, S. M.-H., Chen, J.
(2009). Functional Interaction between Chfr and Kif22 Controls Genomic Stability. J. Biol. Chem.
284: 12998-13003
[Abstract]
[Full Text]
-
Marrocco, K., Thomann, A., Parmentier, Y., Genschik, P., Criqui, M. C.
(2009). The APC/C E3 ligase remains active in most post-mitotic Arabidopsis cells and is required for proper vasculature development and organization. Development
136: 1475-1485
[Abstract]
[Full Text]
-
Liu, J., Desai, A., Onuchic, J. N., Hwa, T.
(2008). An integrated mechanobiochemical feedback mechanism describes chromosome motility from prometaphase to anaphase in mitosis. Proc. Natl. Acad. Sci. USA
105: 13752-13757
[Abstract]
[Full Text]
-
Laan, L., Husson, J., Munteanu, E. L., Kerssemakers, J. W. J., Dogterom, M.
(2008). Force-generation and dynamic instability of microtubule bundles. Proc. Natl. Acad. Sci. USA
105: 8920-8925
[Abstract]
[Full Text]
-
Tahara, K., Takagi, M., Ohsugi, M., Sone, T., Nishiumi, F., Maeshima, K., Horiuchi, Y., Tokai-Nishizumi, N., Imamoto, F., Yamamoto, T., Kose, S., Imamoto, N.
(2008). Importin-{beta} and the small guanosine triphosphatase Ran mediate chromosome loading of the human chromokinesin Kid. JCB
180: 493-506
[Abstract]
[Full Text]
-
Liu, J., Desai, A., Onuchic, J. N., Hwa, T.
(2007). A mechanobiochemical mechanism for monooriented chromosome oscillation in mitosis. Proc. Natl. Acad. Sci. USA
104: 16104-16109
[Abstract]
[Full Text]
-
Manning, A. L., Ganem, N. J., Bakhoum, S. F., Wagenbach, M., Wordeman, L., Compton, D. A.
(2007). The Kinesin-13 Proteins Kif2a, Kif2b, and Kif2c/MCAK Have Distinct Roles during Mitosis in Human Cells. Mol. Biol. Cell
18: 2970-2979
[Abstract]
[Full Text]
-
Tsuduki, T., Nakano, M., Yasuoka, N., Yamazaki, S., Okada, T., Okamoto, Y., Masumoto, H.
(2006). An Artificially Constructed De Novo Human Chromosome Behaves Almost Identically to Its Natural Counterpart during Metaphase and Anaphase in Living Cells.. Mol. Cell. Biol.
26: 7682-7695
[Abstract]
[Full Text]
-
Haraguchi, K., Hayashi, T., Jimbo, T., Yamamoto, T., Akiyama, T.
(2006). Role of the Kinesin-2 Family Protein, KIF3, during Mitosis. J. Biol. Chem.
281: 4094-4099
[Abstract]
[Full Text]
-
Brunet, S., Maro, B.
(2005). Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction
130: 801-811
[Abstract]
[Full Text]
-
Cui, W., Hawley, R. S.
(2005). The HhH(2)/NDD Domain of the Drosophila Nod Chromokinesin-like Protein Is Required for Binding to Chromosomes in the Oocyte Nucleus. Genetics
171: 1823-1835
[Abstract]
[Full Text]
-
Tokai-Nishizumi, N., Ohsugi, M., Suzuki, E., Yamamoto, T.
(2005). The Chromokinesin Kid Is Required for Maintenance of Proper Metaphase Spindle Size. Mol. Biol. Cell
16: 5455-5463
[Abstract]
[Full Text]
-
Brouhard, G. J., Hunt, A. J.
(2005). Microtubule movements on the arms of mitotic chromosomes: Polar ejection forces quantified in vitro. Proc. Natl. Acad. Sci. USA
102: 13903-13908
[Abstract]
[Full Text]
-
Zhu, C., Zhao, J., Bibikova, M., Leverson, J. D., Bossy-Wetzel, E., Fan, J.-B., Abraham, R. T., Jiang, W.
(2005). Functional Analysis of Human Microtubule-based Motor Proteins, the Kinesins and Dyneins, in Mitosis/Cytokinesis Using RNA Interference. Mol. Biol. Cell
16: 3187-3199
[Abstract]
[Full Text]
-
Salmon, E.D, Cimini, D, Cameron, L.A, DeLuca, J.G
(2005). Merotelic kinetochores in mammalian tissue cells. Phil Trans R Soc B
360: 553-568
[Abstract]
[Full Text]
-
Rogers, G. C., Rogers, S. L., Sharp, D. J.
(2005). Spindle microtubules in flux. J. Cell Sci.
118: 1105-1116
[Abstract]
[Full Text]
-
LaFountain, J. R. Jr., Oldenbourg, R.
(2004). Maloriented Bivalents Have Metaphase Positions at the Spindle Equator with More Kinetochore Microtubules to One Pole than to the Other. Mol. Biol. Cell
15: 5346-5355
[Abstract]
[Full Text]
-
Gruss, O. J., Vernos, I.
(2004). The mechanism of spindle assembly: functions of Ran and its target TPX2. JCB
166: 949-955
[Abstract]
[Full Text]
-
Powers, J., Rose, D. J., Saunders, A., Dunkelbarger, S., Strome, S., Saxton, W. M.
(2004). Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. JCB
166: 991-1001
[Abstract]
[Full Text]
-
DeBonis, S., Skoufias, D. A., Lebeau, L., Lopez, R., Robin, G., Margolis, R. L., Wade, R. H., Kozielski, F.
(2004). In vitro screening for inhibitors of the human mitotic kinesin Eg5 with antimitotic and antitumor activities. Molecular Cancer Therapeutics
3: 1079-1090
[Abstract]
[Full Text]
-
Mazumdar, M., Sundareshan, S., Misteli, T.
(2004). Human chromokinesin KIF4A functions in chromosome condensation and segregation. JCB
166: 613-620
[Abstract]
[Full Text]
-
Ganem, N. J., Compton, D. A.
(2004). The KinI kinesin Kif2a is required for bipolar spindle assembly through a functional relationship with MCAK. JCB
166: 473-478
[Abstract]
[Full Text]
-
Ono, T., Fang, Y., Spector, D. L., Hirano, T.
(2004). Spatial and Temporal Regulation of Condensins I and II in Mitotic Chromosome Assembly in Human Cells. Mol. Biol. Cell
15: 3296-3308
[Abstract]
[Full Text]
-
Chakravarty, A., Howard, L., Compton, D. A.
(2004). A Mechanistic Model for the Organization of Microtubule Asters by Motor and Non-Motor Proteins in a Mammalian Mitotic Extract. Mol. Biol. Cell
15: 2116-2132
[Abstract]
[Full Text]
-
Honda, S., Marumoto, T., Hirota, T., Nitta, M., Arima, Y., Ogawa, M., Saya, H.
(2004). Activation of m-Calpain Is Required for Chromosome Alignment on the Metaphase Plate during Mitosis. J. Biol. Chem.
279: 10615-10623
[Abstract]
[Full Text]
-
Li, H.-Y., Zheng, Y.
(2004). Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev.
18: 512-527
[Abstract]
[Full Text]
-
Trieselmann, N., Armstrong, S., Rauw, J., Wilde, A.
(2003). Ran modulates spindle assembly by regulating a subset of TPX2 and Kid activities including Aurora A activation. J. Cell Sci.
116: 4791-4798
[Abstract]
[Full Text]
-
Cimini, D., Moree, B., Canman, J. C., Salmon, E. D.
(2003). Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J. Cell Sci.
116: 4213-4225
[Abstract]
[Full Text]
-
Goshima, G., Vale, R. D.
(2003). The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. JCB
162: 1003-1016
[Abstract]
[Full Text]
-
Levesque, A. A., Howard, L., Gordon, M. B., Compton, D. A.
(2003). A Functional Relationship between NuMA and Kid Is Involved in Both Spindle Organization and Chromosome Alignment in Vertebrate Cells. Mol. Biol. Cell
14: 3541-3552
[Abstract]
[Full Text]
-
Shiroguchi, K., Ohsugi, M., Edamatsu, M., Yamamoto, T., Toyoshima, Y. Y.
(2003). The Second Microtubule-binding Site of Monomeric Kid Enhances the Microtubule Affinity. J. Biol. Chem.
278: 22460-22465
[Abstract]
[Full Text]
-
Frew, I. J., Dickins, R. A., Cuddihy, A. R., Del Rosario, M., Reinhard, C., O'Connell, M. J., Bowtell, D. D. L.
(2002). Normal p53 Function in Primary Cells Deficient for Siah Genes. Mol. Cell. Biol.
22: 8155-8164
[Abstract]
[Full Text]
-
Kapoor, T. M., Compton, D. A.
(2002). Searching for the middle ground: mechanisms of chromosome alignment during mitosis. JCB
157: 551-556
[Abstract]
[Full Text]