Abstract
Kif15 is a kinesin-related protein whose mitotic homologues are believed to crosslink and immobilize spindle microtubules. We have obtained rodent sequences of Kif15, and have studied their expression and distribution in the developing nervous system. Kif15 is indeed expressed in actively dividing fibroblasts, but is also expressed in terminally postmitotic neurons. In mitotic cells, Kif15 localizes to spindle poles and microtubules during prometaphase to early anaphase, but then to the actin-based cleavage furrow during cytokinesis. In interphase fibroblasts, Kif15 localizes to actin bundles but not to microtubules. In cultured neurons, Kif15 localizes to microtubules but shows no apparent co-localization with actin. Localization of Kif15 to microtubules is particularly good when the microtubules are bundled, and there is a notable enrichment of Kif15 in the microtubule bundles that occupy stalled growth cones and dendrites. Studies on developing rodent brain show a pronounced enrichment of Kif15 in migratory neurons compared to other neurons. Notably, migratory neurons have a cage-like configuration of microtubules around their nucleus that is linked to the microtubule array within the leading process, such that the entire array moves in unison as the cell migrates. Since the capacity of microtubules to move independently of one another is restricted in all of these cases, we propose that Kif15 opposes the capacity of other motors to generate independent microtubule movements within key regions of developing neurons.
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AHMAD, F. J., ECHEVERRI, C. J., VALLEE, R. B. & BAAS, P. W. (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. Journal of Cell Biology 140, 246–256.
AHMAD, F. J., HUGHEY, J., WITTMANN, T., HYMAN, A., GREASER, M. & BAAS, P. W. (2000) Motor proteins regulate force interactions between microtubules and microfilaments in the axon. Nature Cell Biology 2, 276–280.
AHMAD, F. J., YU, W., MCNALLY, F. J. & BAAS, P. W. (1999) An essential role for katanin in severing microtubules in the neuron. Journal of Cell Biology 145, 305–315.
BAAS, P. W. (1999) Microtubules and neuronal polarity: Lessons from mitosis. Neuron 22, 23–31.
BOLETI, H., KARSENTI, E. & VERNOS, I. (1996) Xklp2, a novel Xenopus centrosomal kinesin-like protein required for centrosome separation during mitosis. Cell 84, 49–59.
DENT, E. W., CALLAWAY, J. L., SZEBENYI, G., BAAS, P. W. & KALIL, K. (1999) Reorganization and movement of microtubules in growth cones and developing interstitial branches. Journal of Neuroscience 9, 8894–8904.
DILLMANN III, J. F., DABNEY, L. P. & PFISTER, K. K. (1996) Cytoplasmic dynein is associated with slow axonal transport. Proceedings of the National Acadamy Science USA 93, 141–144.
FENG, Y. & WALSH, C. A. (2001) Protein-protein interactions, cytoskeletal regulation and neuronal migration. Nature Reviews Neuroscience 2, 408–416.
FERHAT, L., COOK, C., CHAUVIERE, M., HARPER, M., KRESS, M., LYONS, G. E. & BAAS, P. W. (1998) Expression of the mitotic motor protein Eg5 in postmitotic neurons: Implications for neuronal development. Journal of Neuroscience 18, 7822–7835.
HAENDEL, M. A., BOLLINGER, K. E. & BAAS, P. W. (1996) Cytoskeletal changes during neurogenesis in cultures of avian neural crest cells. Journal of Neurocytology 25, 289–301.
HATTEN, M. E. (1999) Central nervous system neuronal migration. Annual Review of Neuroscience 22, 511–539.
HE, Y. & BAAS, P. W. (2003) Growing and working with peripheral neurons. In Nerve Cell Biology (edited by HOLLENBECK, P. & BAMBURG, J.), a volume in Methods in Cell Biology 71, 17–35.
HUANG, J.-D., BRADY, S. T., RICHARDS, B. W., STENOLEN, D., RESAU, J. H., COPELAND, N. G. & JENKINS, N. A. (1999) Direct interaction of microtubule-and actin-based transport motors. Nature 397, 267–270.
KURIYAMA, R., GUSTUS, C., TERADA, Y., UETAKE, Y. & MATULIENE, J. (2002) CHO1, a mammalian kinesinlike protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. Journal of Cell Biology 156, 783–790.
NAKAGAWA, T., TANAKA, Y., MATSUOKA, E., KONDO, S., OKADA, Y., NODA, Y., KANAI, Y. & HIROKAWA, N. (1997) Identification and classification of 16 new kinesin superfamily (KIF) proteins in mouse genome. Proceedings of the National Academy Science USA 94, 9654–9659.
RIVAS, R. J., BURMEISTER, D. W. & GOLDBERG, D. J. (1992) Rapid effects of laminin on the growth cone. Neuron 8, 107–115.
RIVAS, R. J. & HATTEN, M. E. (1995) Motility and cytoskeletal organization of migrating cerebellar granule neurons. Journal of Neuroscience 15, 981–989.
ROGERS, G. C., CHUI, K. K., LEE, E. W., WEDAMAN, K. P., SHARP, D. J., HOLLAND, G., MORRIS, R. L. & SCHOLEY, J. M. (2000) A kinesin-related protein, KRP180, positions prometaphase spindle poles during early sea urchin embryonic cell division. Journal of Cell Biology 150, 499–511.
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. (1989) Molecular Cloning. A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press.
SHARP, D. J., ROGERS, G. C. & SCHOLEY, J. M. (2000) Microtubule motors in mitosis. Nature 407, 41–47.
SHARP, D. J., YU, W. & BAAS, P. W. (1995) Transport of dendritic microtubules establishes their nonuniform polarity orientation. Journal of Cell Biology 130, 93–104.
SHARP, D. J., YU, W., FERHAT, L., KURIYAMA, R., RUEGER, D. C. & BAAS, P. W. (1997) Identification of a microtubule-associated motor protein essential for dendritic differentiation. Journal of Cell Biology 138, 833–843.
SLAUGHTER, T. S., WANG, J. & BLACK, M. M. (1997) Transport of microtubules from the cell body into the axons of cultured neurons. Journal of Neuroscience 17, 5807–5819.
SMITH, D. S., NIETHAMMER, M., AYALA, R., ZHOU, Y., GAMBELLO, M. J., WYNSHAW-BORIS, A. & TSIA, L.-H. (2000) Regulation of cytoplasmic dynein behavior and microtubule organization by mammalian Lis1. Nature Cell Biology 2, 767–775.
SUEISHI, M., TAKAGI, M. & YONEDA, Y. (2000) The forkhead-associated domain of Ki-67 antigen interacts with the novel kinesin-like protein Hklp2. Journal of Biological Chemistry 275, 28888–28892.
TRENKNER, E. (1991) Cerebellar cells in culture. In Culturing Nerve Cells (edited by BANKER, G. & GOSLIN, K.) pp. 283–307. MIT Press.
TANG, D. & GOLDBERG, D. J. (2000) Bundling of microtubules in the growth cone induced by laminin. Molecular and Cellular Neuroscience 15, 303–313.
WANG, L. & BROWN, A. (2002) Rapid movement of microtubules in axons. Current Biology 12, 1496–1501.
WITTMANN, T., HYMAN, A. & DESAI, A. (2001) The spindle: A dynamic assembly of microtubules and motors. Nature Cell Biology 3, E28–E34.
WITTMANN, T., WILM, M., KARSENTI, E. & VERNOS, I. (2000) TPX2, a novel XenopusMAPinvolved in spindle pole organization. Journal of Cell Biology 149, 1405–1418.
WYNSHAW-BORIS, A. & GAMBELLO, M. J. (2001) LIS1 and dynein motor function in neuronal migration and development. Genes & Development 15, 639–651.
YU, W., AHMAD, F. J. & BAAS, P. W. (1994) Microtubule fragmentation and partitioning in the axon during collateral branch formation. Journal of Neuroscience 14, 5872–5984.
YU, W., COOK, C., KURIYAMA, R., KAPLAN, P. L. & BAAS, P. W. (2000) Depletion of a microtubuleassociated motor protein induces the loss of dendritic identity. Journal of Neuroscience 20, 5782–5781.
YU, W., LING, C. & BAAS, P. W. (2001) Microtubule reconfiguration during axogenesis. Journal of Neurocytology 30, 861–875.
YU, W., SCHWEI, M. J. & BAAS, P. W. (1996) Microtubule transport and assembly during axon growth. Journal of Cell Biology 133, 151–157.
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Buster, D.W., Baird, D.H., Yu, W. et al. Expression of the mitotic kinesin Kif15 in postmitotic neurons: Implications for neuronal migration and development. J Neurocytol 32, 79–96 (2003). https://doi.org/10.1023/A:1027332432740
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DOI: https://doi.org/10.1023/A:1027332432740