© The Rockefeller University Press,
0021-9525/1997//833 $5.00
The Journal of Cell Biology, Volume 138, Number 4,
, 1997 833-843
Identification of a Microtubule-associated Motor Protein Essential for Dendritic Differentiation
David J. Sharp*,
Wenqian Yu*,
Lotfi Ferhat*,
Ryoko Kuriyama
,
David C. Rueger
, and
Peter W. Baas*
* Department of Anatomy and Program in Neuroscience, The University of Wisconsin Medical School, Madison, Wisconsin 53706;
Department of Cell Biology and Neuroanatomy, The University of Minnesota Medical School, Minneapolis, Minnesota 55455; and
Creative Biomolecules, Hopkinton, Massachusetts 01748
The quintessential feature of the dendritic microtubule array is its nonuniform pattern of polarity orientation. During the development of the dendrite, a population of plus end–distal microtubules first appears, and these microtubules are subsequently joined by a population of oppositely oriented microtubules. Studies from our laboratory indicate that the latter microtubules are intercalated within the microtubule array by their specific transport from the cell body of the neuron during a critical stage in development (Sharp, D.J., W. Yu, and P.W. Baas. 1995. J. Cell Biol. 130:93– 104). In addition, we have established that the mitotic motor protein termed CHO1/MKLP1 has the appropriate properties to transport microtubules in this manner (Sharp, D.J., R. Kuriyama, and P.W. Baas. 1996. J. Neurosci. 16:4370–4375). In the present study we have sought to determine whether CHO1/MKLP1 continues to be expressed in terminally postmitotic neurons and whether it is required for the establishment of the dendritic microtubule array. In situ hybridization analyses reveal that CHO1/MKLP1 is expressed in postmitotic cultured rat sympathetic and hippocampal neurons. Immunofluorescence analyses indicate that the motor is absent from axons but is enriched in developing dendrites, where it appears as discrete patches associated with the microtubule array. Treatment of the neurons with antisense oligonucleotides to CHO1/MKLP1 suppresses dendritic differentiation, presumably by inhibiting the establishment of their nonuniform microtubule polarity pattern. We conclude that CHO1/MKLP1 transports microtubules from the cell body into the developing dendrite with their minus ends leading, thereby establishing the nonuniform microtubule polarity pattern of the dendrite.
Abbreviations used in this paper: AFU, arbitrary fluorescence unit; DIC, differential interference contrast.
Please address all correspondence to Peter W. Baas, Department of Anatomy, The University of Wisconsin Medical School, 1300 University Avenue, Madison, WI 53706. Tel: (608) 262-7307. Fax: (608) 262-7306. e-mail: pwbaas{at}facstaff.wisc.edu

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Stone, M. C., Roegiers, F., Rolls, M. M.
(2008). Microtubules Have Opposite Orientation in Axons and Dendrites of Drosophila Neurons. Mol. Biol. Cell
19: 4122-4129
[Abstract]
[Full Text]
-
Hirokawa, N., Noda, Y.
(2008). Intracellular Transport and Kinesin Superfamily Proteins, KIFs: Structure, Function, and Dynamics. Physiol. Rev.
88: 1089-1118
[Abstract]
[Full Text]
-
Bartolini, F., Gundersen, G. G.
(2006). Generation of noncentrosomal microtubule arrays. J. Cell Sci.
119: 4155-4163
[Abstract]
[Full Text]
-
Fink, G., Steinberg, G.
(2006). Dynein-dependent Motility of Microtubules and Nucleation Sites Supports Polarization of the Tubulin Array in the Fungus Ustilago maydis. Mol. Biol. Cell
17: 3242-3253
[Abstract]
[Full Text]
-
Medina, P. M. B., Swick, L. L., Andersen, R., Blalock, Z., Brenman, J. E.
(2006). A Novel Forward Genetic Screen for Identifying Mutations Affecting Larval Neuronal Dendrite Development in Drosophila melanogaster. Genetics
172: 2325-2335
[Abstract]
[Full Text]
-
Xu, X., He, C., Zhang, Z., Chen, Y.
(2006). MKLP1 requires specific domains for its dendritic targeting. J. Cell Sci.
119: 452-458
[Abstract]
[Full Text]
-
Reuter, J. E., Nardine, T. M., Penton, A., Billuart, P., Scott, E. K., Usui, T., Uemura, T., Luo, L.
(2003). A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development
130: 1203-1213
[Abstract]
[Full Text]
-
Pavenstadt, H., Kriz, W., Kretzler, M.
(2003). Cell Biology of the Glomerular Podocyte. Physiol. Rev.
83: 253-307
[Abstract]
[Full Text]
-
McAllister, A. K.
(2000). Cellular and Molecular Mechanisms of Dendrite Growth. Cereb Cortex
10: 963-973
[Abstract]
[Full Text]
-
Yu, W., Cook, C., Sauter, C., Kuriyama, R., Kaplan, P. L., Baas, P. W.
(2000). Depletion of a Microtubule-Associated Motor Protein Induces the Loss of Dendritic Identity. J. Neurosci.
20: 5782-5791
[Abstract]
[Full Text]
-
Gao, F.-B., Brenman, J. E., Jan, L. Y., Jan, Y. N.
(1999). Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev.
13: 2549-2561
[Abstract]
[Full Text]
-
Ahmad, F. J., Yu, W., McNally, F. J., Baas, P. W.
(1999). An Essential Role for Katanin in Severing Microtubules in the Neuron. JCB
145: 305-315
[Abstract]
[Full Text]
-
Matuliene, J, Essner, R, Ryu, J, Hamaguchi, Y, Baas, P., Haraguchi, T, Hiraoka, Y, Kuriyama, R
(1999). Function of a minus-end-directed kinesin-like motor protein in mammalian cells. J. Cell Sci.
112: 4041-4050
[Abstract]
-
Kobayashi, N., Reiser, J., Kriz, W., Kuriyama, R., Mundel, P.
(1998). Nonuniform Microtubular Polarity Established by CHO1/MKLP1 Motor Protein Is Necessary for Process Formation of Podocytes. JCB
143: 1961-1970
[Abstract]
[Full Text]
-
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. J. Neurosci.
18: 7822-7835
[Abstract]
[Full Text]
-
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. JCB
140: 391-401
[Abstract]
[Full Text]
-
Sharp, D., Kuriyama, R, Essner, R, Baas, P.
(1997). Expression of a minus-end-directed motor protein induces Sf9 cells to form axon-like processes with uniform microtubule polarity orientation. J. Cell Sci.
110: 2373-2380
[Abstract]
-
Chen, M.-C., Zhou, Y., Detrich, H. W. III
(2002). Zebrafish mitotic kinesin-like protein 1 (Mklp1) functions in embryonic cytokinesis. Physiol. Genomics
8: 51-66
[Abstract]
[Full Text]