Interactions and regulation of molecular motors in Xenopus melanophores

doi:10.1083/jcb.200105055

Published online 25 February 2002. doi:10.1083/jcb.200105055

This Article

Full Text

PDF (Full Text)

PPT slides of all figures

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JCB

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Gross, S. P.

Articles by Gelfand, V. I.

Search for Related Content

PubMed

PubMed Citation

Articles by Gross, S. P.

Articles by Gelfand, V. I.

Pubmed/NCBI databases

Hazardous Substances DB
Compound via MeSH
Substance via MeSH
1-PHENYL-2-THIOUREA

Social Bookmarking

What's this?

© The Rockefeller University Press, 0021-9525/2002/3/855 $5.00
The Journal of Cell Biology, Volume 156, Number 5, March 4, 2002 855-865

Article

Interactions and regulation of molecular motors in Xenopus melanophores

Steven P. Gross¹, M. Carolina Tuma², Sean W. Deacon², Anna S. Serpinskaya², Amy R. Reilein² and Vladimir I. Gelfand²

¹ Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA 92697
² Department of Cell and Structural Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801

Address correspondence to Vladimir I. Gelfand, Dept. of Cell and Structural Biology, University of Illinois, B107 CLSL, 601 S. Goodwin Ave., Urbana, IL 61801. Tel.: (217) 333-5972. Fax: (217) 244-1648. E-mail: vgelfand{at}life.uiuc.edu

Many cellular components are transported using a combinationof the actin- and microtubule-based transport systems. However,how these two systems work together to allow well-regulatedtransport is not clearly understood. We investigate this questionin the Xenopus melanophore model system, where three motors,kinesin II, cytoplasmic dynein, and myosin V, drive aggregationor dispersion of pigment organelles called melanosomes. Duringdispersion, myosin V functions as a "molecular ratchet" to increaseoutward transport by selectively terminating dynein-driven minusend runs. We show that there is a continual tug-of-war betweenthe actin and microtubule transport systems, but the microtubulemotors kinesin II and dynein are likely coordinated. Finally,we find that the transition from dispersion to aggregation increasesdynein-mediated motion, decreases myosin V–mediated motion,and does not change kinesin II–dependent motion. Down-regulationof myosin V contributes to aggregation by impairing its abilityto effectively compete with movement along microtubules.

Key Words: dynein; kinesin II; myosin V; melanophore; organelle transport

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Boyle, R. T., McNamara, J. C. (2008). A Spring-Matrix Model for Pigment Translocation in the Red Ovarian Chromatophores of the Freshwater Shrimp Macrobrachium olfersi (Crustacea, Decapoda). Biol. Bull. 214: 111-121 [Abstract] [Full Text]
Muller, M. J. I., Klumpp, S., Lipowsky, R. (2008). Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc. Natl. Acad. Sci. USA 105: 4609-4614 [Abstract] [Full Text]
Ali, M. Y., Lu, H., Bookwalter, C. S., Warshaw, D. M., Trybus, K. M. (2008). Myosin V and Kinesin act as tethers to enhance each others' processivity. Proc. Natl. Acad. Sci. USA 105: 4691-4696 [Abstract] [Full Text]
Hodges, A. R., Krementsova, E. B., Trybus, K. M. (2008). She3p Binds to the Rod of Yeast Myosin V and Prevents It from Dimerizing, Forming a Single-headed Motor Complex. J. Biol. Chem. 283: 6906-6914 [Abstract] [Full Text]
Slepchenko, B. M., Semenova, I., Zaliapin, I., Rodionov, V. (2007). Switching of membrane organelles between cytoskeletal transport systems is determined by regulation of the microtubule-based transport. J. Cell Biol. 179: 635-641 [Abstract] [Full Text]
Desnos, C., Huet, S., Fanget, I., Chapuis, C., Bottiger, C., Racine, V., Sibarita, J.-B., Henry, J.-P., Darchen, F. (2007). Myosin Va Mediates Docking of Secretory Granules at the Plasma Membrane. J. Neurosci. 27: 10636-10645 [Abstract] [Full Text]
Leduc, C., Ruhnow, F., Howard, J., Diez, S. (2007). From the Cover: Detection of fractional steps in cargo movement by the collective operation of kinesin-1 motors. Proc. Natl. Acad. Sci. USA 104: 10847-10852 [Abstract] [Full Text]
Haghnia, M., Cavalli, V., Shah, S. B., Schimmelpfeng, K., Brusch, R., Yang, G., Herrera, C., Pilling, A., Goldstein, L. S.B. (2007). Dynactin Is Required for Coordinated Bidirectional Motility, but Not for Dynein Membrane Attachment. Mol. Biol. Cell 18: 2081-2089 [Abstract] [Full Text]
Petrov, D. Y., Mallik, R., Shubeita, G. T., Vershinin, M., Gross, S. P., Yu, C. C. (2007). Studying Molecular Motor-Based Cargo Transport: What Is Real and What Is Noise?. Biophys. J 92: 2953-2963 [Abstract] [Full Text]
Kural, C., Serpinskaya, A. S., Chou, Y.-H., Goldman, R. D., Gelfand, V. I., Selvin, P. R. (2007). Tracking melanosomes inside a cell to study molecular motors and their interaction. Proc. Natl. Acad. Sci. USA 104: 5378-5382 [Abstract] [Full Text]
Ali, M. Y., Krementsova, E. B., Kennedy, G. G., Mahaffy, R., Pollard, T. D., Trybus, K. M., Warshaw, D. M. (2007). From the Cover: Myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc. Natl. Acad. Sci. USA 104: 4332-4336 [Abstract] [Full Text]
Romagnoli, S., Cai, G., Faleri, C., Yokota, E., Shimmen, T., Cresti, M. (2007). Microtubule- and Actin Filament-Dependent Motors are Distributed on Pollen Tube Mitochondria and Contribute Differently to Their Movement. Plant Cell Physiol 48: 345-361 [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]
Dinh, A.-T., Pangarkar, C., Theofanous, T., Mitragotri, S. (2006). Theory of Spatial Patterns of Intracellular Organelles. Biophys. J 90: L67-L69 [Abstract] [Full Text]
Adams, D. S., Robinson, K. R., Fukumoto, T., Yuan, S., Albertson, R. C., Yelick, P., Kuo, L., McSweeney, M., Levin, M. (2006). Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133: 1657-1671 [Abstract] [Full Text]
Levi, V., Serpinskaya, A. S., Gratton, E., Gelfand, V. (2006). Organelle Transport along Microtubules in Xenopus Melanophores: Evidence for Cooperation between Multiple Motors. Biophys. J 90: 318-327 [Abstract] [Full Text]
Levi, V., Gelfand, V. I., Serpinskaya, A. S., Gratton, E. (2006). Melanosomes Transported by Myosin-V in Xenopus Melanophores Perform Slow 35 nm Steps. Biophys. J 90: L07-L09 [Abstract] [Full Text]
Hollenbeck, P. J., Saxton, W. M. (2005). The axonal transport of mitochondria. J. Cell Sci. 118: 5411-5419 [Abstract] [Full Text]
Serbus, L. R., Cha, B.-J., Theurkauf, W. E., Saxton, W. M. (2005). Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132: 3743-3752 [Abstract] [Full Text]
Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V. I., Selvin, P. R. (2005). Kinesin and Dynein Move a Peroxisome in Vivo: A Tug-of-War or Coordinated Movement?. Science 308: 1469-1472 [Abstract] [Full Text]
Zaliapin, I., Semenova, I., Kashina, A., Rodionov, V. (2005). Multiscale Trend Analysis of Microtubule Transport in Melanophores. Biophys. J 88: 4008-4016 [Abstract] [Full Text]
Chabrillat, M. L., Wilhelm, C., Wasmeier, C., Sviderskaya, E. V., Louvard, D., Coudrier, E. (2005). Rab8 Regulates the Actin-based Movement of Melanosomes. Mol. Biol. Cell 16: 1640-1650 [Abstract] [Full Text]
Takeshita, N., Ohta, A., Horiuchi, H. (2005). CsmA, a Class V Chitin Synthase with a Myosin Motor-like Domain, Is Localized through Direct Interaction with the Actin Cytoskeleton in Aspergillus nidulans. Mol. Biol. Cell 16: 1961-1970 [Abstract] [Full Text]
Gibbs, D., Azarian, S. M., Lillo, C., Kitamoto, J., Klomp, A. E., Steel, K. P., Libby, R. T., Williams, D. S. (2004). Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes. J. Cell Sci. 117: 6473-6483 [Abstract] [Full Text]
Smith, G. A., Pomeranz, L., Gross, S. P., Enquist, L. W. (2004). Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl. Acad. Sci. USA 101: 16034-16039 [Abstract] [Full Text]
Wagner, O. I., Ascano, J., Tokito, M., Leterrier, J.-F., Janmey, P. A., Holzbaur, E. L. F. (2004). The Interaction of Neurofilaments with the Microtubule Motor Cytoplasmic Dynein. Mol. Biol. Cell 15: 5092-5100 [Abstract] [Full Text]
Snider, J., Lin, F., Zahedi, N., Rodionov, V., Yu, C. C., Gross, S. P. (2004). Intracellular actin-based transport: How far you go depends on how often you switch. Proc. Natl. Acad. Sci. USA 101: 13204-13209 [Abstract] [Full Text]
Cytrynbaum, E. N., Rodionov, V., Mogilner, A. (2004). Computational model of dynein-dependent self-organization of microtubule asters. J. Cell Sci. 117: 1381-1397 [Abstract] [Full Text]
Provance, D. W. Jr., Gourley, C. R., Silan, C. M., Cameron, L. C., Shokat, K. M., Goldenring, J. R., Shah, K., Gillespie, P. G., Mercer, J. A. (2004). From the Cover: Chemical-genetic inhibition of a sensitized mutant myosin Vb demonstrates a role in peripheral-pericentriolar membrane traffic. Proc. Natl. Acad. Sci. USA 101: 1868-1873 [Abstract] [Full Text]
Bannai, H., Inoue, T., Nakayama, T., Hattori, M., Mikoshiba, K. (2004). Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons. J. Cell Sci. 117: 163-175 [Abstract] [Full Text]
Lalli, G., Gschmeissner, S., Schiavo, G. (2003). Myosin Va and microtubule-based motors are required for fast axonal retrograde transport of tetanus toxin in motor neurons. J. Cell Sci. 116: 4639-4650 [Abstract] [Full Text]
Manneville, J.-B., Etienne-Manneville, S., Skehel, P., Carter, T., Ogden, D., Ferenczi, M. (2003). Interaction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells. J. Cell Sci. 116: 3927-3938 [Abstract] [Full Text]
De Vos, K. J., Sable, J., Miller, K. E., Sheetz, M. P. (2003). Expression of Phosphatidylinositol (4,5) Bisphosphate-specific Pleckstrin Homology Domains Alters Direction But Not the Level of Axonal Transport of Mitochondria. Mol. Biol. Cell 14: 3636-3649 [Abstract] [Full Text]
Kuroda, T. S., Ariga, H., Fukuda, M. (2003). The Actin-Binding Domain of Slac2-a/Melanophilin Is Required for Melanosome Distribution in Melanocytes. Mol. Cell. Biol. 23: 5245-5255 [Abstract] [Full Text]
Burgoyne, R. D., Morgan, A. (2003). Secretory Granule Exocytosis. Physiol. Rev. 83: 581-632 [Abstract] [Full Text]
Deacon, S. W., Serpinskaya, A. S., Vaughan, P. S., Fanarraga, M. L., Vernos, I., Vaughan, K. T., Gelfand, V. I. (2003). Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160: 297-301 [Abstract] [Full Text]
Dell, K. R. (2003). Dynactin polices two-way organelle traffic. J. Cell Biol. 160: 291-293 [Abstract] [Full Text]
Romagnoli, S., Cai, G., Cresti, M. (2003). In Vitro Assays Demonstrate That Pollen Tube Organelles Use Kinesin-Related Motor Proteins to Move along Microtubules. Plant Cell 15: 251-269 [Abstract] [Full Text]
Palacios, I. M., Johnston, D. S. (2002). Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129: 5473-5485 [Abstract] [Full Text]