MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties

doi:10.1083/jcb.105.3.1273

This Article

Full Text (PDF, 2750K)

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 Paschal, B. M.

Articles by Vallee, R. B.

Search for Related Content

PubMed

PubMed Citation

Articles by Paschal, B. M.

Articles by Vallee, R. B.

Pubmed/NCBI databases

Compound via MeSH
Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties

BM Paschal, HS Shpetner and RB Vallee
Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 01545.

We observe that one of the high molecular mass microtubule-associated proteins (MAPs) from brain exhibits nucleotide-dependent binding to microtubules. We identify the protein as MAP IC, which was previously described in this laboratory as a minor component of standard microtubule preparations (Bloom, G.S., T. Schoenfeld, and R.B. Vallee, 1984, J. Cell Biol., 98:320-330). We find that MAP 1C is enriched in microtubules prepared in the absence of nucleotide. Kinesin is also found in these preparations, but can be specifically extracted with GTP. A fraction highly enriched in MAP 1C can be prepared by subsequent extraction of the microtubules with ATP. Two activities cofractionate with MAP 1C upon further purification, a microtubule-activated ATPase activity and a microtubule-translocating activity. These activities indicate a role for the protein in cytoplasmic motility. MAP 1C coelectrophoreses with the beta heavy chain of Chlamydomonas flagellar dynein, and has a sedimentation coefficient of 20S. Exposure to ultraviolet light in the presence of vanadate and ATP results in the production of two large fragments of MAP 1C. These characteristics suggest that MAP 1C may be a cytoplasmic analogue of axonemal dynein.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Kimura, N., Inoue, M., Okabayashi, S., Ono, F., Negishi, T. (2009). Dynein Dysfunction Induces Endocytic Pathology Accompanied by an Increase in Rab GTPases: A POTENTIAL MECHANISM UNDERLYING AGE-DEPENDENT ENDOCYTIC DYSFUNCTION. J. Biol. Chem. 284: 31291-31302 [Abstract] [Full Text]
Kannan, H., Fan, S., Patel, D., Bossis, I., Zhang, Y.-J. (2009). The Hepatitis E Virus Open Reading Frame 3 Product Interacts with Microtubules and Interferes with Their Dynamics. J. Virol. 83: 6375-6382 [Abstract] [Full Text]
Ha, J., Lo, K. W.-H., Myers, K. R., Carr, T. M., Humsi, M. K., Rasoul, B. A., Segal, R. A., Pfister, K. K. (2008). A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. JCB 181: 1027-1039 [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]
Stehman, S. A., Chen, Y., McKenney, R. J., Vallee, R. B. (2007). NudE and NudEL are required for mitotic progression and are involved in dynein recruitment to kinetochores. JCB 178: 583-594 [Abstract] [Full Text]
Mogami, T., Kon, T., Ito, K., Sutoh, K. (2007). Kinetic Characterization of Tail Swing Steps in the ATPase Cycle of Dictyostelium Cytoplasmic Dynein. J. Biol. Chem. 282: 21639-21644 [Abstract] [Full Text]
Kelkar, S., De, B. P., Gao, G., Wilson, J. M., Crystal, R. G., Leopold, P. L. (2006). A Common Mechanism for Cytoplasmic Dynein-Dependent Microtubule Binding Shared among Adeno-Associated Virus and Adenovirus Serotypes.. J. Virol. 80: 7781-7785 [Abstract] [Full Text]
Toba, S., Watanabe, T. M., Yamaguchi-Okimoto, L., Toyoshima, Y. Y., Higuchi, H. (2006). Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc. Natl. Acad. Sci. USA 103: 5741-5745 [Abstract] [Full Text]
Powell, K. (2006). MAP 1C is a motor. JCB 172: 7-7 [Full Text]
Pfister, K. K., Fisher, E. M.C., Gibbons, I. R., Hays, T. S., Holzbaur, E. L.F., McIntosh, J. R., Porter, M. E., Schroer, T. A., Vaughan, K. T., Witman, G. B., King, S. M., Vallee, R. B. (2005). Cytoplasmic dynein nomenclature. JCB 171: 411-413 [Abstract] [Full Text]
Emanuele, M. J., McCleland, M. L., Satinover, D. L., Stukenberg, P. T. (2005). Measuring the Stoichiometry and Physical Interactions between Components Elucidates the Architecture of the Vertebrate Kinetochore. Mol. Biol. Cell 16: 4882-4892 [Abstract] [Full Text]
Yeh, T.-Y., Chuang, J.-Z., Sung, C.-H. (2005). Dynein light chain rp3 acts as a nuclear matrix-associated transcriptional modulator in a dynein-independent pathway. J. Cell Sci. 118: 3431-3443 [Abstract] [Full Text]
Schmidt, D. J., Rose, D. J., Saxton, W. M., Strome, S. (2005). Functional Analysis of Cytoplasmic Dynein Heavy Chain in Caenorhabditis elegans with Fast-acting Temperature-sensitive Mutations. Mol. Biol. Cell 16: 1200-1212 [Abstract] [Full Text]
Kelkar, S. A., Pfister, K. K., Crystal, R. G., Leopold, P. L. (2004). Cytoplasmic Dynein Mediates Adenovirus Binding to Microtubules. J. Virol. 78: 10122-10132 [Abstract] [Full Text]
Nishiura, M., Kon, T., Shiroguchi, K., Ohkura, R., Shima, T., Toyoshima, Y. Y., Sutoh, K. (2004). A Single-headed Recombinant Fragment of Dictyostelium Cytoplasmic Dynein Can Drive the Robust Sliding of Microtubules. J. Biol. Chem. 279: 22799-22802 [Abstract] [Full Text]
Ma, S., Chisholm, R. L. (2002). Cytoplasmic dynein-associated structures move bidirectionally in vivo. J. Cell Sci. 115: 1453-1460 [Abstract] [Full Text]
Chennathukuzhi, V. M., Kurihara, Y., Bray, J. D., Yang, J., Hecht, N. B. (2001). Altering the GTP binding site of the DNA/RNA-binding protein, Translin/TB-RBP, decreases RNA binding and may create a dominant negative phenotype. Nucleic Acids Res 29: 4433-4440 [Abstract] [Full Text]
Tai, A. W., Chuang, J.-Z., Sung, C.-H. (2001). Cytoplasmic Dynein Regulation by Subunit Heterogeneity and Its Role in Apical Transport. JCB 153: 1499-1510 [Abstract] [Full Text]
King, J. M., Hays, T. S., Nicklas, R. B. (2000). Dynein Is a Transient Kinetochore Component Whose Binding Is Regulated by Microtubule Attachment, Not Tension. JCB 151: 739-748 [Abstract] [Full Text]
Riquelme, M., Gierz, G., Bartnicki-García, S. (2000). Dynein and dynactin deficiencies affect the formation and function of the Spitzenkorper and distort hyphal morphogenesis of Neurospora crassa. Microbiology 146: 1743-1752 [Abstract] [Full Text]
Ye, G.-J., Vaughan, K. T., Vallee, R. B., Roizman, B. (2000). The Herpes Simplex Virus 1 UL34 Protein Interacts with a Cytoplasmic Dynein Intermediate Chain and Targets Nuclear Membrane. J. Virol. 74: 1355-1363 [Abstract] [Full Text]
Purohit, A., Tynan, S. H., Vallee, R., Doxsey, S. J. (1999). Direct Interaction of Pericentrin with Cytoplasmic Dynein Light Intermediate Chain Contributes to Mitotic Spindle Organization. JCB 147: 481-492 [Abstract] [Full Text]
Pollock, N., de Hostos, E. L., Turck, C. W., Vale, R. D. (1999). Reconstitution of Membrane Transport Powered by a Novel Dimeric Kinesin Motor of the Unc104/Kif1a Family Purified from Dictyostelium. JCB 147: 493-506 [Abstract] [Full Text]
Gonczy, P., Pichler, S., Kirkham, M., Hyman, A. A. (1999). Cytoplasmic Dynein Is Required for Distinct Aspects of Mtoc Positioning, Including Centrosome Separation, in the One Cell Stage Caenorhabditis elegans Embryo. JCB 147: 135-150 [Abstract] [Full Text]
Timm, S., Titus, B., Bernd, K., Barroso, M. (1999). The EF-hand Ca2+-binding Protein p22 Associates with Microtubules in an N-Myristoylation-dependent Manner. Mol. Biol. Cell 10: 3473-3488 [Abstract] [Full Text]
Lane, J. D., Allan, V. J. (1999). Microtubule-based Endoplasmic Reticulum Motility in Xenopus laevis: Activation of Membrane-associated Kinesin during Development. Mol. Biol. Cell 10: 1909-1922 [Abstract] [Full Text]
Marszalek, J. R., Weiner, J. A., Farlow, S. J., Chun, J., Goldstein, L. S.B. (1999). Novel Dendritic Kinesin Sorting Identified by Different Process Targeting of Two Related Kinesins: KIF21A and KIF21B. JCB 145: 469-479 [Abstract] [Full Text]
Hurst, S, Talbot, N., Stebbings, H (1999). A staufen-like RNA-binding protein in translocation channels linking nurse cells to oocytes in Notonecta shows nucleotide-dependent attachment to microtubules. J. Cell Sci. 112: 2947-2955 [Abstract]
Wubbolts, R, Fernandez-Borja, M, Jordens, I, Reits, E, Dusseljee, S, Echeverri, C, Vallee, R., Neefjes, J (1999). Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 112: 785-795 [Abstract]
Karki, S., LaMonte, B., Holzbaur, E. L.F. (1998). Characterization of the p22 Subunit of Dynactin Reveals the Localization of Cytoplasmic Dynein and Dynactin to the Midbody of Dividing Cells. JCB 142: 1023-1034 [Abstract] [Full Text]
Bashour, A.-M., Bloom, G. S. (1998). 58K, a Microtubule-binding Golgi Protein, Is a Formiminotransferase Cyclodeaminase. J. Biol. Chem. 273: 19612-19617 [Abstract] [Full Text]
Yonekawa, Y., Harada, A., Okada, Y., Funakoshi, T., Kanai, Y., Takei, Y., Terada, S., Noda, T., Hirokawa, N. (1998). Defect in Synaptic Vesicle Precursor Transport and Neuronal Cell Death in KIF1A Motor Protein-deficient Mice. JCB 141: 431-441 [Abstract] [Full Text]
Harada, A., Takei, Y., Kanai, Y., Tanaka, Y., Nonaka, S., Hirokawa, N. (1998). Golgi Vesiculation and Lysosome Dispersion in Cells Lacking Cytoplasmic Dynein. JCB 141: 51-59 [Abstract] [Full Text]
Hirokawa, N. (1998). Kinesin and Dynein Superfamily Proteins and the Mechanism of Organelle Transport. Science 279: 519-526 [Abstract] [Full Text]
Steffen, W., Karki, S., Vaughan, K. T., Vallee, R. B., Holzbaur, E. L.F., Weiss, D. G., Kuznetsov, S. A. (1997). The Involvement of the Intermediate Chain of Cytoplasmic Dynein in Binding the Motor Complex to Membranous Organelles of Xenopus Oocytes. Mol. Biol. Cell 8: 2077-2088 [Abstract] [Full Text]
Keating, T. J., Peloquin, J. G., Rodionov, V. I., Momcilovic, D., Borisy, G. G. (1997). Microtubule release from the�centrosome. Proc. Natl. Acad. Sci. USA 94: 5078-5083 [Abstract] [Full Text]
Rogers, S. L., Tint, I. S., Fanapour, P. C., Gelfand, V. I. (1997). Regulated bidirectional motility of melanophore pigment granules along microtubules�in�vitro. Proc. Natl. Acad. Sci. USA 94: 3720-3725 [Abstract] [Full Text]
King, S. M., Dillman, J. F. III, Benashski, S. E., Lye, R. J., Patel-King, RamilaS., Pfister, K.K. (1996). The Mouse t-Complex-encoded Protein Tctex-1 Is a Light Chain of Brain Cytoplasmic Dynein. J. Biol. Chem. 271: 32281-32287 [Abstract] [Full Text]
Dillman III, J. F., Dabney, L. P., Karki, S., Paschal, B. M., Holzbaur, E. L.�F., Pfister, K. K. (1996). Functional Analysis of Dynactin and Cytoplasmic Dynein in Slow Axonal Transport. J. Neurosci. 16: 6742-6752 [Abstract] [Full Text]
Blocker, A., Severin, F. F., Habermann, A., Hyman, A. A., Griffiths, G., Burkhardt, J. K. (1996). Microtubule-associated Protein-dependent Binding of Phagosomes to Microtubules. J. Biol. Chem. 271: 3803-3811 [Abstract] [Full Text]
Pfister, K. K., Salata, M. W., Dillman, J. F. III, Vaughan, K. T., Vallee, R. B., Torre, E., Lye, R. J. (1996). Differential Expression and Phosphorylation of the 74-kDa Intermediate Chains of Cytoplasmic Dynein in Cultured Neurons and Glia. J. Biol. Chem. 271: 1687-1694 [Abstract] [Full Text]
Criswell, P., Ostrowski, L., Asai, D. (1996). A novel cytoplasmic dynein heavy chain: expression of DHC1b in mammalian ciliated epithelial cells. J. Cell Sci. 109: 1891-1898 [Abstract]
Moudjou, M, Bordes, N, Paintrand, M, Bornens, M (1996). gamma-Tubulin in mammalian cells: the centrosomal and the cytosolic forms. J. Cell Sci. 109: 875-887 [Abstract]
Karki, S., Holzbaur, E. L. F. (1995). Affinity Chromatography Demonstrates a Direct Binding between Cytoplasmic Dynein and the Dynactin Complex. J. Biol. Chem. 270: 28806-28811 [Abstract] [Full Text]
Abe, K., Aoki, M., Kawagoe, J., Yoshida, T., Hattori, A., Kogure, K., Itoyama, Y. (1995). Ischemic Delayed Neuronal Death : A Mitochondrial Hypothesis. Stroke 26: 1478-1489 [Abstract] [Full Text]
Oda, H., Stockert, R. J., Collins, C., Wang, H., Novikoff, P. M., Satir, P., Wolkoff, A. W. (1995). Interaction of the Microtubule Cytoskeleton with Endocytic Vesicles and Cytoplasmic Dynein in Cultured Rat Hepatocytes. J. Biol. Chem. 270: 15242-15249 [Abstract] [Full Text]
Ferro, K. L., Collins, C. A. (1995). Microtubule-independent Phospholipid Stimulation of Cytoplasmic Dynein ATPase Activity. J. Biol. Chem. 270: 4492-4496 [Abstract] [Full Text]
Tanaka, Y, Zhang, Z, Hirokawa, N (1995). Identification and molecular evolution of new dynein-like protein sequences in rat brain. J. Cell Sci. 108: 1883-1893 [Abstract]
Dhamodharan, R, Wadsworth, P (1995). Modulation of microtubule dynamic instability in vivo by brain microtubule associated proteins. J. Cell Sci. 108: 1679-1689 [Abstract]
Moscatelli, A, Del Casino, C, Lozzi, L, Cai, G, Scali, M, Tiezzi, A, Cresti, M (1995). High molecular weight polypeptides related to dynein heavy chains in Nicotiana tabacum pollen tubes. J. Cell Sci. 108: 1117-1125 [Abstract]
Vallee, R.B., Vaughan, K.T., Escheverri, C.J. (1995). Targeting of Cytoplasmic Dynein to Membranous Organelles and Kinetochores via Dynactin. Cold Spring Harb Symp Quant Biol 60: 803-811 [Abstract]
Hughes, S., Vaughan, K., Herskovits, J., Vallee, R. (1995). Molecular analysis of a cytoplasmic dynein light intermediate chain reveals homology to a family of ATPases. J. Cell Sci. 108: 17-24 [Abstract]
Allan, V., Vale, R. (1994). Movement of membrane tubules along microtubules in vitro: evidence for specialised sites of motor attachment. J. Cell Sci. 107: 1885-1897 [Abstract]
Hays, T., Porter, M., McGrail, M, Grissom, P, Gosch, P, Fuller, M., McIntosh, J. (1994). A cytoplasmic dynein motor in Drosophila: identification and localization during embryogenesis. J. Cell Sci. 107: 1557-1569 [Abstract]
Asai, D., Beckwith, S., Kandl, K., Keating, H., Tjandra, H, Forney, J. (1994). The dynein genes of Paramecium tetraurelia. Sequences adjacent to the catalytic P-loop identify cytoplasmic and axonemal heavy chain isoforms. J. Cell Sci. 107: 839-847 [Abstract]
Wilkerson, C., King, S., Witman, G. (1994). Molecular analysis of the gamma heavy chain of Chlamydomonas flagellar outer-arm dynein. J. Cell Sci. 107: 497-506 [Abstract]
Yoshida, T, Ioshii, S., Imanaka-Yoshida, K, Izutsu, K (1994). Association of cytoplasmic dynein with manchette microtubules and spermatid nuclear envelope during spermiogenesis in rats. J. Cell Sci. 107: 625-633 [Abstract]
Yokota, E, Mabuchi, I (1994). Isolation and characterization of a novel dynein that contains C and A heavy chains from sea urchin sperm flagellar axonemes. J. Cell Sci. 107: 345-351 [Abstract]
Yokota, E, Mabuchi, I (1994). C/A dynein isolated from sea urchin sperm flagellar axonemes. Enzymatic properties and interaction with microtubules. J. Cell Sci. 107: 353-361 [Abstract]
Morris, R., Hollenbeck, P. (1993). The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci. 104: 917-927 [Abstract]
Kagami, O., Kamiya, R. (1992). Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J. Cell Sci. 103: 653-664 [Abstract]
Theurkauf, W., Smiley, S, Wong, M., Alberts, B. (1992). Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115: 923-936 [Abstract]
Walter, R. J., Danielson, J. R., Reyes, H. M. (1990). Characterization of a Chemotactic Defect in Patients With Kartagener Syndrome. Arch Otolaryngol Head Neck Surg 116: 465-469 [Abstract]