The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau

doi:10.1083/jcb.109.6.3367

This Article

	Full Text (PDF, 2313K)
	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 Noble, M.
	Articles by Cowan, N. J.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Noble, M.
	Articles by Cowan, N. J.


Social Bookmarking

	What's this?

ARTICLES

The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau

M Noble, SA Lewis and NJ Cowan
Department of Biochemistry, New York University Medical Center 10016.

We report the complete sequence of the microtubule-associated protein MAP1B, deduced from a series of overlapping genomic and cDNA clones. The encoded protein has a predicted molecular mass of 255,534 D and contains two unusual sequences. The first is a highly basic region that includes multiple copies of a short motif of the form KKEE or KKEVI that are repeated, but not at exact intervals. The second is a set of 12 imperfect repeats, each of 15 amino acids and each spaced by two amino acids. Subcloned fragments spanning these two distinctive regions were expressed as labeled polypeptides by translation in a cell-free system in vitro. These polypeptides were tested for their ability to copurify with unlabeled brain microtubules through successive cycles of polymerization and depolymerization. The peptide corresponding to the region containing the KKEE and KKEVI motifs cycled with brain microtubules, whereas the peptide corresponding to the set of 12 imperfect repeats did not. To define the microtubule binding domain in vivo, full-length and deletion constructs encoding MAP1B were assembled and introduced into cultured cells by transfection. The expression of transfected polypeptides was monitored by indirect immunofluorescence using anti-MAP1B-specific antisera. These experiments showed that the basic region containing the KKEE and KKEVI motifs is responsible for the interaction between MAP1B and microtubules in vivo. This region bears no sequence relationship to the microtubule binding domains of kinesin, MAP2, or tau.
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:

Patel, P. C., Fisher, K. H., Yang, E. C. C., Deane, C. M., Harrison, R. E. (2009). Proteomic Analysis of Microtubule-associated Proteins during Macrophage Activation. Mol. Cell. Proteomics 8: 2500-2514 [Abstract] [Full Text]
Scales, T. M. E., Lin, S., Kraus, M., Goold, R. G., Gordon-Weeks, P. R. (2009). Nonprimed and DYRK1A-primed GSK3{beta}-phosphorylation sites on MAP1B regulate microtubule dynamics in growing axons. J. Cell Sci. 122: 2424-2435 [Abstract] [Full Text]
Sun, H., Hu, X.-Q., Emerit, M. B., Schoenebeck, J. C., Kimmel, C. E., Peoples, R. W., Miko, A., Zhang, L. (2008). Modulation of 5-HT3 receptor desensitization by the light chain of microtubule-associated protein 1B expressed in HEK 293 cells. J. Physiol. 586: 751-762 [Abstract] [Full Text]
Sines, T., Granot-Attas, S., Weisman-Welcher, S., Elson, A. (2007). Association of Tyrosine Phosphatase Epsilon with Microtubules Inhibits Phosphatase Activity and Is Regulated by the Epidermal Growth Factor Receptor. Mol. Cell. Biol. 27: 7102-7112 [Abstract] [Full Text]
Wang, X., Zhu, L., Liu, B., Wang, C., Jin, L., Zhao, Q., Yuan, M. (2007). Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 Functions in Directional Cell Growth by Destabilizing Cortical Microtubules. Plant Cell 19: 877-889 [Abstract] [Full Text]
Hanson, S. M., Francis, D. J., Vishnivetskiy, S. A., Klug, C. S., Gurevich, V. V. (2006). Visual Arrestin Binding to Microtubules Involves a Distinct Conformational Change. J. Biol. Chem. 281: 9765-9772 [Abstract] [Full Text]
Kouno, T., Mizuguchi, M., Tanida, I., Ueno, T., Kanematsu, T., Mori, Y., Shinoda, H., Hirata, M., Kominami, E., Kawano, K. (2005). Solution Structure of Microtubule-associated Protein Light Chain 3 and Identification of Its Functional Subdomains. J. Biol. Chem. 280: 24610-24617 [Abstract] [Full Text]
Cho, H. P., Liu, Y., Gomez, M., Dunlap, J., Tyers, M., Wang, Y. (2005). The Dual-Specificity Phosphatase CDC14B Bundles and Stabilizes Microtubules. Mol. Cell. Biol. 25: 4541-4551 [Abstract] [Full Text]
Trivedi, N., Marsh, P., Goold, R. G., Wood-Kaczmar, A., Gordon-Weeks, P. R. (2005). Glycogen synthase kinase-3{beta} phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J. Cell Sci. 118: 993-1005 [Abstract] [Full Text]
Orban-Nemeth, Z., Simader, H., Badurek, S., Trancikova, A., Propst, F. (2005). Microtubule-associated Protein 1S, a Short and Ubiquitously Expressed Member of the Microtubule-associated Protein 1 Family. J. Biol. Chem. 280: 2257-2265 [Abstract] [Full Text]
Franz, C. M., Ridley, A. J. (2004). p120 Catenin Associates with Microtubules: INVERSE RELATIONSHIP BETWEEN MICROTUBULE BINDING AND RHO GTPase REGULATION. J. Biol. Chem. 279: 6588-6594 [Abstract] [Full Text]
Bu, W., Su, L.-K. (2003). Characterization of Functional Domains of Human EB1 Family Proteins. J. Biol. Chem. 278: 49721-49731 [Abstract] [Full Text]
Hayano, T., Yanagida, M., Yamauchi, Y., Shinkawa, T., Isobe, T., Takahashi, N. (2003). Proteomic Analysis of Human Nop56p-associated Pre-ribosomal Ribonucleoprotein Complexes: POSSIBLE LINK BETWEEN Nop56p AND THE NUCLEOLAR PROTEIN TREACLE RESPONSIBLE FOR TREACHER COLLINS SYNDROME. J. Biol. Chem. 278: 34309-34319 [Abstract] [Full Text]
Opal, P., Garcia, J. J., Propst, F., Matilla, A., Orr, H. T., Zoghbi, H. Y. (2003). Mapmodulin/Leucine-rich Acidic Nuclear Protein Binds the Light Chain of Microtubule-associated Protein 1B and Modulates Neuritogenesis. J. Biol. Chem. 278: 34691-34699 [Abstract] [Full Text]
Tokuraku, K., Matsushima, K., Matui, T., Nakagawa, H., Katsuki, M., Majima, R., Kotani, S. (2003). The Number of Repeat Sequences in Microtubule-associated Protein 4 Affects the Microtubule Surface Properties. J. Biol. Chem. 278: 29609-29618 [Abstract] [Full Text]
Pfannenschmid, F., Wimmer, V. C., Rios, R.-M., Geimer, S., Krockel, U., Leiherer, A., Haller, K., Nemcova, Y., Mages, W. (2003). Chlamydomonas DIP13 and human NA14: a new class of proteins associated with microtubule structures is involved in cell division. J. Cell Sci. 116: 1449-1462 [Abstract] [Full Text]
Hu, K., Roos, D. S., Murray, J. M. (2002). A novel polymer of tubulin forms the conoid of Toxoplasma gondii. JCB 156: 1039-1050 [Abstract] [Full Text]
Noiges, R., Eichinger, R., Kutschera, W., Fischer, I., Nemeth, Z., Wiche, G., Propst, F. (2002). Microtubule-Associated Protein 1A (MAP1A) and MAP1B: Light Chains Determine Distinct Functional Properties. J. Neurosci. 22: 2106-2114 [Abstract] [Full Text]
Haren, L., Merdes, A. (2002). Direct binding of NuMA to tubulin is mediated by a novel sequence motif in the tail domain that bundles and stabilizes microtubules. J. Cell Sci. 115: 1815-1824 [Abstract] [Full Text]
Teng, J., Takei, Y., Harada, A., Nakata, T., Chen, J., Hirokawa, N. (2001). Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. JCB 155: 65-76 [Abstract] [Full Text]
Takei, Y., Teng, J., Harada, A., Hirokawa, N. (2000). Defects in Axonal Elongation and Neuronal Migration in Mice with Disrupted tau and map1b Genes. JCB 150: 989-1000 [Abstract] [Full Text]
Koonce, M. P., Tikhonenko, I. (2000). Functional Elements within the Dynein Microtubule-binding Domain. Mol. Biol. Cell 11: 523-529 [Abstract] [Full Text]
Leung, C. L., Sun, D., Zheng, M., Knowles, D. R., Liem, R. K.H. (1999). Microtubule Actin Cross-Linking Factor (Macf): A Hybrid of Dystonin and Dystrophin That Can Interact with the Actin and Microtubule Cytoskeletons. JCB 147: 1275-1286 [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]
Goold, R., Owen, R, Gordon-Weeks, P. (1999). Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112: 3373-3384 [Abstract]
Trimbur, G., Goeckeler, J., Brodsky, J., Walsh, C. (1999). Cloning, sequencing, and nucleolar targeting of the basal-body-binding nucleolar protein BN46/51. J. Cell Sci. 112: 1159-1168 [Abstract]
Gachet, Y, Tournier, S, Lee, M, Lazaris-Karatzas, A, Poulton, T, Bommer, U. (1999). The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J. Cell Sci. 112: 1257-1271 [Abstract]
Togel, M., Wiche, G., Propst, F. (1998). Novel Features of the Light Chain of Microtubule-associated Protein MAP1B: Microtubule Stabilization, Self Interaction, Actin Filament Binding, and Regulation by the Heavy Chain. JCB 143: 695-707 [Abstract] [Full Text]
Hamill, D. R., Howell, B., Cassimeris, L., Suprenant, K. A. (1998). Purification of a WD Repeat Protein, EMAP, That Promotes Microtubule Dynamics through an Inhibition of Rescue. J. Biol. Chem. 273: 9285-9291 [Abstract] [Full Text]
Charrasse, S, Schroeder, M, Gauthier-Rouviere, C, Ango, F, Cassimeris, L, Gard, D., Larroque, C (1998). The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J. Cell Sci. 111: 1371-1383 [Abstract]
Roghi, C, Giet, R, Uzbekov, R, Morin, N, Chartrain, I, Le Guellec, R, Couturier, A, Doree, M, Philippe, M, Prigent, C (1998). The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J. Cell Sci. 111: 557-572 [Abstract]
Wang, P. J., Huffaker, T. C. (1997). Stu2p: A Microtubule-Binding Protein that Is an Essential Component of the Yeast Spindle Pole Body. JCB 139: 1271-1280 [Abstract] [Full Text]
Yamauchi, E., Titani, K., Taniguchi, H. (1997). Specific Binding of Acidic Phospholipids to Microtubule-associated Protein MAP1B Regulates Its Interaction with Tubulin. J. Biol. Chem. 272: 22948-22953 [Abstract] [Full Text]
Takei, Y., Kondo, S., Harada, A., Inomata, S., Noda, T., Hirokawa, N. (1997). Delayed Development of Nervous System in Mice Homozygous for Disrupted Microtubule-associated Protein 1B (MAP1B) Gene. JCB 137: 1615-1626 [Abstract] [Full Text]
Marten, I., Hoshi, T. (1997). Voltage-dependent gating characteristics of the K+ channel KAT1 depend on the N and C�termini. Proc. Natl. Acad. Sci. USA 94: 3448-3453 [Abstract] [Full Text]
Ye, X., Sloboda, R. D. (1997). Molecular Characterization of p62, a Mitotic Apparatus Protein Required for Mitotic Progression. J. Biol. Chem. 272: 3606-3614 [Abstract] [Full Text]
Liu, D., Fischer, I. (1996). Two Alternative Promoters Direct Neuron-Specific Expression of the Rat Microtubule-Associated Protein 1B Gene. J. Neurosci. 16: 5026-5036 [Abstract] [Full Text]
Black, M. M., Slaughter, T., Moshiach, S., Obrocka, M., Fischer, I. (1996). Tau Is Enriched on Dynamic Microtubules in the Distal Region of Growing Axons. J. Neurosci. 16: 3601-3619 [Abstract] [Full Text]
Goedert, M, Baur, C., Ahringer, J, Jakes, R, Hasegawa, M, Spillantini, M., Smith, M., Hill, F (1996). PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J. Cell Sci. 109: 2661-2672 [Abstract]
Zachow, K., Bentley, D (1996). Blackjack, a novel protein associated with microtubules in embryonic neurons. J. Cell Sci. 109: 1497-1507 [Abstract]
Mangan, M., Olmsted, J. (1996). A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122: 771-781 [Abstract]
DiTella, M., Feiguin, F, Carri, N, Kosik, K., Caceres, A (1996). MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J. Cell Sci. 109: 467-477 [Abstract]
Dominguez, J., Buendia, B, Lopez-Otin, C, Antony, C, Karsenti, E, Avila, J (1994). A protein related to brain microtubule-associated protein MAP1B is a component of the mammalian centrosome. J. Cell Sci. 107: 601-611 [Abstract]
Marya, P., Syed, Z, Fraylich, P., Eagles, P. (1994). Kinesin and tau bind to distinct sites on microtubules. J. Cell Sci. 107: 339-344 [Abstract]
Maekawa, T, Kuriyama, R (1993). Primary structure and microtubule-interacting domain of the SP-H antigen: a mitotic MAP located at the spindle pole and characterized as a homologous protein to NuMA. J. Cell Sci. 105: 589-600 [Abstract]
Tang, T., Tang, C., Chen, Y., Wu, C. (1993). Nuclear proteins of the bovine esophageal epithelium. II. The NuMA gene gives rise to multiple mRNAs and gene products reactive with monoclonal antibody W1. J. Cell Sci. 104: 249-260 [Abstract]
Takemura, R., Okabe, S., Umeyama, T., Kanai, Y., Cowan, N. J., Hirokawa, N. (1992). Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J. Cell Sci. 103: 953-964 [Abstract]
Ling, L., Goeddel, D. V. (2000). MIP-T3, a Novel Protein Linking Tumor Necrosis Factor Receptor-associated Factor 3 to the Microtubule Network. J. Biol. Chem. 275: 23852-23860 [Abstract] [Full Text]
Taylor, K. R., Holzer, A. K., Bazan, J. F., Walsh, C. A., Gleeson, J. G. (2000). Patient Mutations in Doublecortin Define a Repeated Tubulin-binding Domain. J. Biol. Chem. 275: 34442-34450 [Abstract] [Full Text]
Bonnet, C., Boucher, D., Lazereg, S., Pedrotti, B., Islam, K., Denoulet, P., Larcher, J. C. (2001). Differential Binding Regulation of Microtubule-associated Proteins MAP1A, MAP1B, and MAP2 by Tubulin Polyglutamylation. J. Biol. Chem. 276: 12839-12848 [Abstract] [Full Text]