J. Cell Biol., Volume 144, Number 3, February 8, 1999 473-481

The DHC1b (DHC2) Isoform of Cytoplasmic Dynein Is Required for Flagellar Assembly

Gregory J. Pazour, Bethany L. Dickert, and George B. Witman

Department of Cell Biology, University of Massachusetts Medical School, Worcester, Massachusetts 01655

Dyneins are microtubule-based molecular motors involved in many different types of cell movement. Most dynein heavy chains (DHCs) clearly group into cytoplasmic or axonemal isoforms. However, DHC1b has been enigmatic. To learn more about this isoform, we isolated Chlamydomonas cDNA clones encoding a portion of DHC1b, and used these clones to identify a Chlamydomonas cell line with a deletion mutation in DHC1b. The mutant grows normally and appears to have a normal Golgi apparatus, but has very short flagella. The deletion also results in a massive redistribution of raft subunits from a peri-basal body pool (Cole, D.G., D.R. Diener, A.L. Himelblau, P.L. Beech, J.C. Fuster, and J.L. Rosenbaum. 1998. J. Cell Biol. 141:993-1008) to the flagella. Rafts are particles that normally move up and down the flagella in a process known as intraflagellar transport (IFT) (Kozminski, K.G., K.A. Johnson, P. Forscher, and J.L. Rosenbaum. 1993. Proc. Natl. Acad. Sci. USA. 90:5519-5523), which is essential for assembly and maintenance of flagella. The redistribution of raft subunits apparently occurs due to a defect in the retrograde component of IFT, suggesting that DHC1b is the motor for retrograde IFT. Consistent with this, Western blots indicate that DHC1b is present in the flagellum, predominantly in the detergent- and ATP-soluble fractions. These results indicate that DHC1b is a cytoplasmic dynein essential for flagellar assembly, probably because it is the motor for retrograde IFT.

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

This article has been cited by other articles:

• Tsao, C.-C., Gorovsky, M. A. (2008). Different Effects of Tetrahymena IFT172 Domains on Anterograde and Retrograde Intraflagellar Transport. Mol. Biol. Cell 19: 1450-1461 [Abstract] [Full Text]  
• Jauregui, A. R., Nguyen, K. C.Q., Hall, D. H., Barr, M. M. (2008). The Caenorhabditis elegans nephrocystins act as global modifiers of cilium structure. J. Cell Biol. 180: 973-988 [Abstract] [Full Text]  
• Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Dore, G., Julkowska, D., Tavenet, A., Bastin, P. (2008). Intraflagellar Transport and Functional Analysis of Genes Required for Flagellum Formation in Trypanosomes. Mol. Biol. Cell 19: 929-944 [Abstract] [Full Text]  
• Tsao, C.-C., Gorovsky, M. A. (2008). Tetrahymena IFT122A is not essential for cilia assembly but plays a role in returning IFT proteins from the ciliary tip to the cell body. J. Cell Sci. 121: 428-436 [Abstract] [Full Text]  
• Scholey, J. M. (2008). Intraflagellar transport motors in cilia: moving along the cell's antenna. J. Cell Biol. 180: 23-29 [Abstract] [Full Text]  
• Rompolas, P., Pedersen, L. B., Patel-King, R. S., King, S. M. (2007). Chlamydomonas FAP133 is a dynein intermediate chain associated with the retrograde intraflagellar transport motor. J. Cell Sci. 120: 3653-3665 [Abstract] [Full Text]  
• Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G. B., Terry, A., Salamov, A., Fritz-Laylin, L. K., Marechal-Drouard, L., Marshall, W. F., Qu, L.-H., Nelson, D. R., Sanderfoot, A. A., Spalding, M. H., Kapitonov, V. V., Ren, Q., Ferris, P., Lindquist, E., Shapiro, H., Lucas, S. M., Grimwood, J., Schmutz, J., Cardol, P., Cerutti, H., Chanfreau, G., Chen, C.-L., Cognat, V., Croft, M. T., Dent, R., Dutcher, S., Fernandez, E., Fukuzawa, H., Gonzalez-Ballester, D., Gonzalez-Halphen, D., Hallmann, A., Hanikenne, M., Hippler, M., Inwood, W., Jabbari, K., Kalanon, M., Kuras, R., Lefebvre, P. A., Lemaire, S. D., Lobanov, A. V., Lohr, M., Manuell, A., Meier, I., Mets, L., Mittag, M., Mittelmeier, T., Moroney, J. V., Moseley, J., Napoli, C., Nedelcu, A. M., Niyogi, K., Novoselov, S. V., Paulsen, I. T., Pazour, G., Purton, S., Ral, J.-P., Riano-Pachon, D. M., Riekhof, W., Rymarquis, L., Schroda, M., Stern, D., Umen, J., Willows, R., Wilson, N., Zimmer, S. L., Allmer, J., Balk, J., Bisova, K., Chen, C.-J., Elias, M., Gendler, K., Hauser, C., Lamb, M. R., Ledford, H., Long, J. C., Minagawa, J., Page, M. D., Pan, J., Pootakham, W., Roje, S., Rose, A., Stahlberg, E., Terauchi, A. M., Yang, P., Ball, S., Bowler, C., Dieckmann, C. L., Gladyshev, V. N., Green, P., Jorgensen, R., Mayfield, S., Mueller-Roeber, B., Rajamani, S., Sayre, R. T., Brokstein, P., Dubchak, I., Goodstein, D., Hornick, L., Huang, Y. W., Jhaveri, J., Luo, Y., Martinez, D., Ngau, W. C. A., Otillar, B., Poliakov, A., Porter, A., Szajkowski, L., Werner, G., Zhou, K., Grigoriev, I. V., Rokhsar, D. S., Grossman, A. R. (2007). The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions. Science 318: 245-250 [Abstract] [Full Text]  
• Hildebrandt, F., Zhou, W. (2007). Nephronophthisis-Associated Ciliopathies. J. Am. Soc. Nephrol. 18: 1855-1871 [Abstract] [Full Text]  
• Ou, G., Koga, M., Blacque, O. E., Murayama, T., Ohshima, Y., Schafer, J. C., Li, C., Yoder, B. K., Leroux, M. R., Scholey, J. M. (2007). Sensory Ciliogenesis in Caenorhabditis elegans: Assignment of IFT Components into Distinct Modules Based on Transport and Phenotypic Profiles. Mol. Biol. Cell 18: 1554-1569 [Abstract] [Full Text]  
• Hou, Y., Qin, H., Follit, J. A., Pazour, G. J., Rosenbaum, J. L., Witman, G. B. (2007). Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J. Cell Biol. 176: 653-665 [Abstract] [Full Text]  
• Blacque, O. E., Li, C., Inglis, P. N., Esmail, M. A., Ou, G., Mah, A. K., Baillie, D. L., Scholey, J. M., Leroux, M. R. (2006). The WD Repeat-containing Protein IFTA-1 Is Required for Retrograde Intraflagellar Transport. Mol. Biol. Cell 17: 5053-5062 [Abstract] [Full Text]  
• Hook, P., Vallee, R. B. (2006). The dynein family at a glance. J. Cell Sci. 119: 4369-4371 [Full Text]  
• Efimenko, E., Blacque, O. E., Ou, G., Haycraft, C. J., Yoder, B. K., Scholey, J. M., Leroux, M. R., Swoboda, P. (2006). Caenorhabditis elegans DYF-2, an Orthologue of Human WDR19, Is a Component of the Intraflagellar Transport Machinery in Sensory Cilia. Mol. Biol. Cell 17: 4801-4811 [Abstract] [Full Text]  
• Imanishi, M., Endres, N. F., Gennerich, A., Vale, R. D. (2006). Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. J. Cell Biol. 174: 931-937 [Abstract] [Full Text]  
• Dymek, E. E., Goduti, D., Kramer, T., Smith, E. F. (2006). A kinesin-like calmodulin-binding protein in Chlamydomonas: evidence for a role in cell division and flagellar functions. J. Cell Sci. 119: 3107-3116 [Abstract] [Full Text]  
• Evans, J. E., Snow, J. J., Gunnarson, A. L., Ou, G., Stahlberg, H., McDonald, K. L., Scholey, J. M. (2006). Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. J. Cell Biol. 172: 663-669 [Abstract] [Full Text]  
• Davenport, J. R., Yoder, B. K. (2005). An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am. J. Physiol. Renal Physiol. 289: F1159-F1169 [Abstract] [Full Text]  
• Dentler, W. (2005). Intraflagellar transport (IFT) during assembly and disassembly of Chlamydomonas flagella. J. Cell Biol. 170: 649-659 [Abstract] [Full Text]  
• Huangfu, D., Anderson, K. V. (2005). From the Cover: Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102: 11325-11330 [Abstract] [Full Text]  
• Miller, M. S., Esparza, J. M., Lippa, A. M., Lux, F. G. III, Cole, D. G., Dutcher, S. K. (2005). Mutant Kinesin-2 Motor Subunits Increase Chromosome Loss. Mol. Biol. Cell 16: 3810-3820 [Abstract] [Full Text]  
• Lucker, B. F., Behal, R. H., Qin, H., Siron, L. C., Taggart, W. D., Rosenbaum, J. L., Cole, D. G. (2005). Characterization of the Intraflagellar Transport Complex B Core: DIRECT INTERACTION OF THE IFT81 AND IFT74/72 SUBUNITS. J. Biol. Chem. 280: 27688-27696 [Abstract] [Full Text]  
• Mueller, J., Perrone, C. A., Bower, R., Cole, D. G., Porter, M. E. (2005). The FLA3 KAP Subunit Is Required for Localization of Kinesin-2 to the Site of Flagellar Assembly and Processive Anterograde Intraflagellar Transport. Mol. Biol. Cell 16: 1341-1354 [Abstract] [Full Text]  
• Redeker, V., Levilliers, N., Vinolo, E., Rossier, J., Jaillard, D., Burnette, D., Gaertig, J., Bre, M.-H. (2005). Mutations of Tubulin Glycylation Sites Reveal Cross-talk between the C Termini of {alpha}- and {beta}-Tubulin and Affect the Ciliary Matrix in Tetrahymena. J. Biol. Chem. 280: 596-606 [Abstract] [Full Text]  
• Mahjoub, M. R., Qasim Rasi, M., Quarmby, L. M. (2004). A NIMA-related Kinase, Fa2p, Localizes to a Novel Site in the Proximal Cilia of Chlamydomonas and Mouse Kidney Cells. Mol. Biol. Cell 15: 5172-5186 [Abstract] [Full Text]  
• Rana, A. A., Barbera, J. P. M., Rodriguez, T. A., Lynch, D., Hirst, E., Smith, J. C., Beddington, R. S. P. (2004). Targeted deletion of the novel cytoplasmic dynein mD2LIC disrupts the embryonic organiser, formation of the body axes and specification of ventral cell fates. Development 131: 4999-5007 [Abstract] [Full Text]  
• Pazour, G. J. (2004). Intraflagellar Transport and Cilia-Dependent Renal Disease: The Ciliary Hypothesis of Polycystic Kidney Disease. J. Am. Soc. Nephrol. 15: 2528-2536 [Abstract] [Full Text]  
• Hou, Y., Pazour, G. J., Witman, G. B. (2004). A Dynein Light Intermediate Chain, D1bLIC, Is Required for Retrograde Intraflagellar Transport. Mol. Biol. Cell 15: 4382-4394 [Abstract] [Full Text]  
• Levin, M. (2004). THE EMBRYONIC ORIGINS OF LEFT-RIGHT ASYMMETRY. Crit. Rev. Oral Biol. Med. 15: 197-206 [Abstract] [Full Text]  
• Wirschell, M., Pazour, G., Yoda, A., Hirono, M., Kamiya, R., Witman, G. B. (2004). Oda5p, a Novel Axonemal Protein Required for Assembly of the Outer Dynein Arm and an Associated Adenylate Kinase. Mol. Biol. Cell 15: 2729-2741 [Abstract] [Full Text]  
• Iomini, C., Tejada, K., Mo, W., Vaananen, H., Piperno, G. (2004). Primary cilia of human endothelial cells disassemble under laminar shear stress. J. Cell Biol. 164: 811-817 [Abstract] [Full Text]  
• Wang, S., Luo, Y., Wilson, P. D., Witman, G. B., Zhou, J. (2004). The Autosomal Recessive Polycystic Kidney Disease Protein Is Localized to Primary Cilia, with Concentration in the Basal Body Area. J. Am. Soc. Nephrol. 15: 592-602 [Abstract] [Full Text]  
• Qin, H., Diener, D. R., Geimer, S., Cole, D. G., Rosenbaum, J. L. (2004). Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J. Cell Biol. 164: 255-266 [Abstract] [Full Text]  
• Tam, L.-W., Dentler, W. L., Lefebvre, P. A. (2003). Defective flagellar assembly and length regulation in LF3 null mutants in Chlamydomonas. J. Cell Biol. 163: 597-607 [Abstract] [Full Text]  
• Baker, S. A., Freeman, K., Luby-Phelps, K., Pazour, G. J., Besharse, J. C. (2003). IFT20 Links Kinesin II with a Mammalian Intraflagellar Transport Complex That Is Conserved in Motile Flagella and Sensory Cilia. J. Biol. Chem. 278: 34211-34218 [Abstract] [Full Text]  
• Wiese, M., Kuhn, D., Grunfelder, C. G. (2003). Protein Kinase Involved in Flagellar-Length Control. Eukaryot Cell 2: 769-777 [Abstract] [Full Text]  
• Brown, J. M., Fine, N. A., Pandiyan, G., Thazhath, R., Gaertig, J. (2003). Hypoxia Regulates Assembly of Cilia in Suppressors of Tetrahymena Lacking an Intraflagellar Transport Subunit Gene. Mol. Biol. Cell 14: 3192-3207 [Abstract] [Full Text]  
• Pan, J., Snell, W. J. (2003). Kinesin II and regulated intraflagellar transport of Chlamydomonas aurora protein kinase. J. Cell Sci. 116: 2179-2186 [Abstract] [Full Text]  
• Perrone, C. A., Tritschler, D., Taulman, P., Bower, R., Yoder, B. K., Porter, M. E. (2003). A Novel Dynein Light Intermediate Chain Colocalizes with the Retrograde Motor for Intraflagellar Transport at Sites of Axoneme Assembly in Chlamydomonas and Mammalian Cells. Mol. Biol. Cell 14: 2041-2056 [Abstract] [Full Text]  
• Schafer, J. C., Haycraft, C. J., Thomas, J. H., Yoder, B. K., Swoboda, P. (2003). XBX-1 Encodes a Dynein Light Intermediate Chain Required for Retrograde Intraflagellar Transport and Cilia Assembly in Caenorhabditis elegans. Mol. Biol. Cell 14: 2057-2070 [Abstract] [Full Text]  
• Patel-King, R. S., Benashski, S. E., King, S. M. (2002). A Bipartite Ca2+-regulated Nucleoside-diphosphate Kinase System within the Chlamydomonas Flagellum. THE REGULATORY SUBUNIT p72. J. Biol. Chem. 277: 34271-34279 [Abstract] [Full Text]  
• Campbell, P. K., Waymire, K. G., Heier, R. L., Sharer, C., Day, D. E., Reimann, H., Jaje, J. M., Friedrich, G. A., Burmeister, M., Bartness, T. J., Russell, L. D., Young, L. J., Zimmer, M., Jenne, D. E., MacGregor, G. R. (2002). Mutation of a Novel Gene Results in Abnormal Development of Spermatid Flagella, Loss of Intermale Aggression and Reduced Body Fat in Mice. Genetics 162: 307-320 [Abstract] [Full Text]  
• Pazour, G. J., Baker, S. A., Deane, J. A., Cole, D. G., Dickert, B. L., Rosenbaum, J. L., Witman, G. B., Besharse, J. C. (2002). The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J. Cell Biol. 157: 103-114 [Abstract] [Full Text]  
• Grissom, P. M., Vaisberg, E. A., McIntosh, J. R. (2002). Identification of a Novel Light Intermediate Chain (D2LIC) for Mammalian Cytoplasmic Dynein 2. Mol. Biol. Cell 13: 817-829 [Abstract] [Full Text]  
• Takada, S., Wilkerson, C. G., Wakabayashi, K.-i., Kamiya, R., Witman, G. B. (2002). The Outer Dynein Arm-Docking Complex: Composition and Characterization of a Subunit (Oda1) Necessary for Outer Arm Assembly. Mol. Biol. Cell 13: 1015-1029 [Abstract] [Full Text]  
• Silflow, C. D., Lefebvre, P. A. (2001). Assembly and Motility of Eukaryotic Cilia and Flagella. Lessons from Chlamydomonas reinhardtii. Plant Physiol. 127: 1500-1507 [Full Text]  
• Iomini, C., Babaev-Khaimov, V., Sassaroli, M., Piperno, G. (2001). Protein Particles in Chlamydomonas Flagella Undergo a Transport Cycle Consisting of Four Phases. J. Cell Biol. 153: 13-24 [Abstract] [Full Text]  
• Boylan, K., Serr, M., Hays, T. (2000). A Molecular Genetic Analysis of the Interaction between the Cytoplasmic Dynein Intermediate Chain and the Glued (Dynactin) Complex. Mol. Biol. Cell 11: 3791-3803 [Abstract] [Full Text]  
• Pazour, G., Dickert, B., Vucica, , Seeley, E., Rosenbaum, J., Witman, G., Cole, D. (2000). Chlamydomonas IFT88 and Its Mouse Homologue, Polycystic Kidney Disease Gene Tg737, Are Required for Assembly of Cilia and Flagella. J. Cell Biol. 151: 709-718 [Abstract] [Full Text]  
• Prahlad, V, Helfand, B., Langford, G., Vale, R., Goldman, R. (2000). Fast transport of neurofilament protein along microtubules in squid axoplasm. J. Cell Sci. 113: 3939-3946 [Abstract]  
• Bastin, P, Ellis, K, Kohl, L, Gull, K (2000). Flagellum ontogeny in trypanosomes studied via an inherited and regulated RNA interference system. J. Cell Sci. 113: 3321-3328 [Abstract]  
• Bastin, P., MacRae, T. H., Francis, S. B., Matthews, K. R., Gull, K. (1999). Flagellar Morphogenesis: Protein Targeting and Assembly in the Paraflagellar Rod of Trypanosomes. Mol. Cell. Biol. 19: 8191-8200 [Abstract] [Full Text]  
• Cole, D. G. (1999). Kinesin-II, Coming and Going. J. Cell Biol. 147: 463-466 [Abstract] [Full Text]  
• Signor, D., Wedaman, K. P., Orozco, J. T., Dwyer, N. D., Bargmann, C. I., Rose, L. S., Scholey, J. M. (1999). Role of a Class DHC1b Dynein in Retrograde Transport of IFT Motors and IFT Raft Particles Along Cilia, but Not Dendrites, in Chemosensory Neurons of Living Caenorhabditis elegans. J. Cell Biol. 147: 519-530 [Abstract] [Full Text]  
• Pazour, G. J., Koutoulis, A., Benashski, S. E., Dickert, B. L., Sheng, H., Patel-King, R. S., King, S. M., Witman, G. B. (1999). LC2, the Chlamydomonas Homologue of the t Complex-encoded Protein Tctex2, Is Essential for Outer Dynein Arm Assembly. Mol. Biol. Cell 10: 3507-3520 [Abstract] [Full Text]  
• Myster, S. H., Knott, J. A., Wysocki, K. M., O'Toole, E., Porter, M. E. (1999). Domains in the 1{alpha} Dynein Heavy Chain Required for Inner Arm Assembly and Flagellar Motility in Chlamydomonas. J. Cell Biol. 146: 801-818 [Abstract] [Full Text]  
• Bowman, A. B., Patel-King, R. S., Benashski, S. E., McCaffery, J. M., Goldstein, L. S.B., King, S. M. (1999). Drosophila roadblock and Chlamydomonas LC7: A Conserved Family of Dynein-associated Proteins Involved in Axonal Transport, Flagellar Motility, and Mitosis. J. Cell Biol. 146: 165-180 [Abstract] [Full Text]  
• Rosenbaum, J. L., Cole, D. G., Diener, D. R. (1999). Intraflagellar Transport: The Eyes Have It. J. Cell Biol. 144: 385-388 [Full Text]  
• Roghi, C, Allan, V. (1999). Dynamic association of cytoplasmic dynein heavy chain 1a with the Golgi apparatus and intermediate compartment. J. Cell Sci. 112: 4673-4685 [Abstract]  
• Bastin, P, Pullen, T., Sherwin, T, Gull, K (1999). Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J. Cell Sci. 112: 3769-3777 [Abstract]  
• Pan, J., Snell, W. J. (2000). Regulated Targeting of a Protein Kinase into an Intact Flagellum. AN AURORA/Ipl1p-LIKE PROTEIN KINASE TRANSLOCATES FROM THE CELL BODY INTO THE FLAGELLA DURING GAMETE ACTIVATION IN CHLAMYDOMONAS. J. Biol. Chem. 275: 24106-24114 [Abstract] [Full Text]  
• DiBella, L. M., Benashski, S. E., Tedford, H. W., Harrison, A., Patel-King, R. S., King, S. M. (2001). The Tctex1/Tctex2 Class of Dynein Light Chains. DIMERIZATION, DIFFERENTIAL EXPRESSION, AND INTERACTION WITH THE LC8 PROTEIN FAMILY. J. Biol. Chem. 276: 14366-14373 [Abstract] [Full Text]  
• Song, L., Dentler, W. L. (2001). Flagellar Protein Dynamics in Chlamydomonas. J. Biol. Chem. 276: 29754-29763 [Abstract] [Full Text]  
• Pazour, G. J., Baker, S. A., Deane, J. A., Cole, D. G., Dickert, B. L., Rosenbaum, J. L., Witman, G. B., Besharse, J. C. (2002). The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J. Cell Biol. 157: 103-114 [Abstract] [Full Text]  
• Pan, J., Snell, W. J. (2002). Kinesin-II Is Required for Flagellar Sensory Transduction during Fertilization in Chlamydomonas. Mol. Biol. Cell 13: 1417-1426 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents