Coronin Promotes the Rapid Assembly and Cross-linking of Actin Filaments and May Link the Actin and Microtubule Cytoskeletons in Yeast

doi:10.1083/jcb.144.1.83

This Article

	Full Text
	Full Text (PDF, 1889K)
	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 Goode, B. L.
	Articles by Barnes, G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Goode, B. L.
	Articles by Barnes, G.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/1999//83 $5.00
The Journal of Cell Biology, Volume 144, Number 1, , 1999 83-98

Article

Coronin Promotes the Rapid Assembly and Cross-linking of Actin Filaments and May Link the Actin and Microtubule Cytoskeletons in Yeast

Bruce L. Goode^*, Jonathan J. Wong^*, Anne-Christine Butty, Matthias Peter, Ashley L. McCormack, John R. Yates, David G. Drubin^*, and Georjana Barnes^*

^* Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-3202; Swiss Institute for Experimental Cancer Research, Lausanne, Switzerland; and Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195

Coronin is a highly conserved actin-associated protein thatuntil now has had unknown biochemical activities. Using microtubuleaffinity chromatography, we coisolated actin and a homologueof coronin, Crn1p, from Saccharomyces cerevisiae cell extracts. Crn1p is an abundant component of the cortical actin cytoskeletonand binds to F-actin with high affinity (K_d 6 x 10^–9M). Crn1p promotes the rapid barbed-end assembly of actin filamentsand cross-links filaments into bundles and more complex networks,but does not stabilize them. Genetic analyses with a crn1 ${Delta}$ deletionmutation also are consistent with Crn1p regulating filamentassembly rather than stability. Filament cross-linking dependson the coiled coil domain of Crn1p, suggesting a requirementfor Crn1p dimerization. Assembly-promoting activity is independentof cross-linking and could be due to nucleation and/or accelerated polymerization. Crn1p also binds to microtubules in vitro,and microtubule binding is enhanced by the presence of actinfilaments. Microtubule binding is mediated by a region of Crn1pthat contains sequences (not found in other coronins) homologousto the microtubule binding region of MAP1B. These activities,considered with microtubule defects observed in crn1 ${Delta}$ cellsand in cells overexpressing Crn1p, suggest that Crn1p may providea functional link between the actin and microtubule cytoskeletonsin yeast.

Key Words: actin • microtubule • coronin • cytoskeleton • yeast

Abbreviations used in this paper: GFP, green fluorescent protein; GST, glutathione-S-transferase; HSS, high speed supernatant; IPTG, isopropyl-thio-β-D-galactoside.

Address correspondence to Dr. Georjana Barnes, Department ofMolecular and Cell Biology, 401 Barker Hall, University of California,Berkeley, CA 94720-3202. Tel.: (510) 643-2010. Fax: (510) 642-6420.E-mail: gbarnes @socrates.berkeley.edu

We are especially grateful to Lisa Belmont for making the initialobservation of the genetic interactions between the crn1 ${Delta}$ andact1-159 mutations. We also thank Alison Adams for generouslyproviding purified Sac6p, Hadar Haddad for technical assistance,Kent McDonald for instruction and assistance with electronmicroscopy, and Lisa Belmont, Pekka Lappalainen, Jamie Cope,and Keith Kozminski for helpful comments on the manuscript.

CiteULike

Complore

Connotea

Del.icio.us Add to Digg

Digg

Facebook

Technorati

Twitter What's this?

This article has been cited by other articles:

Sahasrabuddhe, A. A., Nayak, R. C., Gupta, C. M. (2009). Ancient Leishmania coronin (CRN12) is involved in microtubule remodeling during cytokinesis. J. Cell Sci. 122: 1691-1699 [Abstract] [Full Text]
Combaluzier, B., Pieters, J. (2009). Chemotaxis and Phagocytosis in Neutrophils Is Independent of Coronin 1. J. Immunol. 182: 2745-2752 [Abstract] [Full Text]
Jayachandran, R., Gatfield, J., Massner, J., Albrecht, I., Zanolari, B., Pieters, J. (2008). RNA Interference in J774 Macrophages Reveals a Role for Coronin 1 in Mycobacterial Trafficking but Not in Actin-dependent Processes. Mol. Biol. Cell 19: 1241-1251 [Abstract] [Full Text]
Cai, L., Makhov, A. M., Bear, J. E. (2007). F-actin binding is essential for coronin 1B function in vivo. J. Cell Sci. 120: 1779-1790 [Abstract] [Full Text]
Yan, M., Di Ciano-Oliveira, C., Grinstein, S., Trimble, W. S. (2007). Coronin Function Is Required for Chemotaxis and Phagocytosis in Human Neutrophils. J. Immunol. 178: 5769-5778 [Abstract] [Full Text]
Moseley, J. B., Bartolini, F., Okada, K., Wen, Y., Gundersen, G. G., Goode, B. L. (2007). Regulated Binding of Adenomatous Polyposis Coli Protein to Actin. J. Biol. Chem. 282: 12661-12668 [Abstract] [Full Text]
Toshima, J., Toshima, J. Y., Duncan, M. C., Cope, M. J. T.V., Sun, Y., Martin, A. C., Anderson, S., Yates, J. R. III, Mizuno, K., Drubin, D. G. (2007). Negative Regulation of Yeast Eps15-like Arp2/3 Complex Activator, Pan1p, by the Hip1R-related Protein, Sla2p, during Endocytosis. Mol. Biol. Cell 18: 658-668 [Abstract] [Full Text]
Smythe, E., Ayscough, K. R. (2006). Actin regulation in endocytosis. J. Cell Sci. 119: 4589-4598 [Abstract] [Full Text]
Brieher, W. M., Kueh, H. Y., Ballif, B. A., Mitchison, T. J. (2006). Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. JCB 175: 315-324 [Abstract] [Full Text]
Moseley, J. B., Goode, B. L. (2006). The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism. Microbiol. Mol. Biol. Rev. 70: 605-645 [Abstract] [Full Text]
Foger, N., Rangell, L., Danilenko, D. M., Chan, A. C. (2006). Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis.. Science 313: 839-842 [Abstract] [Full Text]
Friesen, H., Humphries, C., Ho, Y., Schub, O., Colwill, K., Andrews, B. (2006). Characterization of the Yeast Amphiphysins Rvs161p and Rvs167p Reveals Roles for the Rvs Heterodimer In Vivo. Mol. Biol. Cell 17: 1306-1321 [Abstract] [Full Text]
Cai, L., Holoweckyj, N., Schaller, M. D., Bear, J. E. (2005). Phosphorylation of Coronin 1B by Protein Kinase C Regulates Interaction with Arp2/3 and Cell Motility. J. Biol. Chem. 280: 31913-31923 [Abstract] [Full Text]
Moseley, J. B., Goode, B. L. (2005). Differential Activities and Regulation of Saccharomyces cerevisiae Formin Proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280: 28023-28033 [Abstract] [Full Text]
Yan, M., Collins, R. F., Grinstein, S., Trimble, W. S. (2005). Coronin-1 Function Is Required for Phagosome Formation. Mol. Biol. Cell 16: 3077-3087 [Abstract] [Full Text]
Quintero-Monzon, O., Rodal, A. A., Strokopytov, B., Almo, S. C., Goode, B. L. (2005). Structural and Functional Dissection of the Abp1 ADFH Actin-binding Domain Reveals Versatile In Vivo Adapter Functions. Mol. Biol. Cell 16: 3128-3139 [Abstract] [Full Text]
Wen, K.-K., Rubenstein, P. A. (2005). Acceleration of Yeast Actin Polymerization by Yeast Arp2/3 Complex Does Not Require an Arp2/3-activating Protein. J. Biol. Chem. 280: 24168-24174 [Abstract] [Full Text]
Gatfield, J., Albrecht, I., Zanolari, B., Steinmetz, M. O., Pieters, J. (2005). Association of the Leukocyte Plasma Membrane with the Actin Cytoskeleton through Coiled Coil-mediated Trimeric Coronin 1 Molecules. Mol. Biol. Cell 16: 2786-2798 [Abstract] [Full Text]
Tsukada, M., Prokscha, A., Ungewickell, E., Eichele, G. (2005). Doublecortin Association with Actin Filaments Is Regulated by Neurabin II. J. Biol. Chem. 280: 11361-11368 [Abstract] [Full Text]
Rodal, A. A., Kozubowski, L., Goode, B. L., Drubin, D. G., Hartwig, J. H. (2005). Actin and Septin Ultrastructures at the Budding Yeast Cell Cortex. Mol. Biol. Cell 16: 372-384 [Abstract] [Full Text]
Young, M. E., Cooper, J. A., Bridgman, P. C. (2004). Yeast actin patches are networks of branched actin filaments. JCB 166: 629-635 [Abstract] [Full Text]
Les Erickson, F., Corsa, A. C., Dose, A. C., Burnside, B. (2003). Localization of a Class III Myosin to Filopodia Tips in Transfected HeLa Cells Requires an Actin-binding Site in its Tail Domain. Mol. Biol. Cell 14: 4173-4180 [Abstract] [Full Text]
Goodman, A., Goode, B. L., Matsudaira, P., Fink, G. R. (2003). The Saccharomyces cerevisiae Calponin/Transgelin Homolog Scp1 Functions with Fimbrin to Regulate Stability and Organization of the Actin Cytoskeleton. Mol. Biol. Cell 14: 2617-2629 [Abstract] [Full Text]
Humphries, C. L., Balcer, H. I., D'Agostino, J. L., Winsor, B., Drubin, D. G., Barnes, G., Andrews, B. J., Goode, B. L. (2002). Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. JCB 159: 993-1004 [Abstract] [Full Text]
Spoerl, Z., Stumpf, M., Noegel, A. A., Hasse, A. (2002). Oligomerization, F-actin Interaction, and Membrane Association of the Ubiquitous Mammalian Coronin 3 Are Mediated by Its Carboxyl Terminus. J. Biol. Chem. 277: 48858-48867 [Abstract] [Full Text]
Sklyarova, T., De Corte, V., Meerschaert, K., Devriendt, L., Vanloo, B., Bailey, J., Cook, L. J., Goethals, M., Van Damme, J., Puype, M., Vandekerckhove, J., Gettemans, J. (2002). Fragmin60 Encodes an Actin-binding Protein with a C2 Domain and Controls Actin Thr-203 Phosphorylation in Physarum Plasmodia and Sclerotia. J. Biol. Chem. 277: 39840-39849 [Abstract] [Full Text]
Engqvist-Goldstein, A. E.Y., Warren, R. A., Kessels, M. M., Keen, J. H., Heuser, J., Drubin, D. G. (2001). The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. JCB 154: 1209-1224 [Abstract] [Full Text]
Caron, J. M., Vega, L. R., Fleming, J., Bishop, R., Solomon, F. (2001). Single Site alpha -Tubulin Mutation Affects Astral Microtubules and Nuclear Positioning during Anaphase in Saccharomyces cerevisiae: Possible Role for Palmitoylation of alpha -Tubulin. Mol. Biol. Cell 12: 2672-2687 [Abstract] [Full Text]
Drees, B. L., Sundin, B., Brazeau, E., Caviston, J. P., Chen, G.-C., Guo, W., Kozminski, K. G., Lau, M. W., Moskow, J. J., Tong, A., Schenkman, L. R., McKenzie, A. III, Brennwald, P., Longtine, M., Bi, E., Chan, C., Novick, P., Boone, C., Pringle, J. R., Davis, T. N., Fields, S., Drubin, D. G. (2001). A protein interaction map for cell polarity development. JCB 154: 549-576 [Abstract] [Full Text]
Goode, B. L., Rodal, A. A., Barnes, G., Drubin, D. G. (2001). Activation of the Arp2/3 Complex by the Actin Filament Binding Protein Abp1p. JCB 153: 627-634 [Abstract] [Full Text]
May, R., Machesky, L. (2001). Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114: 1061-1077 [Abstract]
Fuchs, E., Karakesisoglou, I. (2001). Bridging cytoskeletal intersections. Genes Dev. 15: 1-14 [Full Text]
Ouellet, F., Carpentier, E., Cope, M. J. T.V., Monroy, A. F., Sarhan, F. (2001). Regulation of a Wheat Actin-Depolymerizing Factor during Cold Acclimation. Plant Physiol. 125: 360-368 [Abstract] [Full Text]
Waterman-Storer, C., Duey, D. Y., Weber, K. L., Keech, J., Cheney, R. E., Salmon, E.D., Bement, W. M. (2000). Microtubules Remodel Actomyosin Networks in Xenopus Egg Extracts via Two Mechanisms of F-Actin Transport. JCB 150: 361-376 [Abstract] [Full Text]
Pruyne, D, Bretscher, A (2000). Polarization of cell growth in yeast. J. Cell Sci. 113: 571-585 [Abstract]
Kessels, M. M., Engqvist-Goldstein, A. E. Y., Drubin, D. G. (2000). Association of Mouse Actin-binding Protein 1 (mAbp1/SH3P7), an Src Kinase Target, with Dynamic Regions of the Cortical Actin Cytoskeleton in Response to Rac1 Activation. Mol. Biol. Cell 11: 393-412 [Abstract] [Full Text]
Engqvist-Goldstein, A. E.Y., Kessels, M. M., Chopra, V. S., Hayden, M. R., Drubin, D. G. (1999). An Actin-Binding Protein of the Sla2/Huntingtin Interacting Protein 1 Family Is a Novel Component of Clathrin-Coated Pits and Vesicles. JCB 147: 1503-1518 [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]
Fujiwara, T., Tanaka, K., Inoue, E., Kikyo, M., Takai, Y. (1999). Bni1p Regulates Microtubule-Dependent Nuclear Migration through the Actin Cytoskeleton in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 8016-8027 [Abstract] [Full Text]
Rappleye, C. A., Paredez, A. R., Smith, C. W., McDonald, K. L., Aroian, R. V. (1999). The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode Caenorhabditis elegans. Genes Dev. 13: 2838-2851 [Abstract] [Full Text]
Theesfeld, C. L., Irazoqui, J. E., Bloom, K., Lew, D. J. (1999). The Role of Actin in Spindle Orientation Changes during the Saccharomyces cerevisiae Cell Cycle. JCB 146: 1019-1032 [Abstract] [Full Text]
Konzok, A., Weber, I., Simmeth, E., Hacker, U., Maniak, M., Muller-Taubenberger, A. (1999). Daip1, a Dictyostelium Homologue of the Yeast Actin-Interacting Protein 1, Is Involved in Endocytosis, Cytokinesis, and Motility. JCB 146: 453-464 [Abstract] [Full Text]
Rochlin, M. W., Dailey, M. E., Bridgman, P. C. (1999). Polymerizing Microtubules Activate Site-directed F-Actin Assembly in Nerve Growth Cones. Mol. Biol. Cell 10: 2309-2327 [Abstract] [Full Text]
Rodal, A. A., Tetreault, J. W., Lappalainen, P., Drubin, D. G., Amberg, D. C. (1999). Aip1p Interacts with Cofilin to Disassemble Actin Filaments. JCB 145: 1251-1264 [Abstract] [Full Text]
Nakamura, T., Takeuchi, K., Muraoka, S., Takezoe, H., Takahashi, N., Mori, N. (1999). A Neurally Enriched Coronin-like Protein, ClipinC, Is a Novel Candidate for an Actin Cytoskeleton-Cortical Membrane-linking Protein. J. Biol. Chem. 274: 13322-13327 [Abstract] [Full Text]
Cope, M.J. T.V., Yang, S., Shang, C., Drubin, D. G. (1999). Novel Protein Kinases Ark1p and Prk1p Associate with and Regulate the Cortical Actin Cytoskeleton in Budding Yeast. JCB 144: 1203-1218 [Abstract] [Full Text]
Lee, L., Klee, S. K., Evangelista, M., Boone, C., Pellman, D. (1999). Control of Mitotic Spindle Position by the Saccharomyces cerevisiae Formin Bni1p. JCB 144: 947-961 [Abstract] [Full Text]
Mishima, M, Nishida, E (1999). Coronin localizes to leading edges and is involved in cell spreading and lamellipodium extension in vertebrate cells. J. Cell Sci. 112: 2833-2842 [Abstract]
Sider, J., Mandato, C., Weber, K., Zandy, A., Beach, D, Finst, R., Skoble, J, Bement, W. (1999). Direct observation of microtubule-f-actin interaction in cell free lysates. J. Cell Sci. 112: 1947-1956 [Abstract]