Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae

doi:10.1083/jcb.135.6.1535

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Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae

KL Hill, NL Catlett and LS Weisman
Department of Biochemistry, University of Iowa, Iowa City 52242, USA.

During cell division, cytoplasmic organelles are not synthesized de novo, rather they are replicated and partitioned between daughter cells. Partitioning of the vacuole in the budding yeast Saccharomyces cerevisiae is coordinated with the cell cycle and involves a dramatic translocation of a portion of the parental organelle from the mother cell into the bud. While the molecular mechanisms that mediate this event are unknown, the vacuole's rapid and directed movements suggest cytoskeleton involvement. To identify cytoskeletal components that function in this process, vacuole inheritance was examined in a collection of actin mutants. Six strains were identified as being defective in vacuole inheritance. Tetrad analysis verified that the defect cosegregates with the mutant actin gene. One strain with a deletion in a myosin-binding region was analyzed further. The vacuole inheritance defect in this strain appears to result from the loss of a specific actin function; the actin cytoskeleton is intact and protein targeting to the vacuole is normal. Consistent with these findings, a mutation in the actin-binding domain of Myo2p, a class V unconventional myosin, abolishes vacuole inheritance. This suggests that Myo2p serves as a molecular motor for vacuole transport along actin filaments. The location of actin and Myo2p relative to the vacuole membrane is consistent with this model. Additional studies suggest that the actin filaments used for vacuole transport are dynamic, and that profilin plays a critical role in regulating their assembly. These results present the first demonstration that specific cytoskeletal proteins function in vacuole inheritance.
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Isgandarova, S., Jones, L., Forsberg, D., Loncar, A., Dawson, J., Tedrick, K., Eitzen, G. (2007). Stimulation of Actin Polymerization by Vacuoles via Cdc42p-dependent Signaling. J. Biol. Chem. 282: 30466-30475 [Abstract] [Full Text]
Park, H.-O., Bi, E. (2007). Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond. Microbiol. Mol. Biol. Rev. 71: 48-96 [Abstract] [Full Text]
Huckaba, T. M., Lipkin, T., Pon, L. A. (2006). Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 175: 957-969 [Abstract] [Full Text]
McKane, M., Wen, K.-K., Meyer, A., Rubenstein, P. A. (2006). Effect of the Substitution of Muscle Actin-specific Subdomain 1 and 2 Residues in Yeast Actin on Actin Function. J. Biol. Chem. 281: 29916-29928 [Abstract] [Full Text]
Bryan, K. E., Wen, K.-K., Zhu, M., Rendtorff, N. D., Feldkamp, M., Tranebjaerg, L., Friderici, K. H., Rubenstein, P. A. (2006). Effects of Human Deafness {gamma}-Actin Mutations (DFNA20/26) on Actin Function. J. Biol. Chem. 281: 20129-20139 [Abstract] [Full Text]
Legesse-Miller, A., Zhang, S., Santiago-Tirado, F. H., Van Pelt, C. K., Bretscher, A. (2006). Regulated Phosphorylation of Budding Yeast's Essential Myosin V Heavy Chain, Myo2p. Mol. Biol. Cell 17: 1812-1821 [Abstract] [Full Text]
Barelle, C. J., Richard, M. L., Gaillardin, C., Gow, N. A. R., Brown, A. J. P. (2006). Candida albicans VAC8 Is Required for Vacuolar Inheritance and Normal Hyphal Branching. Eukaryot Cell 5: 359-367 [Abstract] [Full Text]
Schmitz, H.-P., Kaufmann, A., Kohli, M., Laissue, P. P., Philippsen, P. (2006). From Function to Shape: A Novel Role of a Formin in Morphogenesis of the Fungus Ashbya gossypii. Mol. Biol. Cell 17: 130-145 [Abstract] [Full Text]
McKane, M., Wen, K.-K., Boldogh, I. R., Ramcharan, S., Pon, L. A., Rubenstein, P. A. (2005). A Mammalian Actin Substitution in Yeast Actin (H372R) Causes a Suppressible Mitochondria/Vacuole Phenotype. J. Biol. Chem. 280: 36494-36501 [Abstract] [Full Text]
Fagarasanu, M., Fagarasanu, A., Tam, Y. Y. C., Aitchison, J. D., Rachubinski, R. A. (2005). Inp1p is a peroxisomal membrane protein required for peroxisome inheritance in Saccharomyces cerevisiae. J. Cell Biol. 169: 765-775 [Abstract] [Full Text]
Kraus, P. R., Nichols, C. B., Heitman, J. (2005). Calcium- and Calcineurin-Independent Roles for Calmodulin in Cryptococcus neoformans Morphogenesis and High-Temperature Growth. Eukaryot Cell 4: 1079-1087 [Abstract] [Full Text]
Pashkova, N., Catlett, N. L., Novak, J. L., Weisman, L. S. (2005). A Point Mutation in the Cargo-Binding Domain of Myosin V Affects Its Interaction with Multiple Cargoes. Eukaryot Cell 4: 787-798 [Abstract] [Full Text]
Pashkova, N., Catlett, N. L., Novak, J. L., Wu, G., Lu, R., Cohen, R. E., Weisman, L. S. (2005). Myosin V attachment to cargo requires the tight association of two functional subdomains. J. Cell Biol. 168: 359-364 [Abstract] [Full Text]
O'Sullivan, T. N., Wu, X. S., Rachel, R. A., Huang, J.-D., Swing, D. A., Matesic, L. E., Hammer, J. A. III, Copeland, N. G., Jenkins, N. A. (2004). dsu functions in a MYO5A-independent pathway to suppress the coat color of dilute mice. Proc. Natl. Acad. Sci. USA 101: 16831-16836 [Abstract] [Full Text]
Huckaba, T. M., Gay, A. C., Pantalena, L. F., Yang, H.-C., Pon, L. A. (2004). Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 167: 519-530 [Abstract] [Full Text]
Frederick, R. L., McCaffery, J. M., Cunningham, K. W., Okamoto, K., Shaw, J. M. (2004). Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 167: 87-98 [Abstract] [Full Text]
Du, Y., Ferro-Novick, S., Novick, P. (2004). Dynamics and inheritance of the endoplasmic reticulum. J. Cell Sci. 117: 2871-2878 [Abstract] [Full Text]
Estrada, P., Kim, J., Coleman, J., Walker, L., Dunn, B., Takizawa, P., Novick, P., Ferro-Novick, S. (2003). Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163: 1255-1266 [Abstract] [Full Text]
Weber, I., Gruber, C., Steinberg, G. (2003). A Class-V Myosin Required for Mating, Hyphal Growth, and Pathogenicity in the Dimorphic Plant Pathogen Ustilago maydis. Plant Cell 15: 2826-2842 [Abstract] [Full Text]
Han, B.-K., Aramayo, R., Polymenis, M. (2003). The G1 Cyclin Cln3p Controls Vacuolar Biogenesis in Saccharomyces cerevisiae. Genetics 165: 467-476 [Abstract] [Full Text]
Singer, J. M., Shaw, J. M. (2003). Mdm20 protein functions with Nat3 protein to acetylate Tpm1 protein and regulate tropomyosin-actin interactions in budding yeast. Proc. Natl. Acad. Sci. USA 100: 7644-7649 [Abstract] [Full Text]
Barelle, C. J., Bohula, E. A., Kron, S. J., Wessels, D., Soll, D. R., Schafer, A., Brown, A. J. P., Gow, N. A. R. (2003). Asynchronous Cell Cycle and Asymmetric Vacuolar Inheritance in True Hyphae of Candida albicans. Eukaryot Cell 2: 398-410 [Abstract] [Full Text]
Bretscher, A. (2003). Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell Biol. 160: 811-816 [Abstract] [Full Text]
Ishikawa, K., Catlett, N. L., Novak, J. L., Tang, F., Nau, J. J., Weisman, L. S. (2003). Identification of an organelle-specific myosin V receptor. J. Cell Biol. 160: 887-897 [Abstract] [Full Text]
Itoh, T., Watabe, A., Toh-e, A., Matsui, Y. (2002). Complex Formation with Ypt11p, a rab-Type Small GTPase, Is Essential To Facilitate the Function of Myo2p, a Class V Myosin, in Mitochondrial Distribution in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 7744-7757 [Abstract] [Full Text]
Eitzen, G., Wang, L., Thorngren, N., Wickner, W. (2002). Remodeling of organelle-bound actin is required for yeast vacuole fusion. J. Cell Biol. 158: 669-679 [Abstract] [Full Text]
Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A., Boone, C. (2002). Role of Formins in Actin Assembly: Nucleation and Barbed-End Association. Science 297: 612-615 [Abstract] [Full Text]
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Yang, H.-C., Pon, L. A. (2002). Actin cable dynamics in budding yeast. Proc. Natl. Acad. Sci. USA 99: 751-756 [Abstract] [Full Text]
Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H. F., Hettema, E. H. (2001). A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155: 979-990 [Abstract] [Full Text]
Moore, J. R., Krementsova, E. B., Trybus, K. M., Warshaw, D. M. (2001). Myosin V exhibits a high duty cycle and large unitary displacement. J. Cell Biol. 155: 625-636 [Abstract] [Full Text]
Ho, J., Bretscher, A. (2001). Ras Regulates the Polarity of the Yeast Actin Cytoskeleton through the Stress Response Pathway. Mol. Biol. Cell 12: 1541-1555 [Abstract] [Full Text]
Rossanese, O. W., Reinke, C. A., Bevis, B. J., Hammond, A. T., Sears, I. B., O'Connor, J., Glick, B. S. (2001). A Role for Actin, Cdc1p, and Myo2p in the Inheritance of Late Golgi Elements in Saccharomyces cerevisiae. J. Cell Biol. 153: 47-62 [Abstract] [Full Text]
Whitacre, J. L., Davis, D. A., Toenjes, K. A., Brower, S. M., Adams, A. E. M. (2001). Generation of an Isogenic Collection of Yeast Actin Mutants and Identification of Three Interrelated Phenotypes. Genetics 157: 533-543 [Abstract] [Full Text]
Win, T., Gachet, Y, Mulvihill, D., May, K., Hyams, J. (2001). Two type V myosins with non-overlapping functions in the fission yeast Schizosaccharomyces pombe: Myo52 is concerned with growth polarity and cytokinesis, Myo51 is a component of the cytokinetic actin ring. J. Cell Sci. 114: 69-79 [Abstract]
Ooms, L. M., McColl, B. K., Wiradjaja, F., Wijayaratnam, A. P. W., Gleeson, P., Gething, M. J., Sambrook, J., Mitchell, C. A. (2000). The Yeast Inositol Polyphosphate 5-Phosphatases Inp52p and Inp53p Translocate to Actin Patches following Hyperosmotic Stress: Mechanism for Regulating Phosphatidylinositol 4,5-Bisphosphate at Plasma Membrane Invaginations. Mol. Cell. Biol. 20: 9376-9390 [Abstract] [Full Text]
Singer, J. M., Hermann, G. J., Shaw, J. M. (2000). Suppressors of mdm20 in Yeast Identify New Alleles of ACT1 and TPM1 Predicted to Enhance Actin-Tropomyosin Interactions. Genetics 156: 523-534 [Abstract] [Full Text]
Catlett, N. L., Duex, J. E., Tang, F., Weisman, L. S. (2000). Two Distinct Regions in a Yeast Myosin-V Tail Domain Are Required for the Movement of Different Cargoes. J. Cell Biol. 150: 513-526 [Abstract] [Full Text]
Bachewich, C, Heath, I. (2000). Radial F-actin arrays precede new hypha formation in Saprolegnia: implications for establishing polar growth and regulating tip morphogenesis. J. Cell Sci. 111: 2005-2016 [Abstract]
Mayer, A., Scheglmann, D., Dove, S., Glatz, A., Wickner, W., Haas, A. (2000). Phosphatidylinositol 4,5-Bisphosphate Regulates Two Steps of Homotypic Vacuole Fusion. Mol. Biol. Cell 11: 807-817 [Abstract] [Full Text]
Beningo, K. A., Lillie, S. H., Brown, S. S. (2000). The Yeast Kinesin-related Protein Smy1p Exerts Its Effects on the Class V Myosin Myo2p via a Physical Interaction. Mol. Biol. Cell 11: 691-702 [Abstract] [Full Text]
Miller, K. E., Sheetz, M. P. (2000). Characterization of Myosin V Binding to Brain Vesicles. J. Biol. Chem. 275: 2598-2606 [Abstract] [Full Text]
Murray, J. M., Johnson, D. I. (2000). Isolation and Characterization of Nrf1p, a Novel Negative Regulator of the Cdc42p GTPase in Schizosaccharomyces pombe. Genetics 154: 155-165 [Abstract] [Full Text]
De La Cruz, E. M., Wells, A. L., Rosenfeld, S. S., Ostap, E. M., Sweeney, H. L. (1999). The kinetic mechanism of myosin V. Proc. Natl. Acad. Sci. USA 96: 13726-13731 [Abstract] [Full Text]
Schott, D., Ho, J., Pruyne, D., Bretscher, A. (1999). The COOH-Terminal Domain of Myo2p, a Yeast Myosin V, Has a Direct Role in Secretory Vesicle Targeting. J. Cell Biol. 147: 791-808 [Abstract] [Full Text]
Heimann, K., Percival, J. M., Weinberger, R., Gunning, P., Stow, J. L. (1999). Specific Isoforms of Actin-binding Proteins on Distinct Populations of Golgi-derived Vesicles. J. Biol. Chem. 274: 10743-10750 [Abstract] [Full Text]
Reck-Peterson, S. L., Novick, P. J., Mooseker, M. S. (1999). The Tail of a Yeast Class V Myosin, Myo2p, Functions as a Localization Domain. Mol. Biol. Cell 10: 1001-1017 [Abstract] [Full Text]
Esnault, K., el Moudni, B., Bouchara, J.-P., Chabasse, D., Tronchin, G. (1999). Association of a Myosin Immunoanalogue with Cell Envelopes of Aspergillus fumigatus Conidia and Its Participation in Swelling and Germination. Infect. Immun. 67: 1238-1244 [Abstract] [Full Text]
Catlett, N. L., Weisman, L. S. (1998). The terminal tail region of a yeast myosin-V mediates its attachment to vacuole membranes and sites of polarized growth. Proc. Natl. Acad. Sci. USA 95: 14799-14804 [Abstract] [Full Text]
Stevens, R. C., Davis, T. N. (1998). Mlc1p Is a Light Chain for the Unconventional Myosin Myo2p in Saccharomyces cerevisiae. J. Cell Biol. 142: 711-722 [Abstract] [Full Text]
Wang, Y.-X., Catlett, N. L., Weisman, L. S. (1998). Vac8p, a Vacuolar Protein with Armadillo Repeats, Functions in both Vacuole Inheritance and Protein Targeting from the Cytoplasm to Vacuole. J. Cell Biol. 140: 1063-1074 [Abstract] [Full Text]
Bryant, N. J., Stevens, T. H. (1998). Vacuole Biogenesis in Saccharomyces cerevisiae: Protein Transport Pathways to the Yeast Vacuole. Microbiol. Mol. Biol. Rev. 62: 230-247 [Abstract] [Full Text]
Tabb, J., Molyneaux, B., Cohen, D., Kuznetsov, S., Langford, G. (1998). Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111: 3221-3234 [Abstract]
Fleckenstein, D, Rohde, M, Klionsky, D., Rudiger, M (1998). Yel013p (Vac8p), an armadillo repeat protein related to plakoglobin and importin alpha is associated with the yeast vacuole membrane. J. Cell Sci. 111: 3109-3118 [Abstract]
Pan, X, Goldfarb, D. (1998). YEB3/VAC8 encodes a myristylated armadillo protein of the Saccharomyces cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. J. Cell Sci. 111: 2137-2147 [Abstract]
Fields, S., Conrad, M., Clarke, M (1998). The S. cerevisiae CLU1 and D. discoideum cluA genes are functional homologues that influence mitochondrial morphology and distribution. J. Cell Sci. 111: 1717-1727 [Abstract]
Geli, M., Riezman, H (1998). Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci. 111: 1031-1037 [Abstract]
Self, T, Mahony, M, Fleming, J, Walsh, J, Brown, S., Steel, K. (1998). Shaker-1 mutations reveal roles for myosin VIIA in both development and function of cochlear hair cells. Development 125: 557-566 [Abstract]
Nascimento, A. A.C., Amaral, R. G., Bizario, J. C.S., Larson, R. E., Espreafico, E. M. (1997). Subcellular Localization of Myosin-V in the B16 Melanoma Cells, a Wild-type Cell Line for the dilute Gene. Mol. Biol. Cell 8: 1971-1988 [Abstract] [Full Text]
Long, R. M., Singer, R. H., Meng, X., Gonzalez, I., Nasmyth, K., Jansen, R. (1997). Mating Type Switching in Yeast Controlled by Asymmetric Localization of ASH1 mRNA. Science 277: 383-387 [Abstract] [Full Text]
Hill, K. L., Hutchings, N. R., Grandgenett, P. M., Donelson, J. E. (2000). T Lymphocyte-triggering Factor of African Trypanosomes Is Associated with the Flagellar Fraction of the Cytoskeleton and Represents a New Family of Proteins That Are Present in Several Divergent Eukaryotes. J. Biol. Chem. 275: 39369-39378 [Abstract] [Full Text]