J. Cell Biol.
© The Rockefeller University Press
0021-9525/97/09/1023/18 $2.00
Volume 138, Number 5, September 8, 1997 1023-1040

Kinesin-related KIP3 of Saccharomyces cerevisiae Is Required for a Distinct Step in Nuclear Migration

Todd M. DeZwaan,^* Eric Ellingson, David Pellman, and David M. Roof^*

^* Department of Physiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6085; and  Departments of Pediatric Oncology, The Dana-Farber Cancer Institute, and Pediatric Hematology, The Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115

Spindle orientation and nuclear migration are crucial events in cell growth and differentiation of many eukaryotes. Here we show that KIP3, the sixth and final kinesin-related gene in Saccharomyces cerevisiae, is required for migration of the nucleus to the bud site in preparation for mitosis. The position of the nucleus in the cell and the orientation of the mitotic spindle was examined by microscopy of fixed cells and by time-lapse microscopy of individual live cells. Mutations in KIP3 and in the dynein heavy chain gene defined two distinct phases of nuclear migration: a KIP3-dependent movement of the nucleus toward the incipient bud site and a dynein-dependent translocation of the nucleus through the bud neck during anaphase. Loss of KIP3 function disrupts the unidirectional movement of the nucleus toward the bud and mitotic spindle orientation, causing large oscillations in nuclear position. The oscillatory motions sometimes brought the nucleus in close proximity to the bud neck, possibly accounting for the viability of a kip3 null mutant. The kip3 null mutant exhibits normal translocation of the nucleus through the neck and normal spindle pole separation kinetics during anaphase. Simultaneous loss of KIP3 and kinesin-related KAR3 function, or of KIP3 and dynein function, is lethal but does not block any additional detectable movement. This suggests that the lethality is due to the combination of sequential and possibly overlapping defects. Epitope-tagged Kip3p localizes to astral and central spindle microtubules and is also present throughout the cytoplasm and nucleus.

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

This article has been cited by other articles:

• Grissom, P. M., Fiedler, T., Grishchuk, E. L., Nicastro, D., West, R. R., Richard McIntosh, J. (2009). Kinesin-8 from Fission Yeast: A Heterodimeric, Plus-End-directed Motor that Can Couple Microtubule Depolymerization to Cargo Movement. Mol. Biol. Cell 20: 963-972 [Abstract] [Full Text]  
• Khmelinskii, A., Lawrence, C., Roostalu, J., Schiebel, E. (2007). Cdc14-regulated midzone assembly controls anaphase B. JCB 177: 981-993 [Abstract] [Full Text]  
• Haarer, B. K., Helfant, A. H., Nelson, S. A., Cooper, J. A., Amberg, D. C. (2007). Stable Preanaphase Spindle Positioning Requires Bud6p and an Apparent Interaction between the Spindle Pole Bodies and the Neck. Eukaryot Cell 6: 797-807 [Abstract] [Full Text]  
• Yamashita, A., Yamamoto, M. (2006). Fission Yeast Num1p Is a Cortical Factor Anchoring Dynein and Is Essential for the Horse-Tail Nuclear Movement During Meiotic Prophase. Genetics 173: 1187-1196 [Abstract] [Full Text]  
• Tytell, J. D., Sorger, P. K. (2006). Analysis of kinesin motor function at budding yeast kinetochores.. JCB 172: 861-874 [Abstract] [Full Text]  
• Clark, S. W., Rose, M. D. (2006). Arp10p Is a Pointed-End-associated Component of Yeast Dynactin. Mol. Biol. Cell 17: 738-748 [Abstract] [Full Text]  
• Moore, J. K., D'Silva, S., Miller, R. K. (2006). The CLIP-170 Homologue Bik1p Promotes the Phosphorylation and Asymmetric Localization of Kar9p. Mol. Biol. Cell 17: 178-191 [Abstract] [Full Text]  
• Clark, S. W., Rose, M. D. (2005). Alanine Scanning of Arp1 Delineates a Putative Binding Site for Jnm1/Dynamitin and Nip100/p150Glued. Mol. Biol. Cell 16: 3999-4012 [Abstract] [Full Text]  
• Schmidt, M. (2004). Survival and cytokinesis of Saccharomyces cerevisiae in the absence of chitin. Microbiology 150: 3253-3260 [Abstract] [Full Text]  
• Whited, J. L., Cassell, A., Brouillette, M., Garrity, P. A. (2004). Dynactin is required to maintain nuclear position within postmitotic Drosophila photoreceptor neurons. Development 131: 4677-4686 [Abstract] [Full Text]  
• Fraschini, R., Bilotta, D., Lucchini, G., Piatti, S. (2004). Functional Characterization of Dma1 and Dma2, the Budding Yeast Homologues of Schizosaccharomyces pombe Dma1 and Human Chfr. Mol. Biol. Cell 15: 3796-3810 [Abstract] [Full Text]  
• Rischitor, P. E., Konzack, S., Fischer, R. (2004). The Kip3-Like Kinesin KipB Moves along Microtubules and Determines Spindle Position during Synchronized Mitoses in Aspergillus nidulans Hyphae. Eukaryot Cell 3: 632-645 [Abstract] [Full Text]  
• Badin-Larcon, A. C., Boscheron, C., Soleilhac, J. M., Piel, M., Mann, C., Denarier, E., Fourest-Lieuvin, A., Lafanechere, L., Bornens, M., Job, D. (2004). From the Cover: Suppression of nuclear oscillations in Saccharomyces cerevisiae expressing Glu tubulin. Proc. Natl. Acad. Sci. USA 101: 5577-5582 [Abstract] [Full Text]  
• Paluh, J. L., Killilea, A. N., Detrich, H. W. 3rd, Downing, K. H. (2004). Meiosis-specific Failure of Cell Cycle Progression in Fission Yeast by Mutation of a Conserved {beta}-Tubulin Residue. Mol. Biol. Cell 15: 1160-1171 [Abstract] [Full Text]  
• Gandhi, R., Bonaccorsi, S., Wentworth, D., Doxsey, S., Gatti, M., Pereira, A. (2004). The Drosophila Kinesin-like Protein KLP67A Is Essential for Mitotic and Male Meiotic Spindle Assembly. Mol. Biol. Cell 15: 121-131 [Abstract] [Full Text]  
• Yamamoto, A., Hiraoka, Y. (2003). Cytoplasmic dynein in fungi: insights from nuclear migration. J. Cell Sci. 116: 4501-4512 [Abstract] [Full Text]  
• Wright, A. J., Hunter, C. P. (2003). Mutations in a {beta}-Tubulin Disrupt Spindle Orientation and Microtubule Dynamics in the Early Caenorhabditis elegans Embryo. Mol. Biol. Cell 14: 4512-4525 [Abstract] [Full Text]  
• Lee, K., Neigeborn, L., Kaufman, R. J. (2003). The Unfolded Protein Response Is Required for Haploid Tolerance in Yeast. J. Biol. Chem. 278: 11818-11827 [Abstract] [Full Text]  
• Lee, W.-L., Oberle, J. R., Cooper, J. A. (2003). The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. JCB 160: 355-364 [Abstract] [Full Text]  
• Kusch, J., Meyer, A., Snyder, M. P., Barral, Y. (2002). Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev. 16: 1627-1639 [Abstract] [Full Text]  
• West, R. R., Malmstrom, T., Troxell, C. L., McIntosh, J. R. (2001). Two Related Kinesins, klp5+ and klp6+, Foster Microtubule Disassembly and Are Required for Meiosis in Fission Yeast. Mol. Biol. Cell 12: 3919-3932 [Abstract] [Full Text]  
• Schaerer, F., Morgan, G., Winey, M., Philippsen, P. (2001). Cnm67p Is a Spacer Protein of the Saccharomyces cerevisiae Spindle Pole Body Outer Plaque. Mol. Biol. Cell 12: 2519-2533 [Abstract] [Full Text]  
• Miki, H., Setou, M., Kaneshiro, K., Hirokawa, N. (2001). All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. USA 98: 7004-7011 [Abstract] [Full Text]  
• Farkasovsky, M., Kuntzel, H. (2001). Cortical Num1p Interacts with the Dynein Intermediate Chain Pac11p and Cytoplasmic Microtubules in Budding Yeast. JCB 152: 251-262 [Abstract] [Full Text]  
• Alberti-Segui, C, Dietrich, F, Altmann-Johl, R, Hoepfner, D, Philippsen, P (2001). Cytoplasmic dynein is required to oppose the force that moves nuclei towards the hyphal tip in the filamentous ascomycete Ashbya gossypii. J. Cell Sci. 114: 975-986 [Abstract]  
• Schuyler, S., Pellman, D (2001). Search, capture and signal: games microtubules and centrosomes play. J. Cell Sci. 114: 247-255 [Abstract]  
• Heil-Chapdelaine, R. A., Oberle, J. R., Cooper, J. A. (2000). The Cortical Protein Num1p Is Essential for Dynein-dependent Interactions of Microtubules with the Cortex. JCB 151: 1337-1344 [Abstract] [Full Text]  
• Miller, R. K., Cheng, S.-C., Rose, M. D. (2000). Bim1p/Yeb1p Mediates the Kar9p-dependent Cortical Attachment of Cytoplasmic Microtubules. Mol. Biol. Cell 11: 2949-2959 [Abstract] [Full Text]  
• Adames, N. R., Cooper, J. A. (2000). Microtubule Interactions with the Cell Cortex Causing Nuclear Movements in Saccharomyces cerevisiae. JCB 149: 863-874 [Abstract] [Full Text]  
• O'Connell, C. B., Wang, Y.-l. (2000). Mammalian Spindle Orientation and Position Respond to Changes in Cell Shape in a Dynein-dependent Fashion. Mol. Biol. Cell 11: 1765-1774 [Abstract] [Full Text]  
• Hoepfner, D., Brachat, A., Philippsen, P. (2000). Time-Lapse Video Microscopy Analysis Reveals Astral Microtubule Detachment in the Yeast Spindle Pole Mutant cnm67. Mol. Biol. Cell 11: 1197-1211 [Abstract] [Full Text]  
• Paluh, J. L., Nogales, E., Oakley, B. R., McDonald, K., Pidoux, A. L., Cande, W. Z. (2000). A Mutation in gamma -Tubulin Alters Microtubule Dynamics and Organization and Is Synthetically Lethal with the Kinesin-like Protein Pkl1p. Mol. Biol. Cell 11: 1225-1239 [Abstract] [Full Text]  
• Lee, L., Tirnauer, J. S., Li, J., Schuyler, S. C., Liu, J. Y., Pellman, D. (2000). Positioning of the Mitotic Spindle by a Cortical-Microtubule Capture Mechanism. Science 287: 2260-2262 [Abstract] [Full Text]  
• Heil-Chapdelaine, R. A., Tran, N. K., Cooper, J. A. (2000). Dynein-dependent Movements of the Mitotic Spindle in Saccharomyces cerevisiae Do Not Require Filamentous Actin. Mol. Biol. Cell 11: 863-872 [Abstract] [Full Text]  
• Hunter, A., Wordeman, L (2000). How motor proteins influence microtubule polymerization dynamics. J. Cell Sci. 113: 4379-4389 [Abstract]  
• Vogel, J, Snyder, M (2000). The carboxy terminus of Tub4p is required for gamma-tubulin function in budding yeast. J. Cell Sci. 113: 3871-3882 [Abstract]  
• Infante, A., Stein, M., Zhai, Y, Borisy, G., Gundersen, G. (2000). Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell Sci. 113: 3907-3919 [Abstract]  
• 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]  
• Cottingham, F. R., Gheber, L., Miller, D. L., Hoyt, M. A. (1999). Novel Roles for Saccharomyces cerevisiae Mitotic Spindle Motors. JCB 147: 335-350 [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]  
• 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]  
• Yamamoto, A., West, R. R., McIntosh, J. R., Hiraoka, Y. (1999). A Cytoplasmic Dynein Heavy Chain Is Required for Oscillatory Nuclear Movement of Meiotic Prophase and Efficient Meiotic Recombination in Fission Yeast. JCB 145: 1233-1250 [Abstract] [Full Text]  
• Tirnauer, J. S., O'Toole, E., Berrueta, L., Bierer, B. E., Pellman, D. (1999). Yeast Bim1p Promotes the G1-specific Dynamics of Microtubules. JCB 145: 993-1007 [Abstract] [Full Text]  
• Manning, B. D., Barrett, J. G., Wallace, J. A., Granok, H., Snyder, M. (1999). Differential Regulation of the Kar3p Kinesin-related Protein by Two Associated Proteins, Cik1p and Vik1p. JCB 144: 1219-1233 [Abstract] [Full Text]  
• Heil-Chapdelaine, R. A., Adames, N. R., Cooper, J. A. (1999). Formin' the Connection between Microtubules and the Cell Cortex. JCB 144: 809-811 [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]  
• Miller, R. K., Matheos, D., Rose, M. D. (1999). The Cortical Localization of the Microtubule Orientation Protein, Kar9p, Is Dependent upon Actin and Proteins Required for Polarization. JCB 144: 963-975 [Abstract] [Full Text]  
• Straight, A. F., Sedat, J. W., Murray, A. W. (1998). Time-Lapse Microscopy Reveals Unique Roles for Kinesins during Anaphase in Budding Yeast. JCB 143: 687-694 [Abstract] [Full Text]  
• Segal, M., Clarke, D. J., Reed, S. I. (1998). Clb5-associated Kinase Activity is Required Early in the Spindle Pathway for Correct Preanaphase Nuclear Positioning in Saccharomyces cerevisiae. JCB 143: 135-145 [Abstract] [Full Text]  
• Miller, R. K., Heller, K. K., Frisèn, L., Wallack, D. L., Loayza, D., Gammie, A. E., Rose, M. D. (1998). The Kinesin-related Proteins, Kip2p and Kip3p, Function Differently in Nuclear Migration in Yeast. Mol. Biol. Cell 9: 2051-2068 [Abstract] [Full Text]  
• de Hostos, E. L., McCaffrey, G., Sucgang, R., Pierce, D. W., Vale, R. D. (1998). A Developmentally Regulated Kinesin-related Motor Protein from Dictyostelium discoideum. Mol. Biol. Cell 9: 2093-2106 [Abstract] [Full Text]  
• Kahana, J. A., Schlenstedt, G., Evanchuk, D. M., Geiser, J. R., Hoyt, M. A., Silver, P. A. (1998). The Yeast Dynactin Complex Is Involved in Partitioning the Mitotic Spindle between Mother and Daughter Cells during Anaphase B. Mol. Biol. Cell 9: 1741-1756 [Abstract] [Full Text]  
• Wigge, P. A., Jensen, O. N., Holmes, S., Soues, S., Mann, M., Kilmartin, J. V. (1998). Analysis of the Saccharomyces Spindle Pole by Matrix-assisted Laser Desorption/Ionization (MALDI) Mass Spectrometry. JCB 141: 967-977 [Abstract] [Full Text]  
• Efimov, V. P., Morris, N. R. (1998). A Screen for Dynein Synthetic Lethals in Aspergillus nidulans Identifies Spindle Assembly Checkpoint Genes and Other Genes Involved in Mitosis. Genetics 149: 101-116 [Abstract] [Full Text]  
• Brachat, A., Kilmartin, J. V., Wach, A., Philippsen, P. (1998). Saccharomyces cerevisiae Cells with Defective Spindle Pole Body Outer Plaques Accomplish Nuclear Migration via Half-Bridge-organized Microtubules. Mol. Biol. Cell 9: 977-991 [Abstract] [Full Text]  
• Lillie, S.H., Brown, S.S. (1998). Smy1p, a Kinesin-related Protein That Does Not Require Microtubules. JCB 140: 873-883 [Abstract] [Full Text]  
• Miller, R. K., Rose, M. D. (1998). Kar9p Is a Novel Cortical Protein Required for Cytoplasmic Microtubule Orientation in Yeast. JCB 140: 377-390 [Abstract] [Full Text]  
• Soues, S, Adams, I. (1998). SPC72: a spindle pole component required for spindle orientation in the yeast Saccharomyces cerevisiae. J. Cell Sci. 111: 2809-2818 [Abstract]  
• Reinsch, S, Gonczy, P (1998). Mechanisms of nuclear positioning. J. Cell Sci. 111: 2283-2295 [Abstract]  
• Compton, D. (1998). Focusing on spindle poles. J. Cell Sci. 111: 1477-1481 [Abstract]  
• Huyett, A, Kahana, J, Silver, P, Zeng, X, Saunders, W. (1998). The Kar3p and Kip2p motors function antagonistically at the spindle poles to influence cytoplasmic microtubule numbers. J. Cell Sci. 111: 295-301 [Abstract]  
• Hoyt, M. A., Hyman, A. A., Bahler, M. (1997). Motor proteins of the eukaryotic cytoskeleton. Proc. Natl. Acad. Sci. USA 94: 12747-12748 [Full Text]  
• Stearns, T. (1997). Motoring to the Finish: Kinesin and Dynein Work Together to Orient the Yeast Mitotic Spindle. JCB 138: 957-960 [Full Text]  
• Cottingham, F. R., Hoyt, M. A. (1997). Mitotic Spindle Positioning in Saccharomyces cerevisiae Is Accomplished by Antagonistically Acting Microtubule Motor Proteins. JCB 138: 1041-1053 [Abstract] [Full Text]  
• Hoepfner, D., Schaerer, F., Brachat, A., Wach, A., Philippsen, P. (2002). Reorientation of Mispositioned Spindles in Short Astral Microtubule Mutant spc72Delta Is Dependent on Spindle Pole Body Outer Plaque and Kar3 Motor Protein. Mol. Biol. Cell 13: 1366-1380 [Abstract] [Full Text]  

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