Dynamics of multiple nuclei in Ashbya gossypii hyphae depend on the control of cytoplasmic microtubules length by Bik1, Kip2, Kip3, and not on a capture/shrinkage mechanism

Molecular Biology of the Cell

Volumn 21, Issue 21, 2010, Pages 3680-3692

  Grava, Sandrine ^a   Philippsen, Peter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; PROTEIN BIK 1; PROTEIN KIP 3; PROTIEN KIP 2; UNCLASSIFIED DRUG;

ARTICLE; ASHBYA GOSSYPII; BUDDING; CELL GROWTH; CELL MOTION; CELL SIZE; CYTOPLASM; CYTOSKELETON; DEPOLYMERIZATION; FUNGUS HYPHAE; INTRANUCLEAR SPACE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; YEAST;

ANIMALS; ARVICOLINAE; CARRIER PROTEINS; CELL MEMBRANE; CELL NUCLEUS; CYTOPLASM; EREMOTHECIUM; HYPHAE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; SACCHAROMYCETALES;

EREMOTHECIUM GOSSYPII; SACCHAROMYCETALES;

EID: 78149288705     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-06-0527     Document Type: Article

References (48)

1. Adames, N. R., and Cooper, J. A. (2000). Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J. Cell Biol. 149, 863-874.
2. Ahringer, J. (2003). Control of cell polarity and mitotic spindle positioning in animal cells. Curr. Opin. Cell Biol. 15, 73-81.
3. Akhmanova, A., and Steinmetz, M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309-322.
4. Alberti-Segui, C., Dietrich, F., Altmann-Johl, R., Hoepfner, D., and 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.
5. Ayad-Durieux, Y., Knechtle, P., Goff, S., Dietrich, F., and Philippsen, P. (2000). A PAK-like protein kinase is required for maturation of young hyphae and septation in the filamentous ascomycete Ashbya gossypii. J. Cell Sci. 113, 4563-4575.
6. Berlin, V., Styles, C. A., and Fink, G. R. (1990). BIK1, a protein required for microtubule function during mating and mitosis in Saccharomyces cerevisiae, colocalizes with tubulin. J. Cell Biol. 111, 2573-2586.
7. Bode, C. J., Gupta, M. L., Suprenant, K. A., and Himes, R. H. (2003). The two alpha-tubulin isotypes in budding yeast have opposing effects on microtubule dynamics in vitro. EMBO Rep. 4, 94-99.
8. Brunner, D., and Nurse, P. (2000). CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102, 695-704.
9. Carvalho, P., Gupta, M. L., Jr., Hoyt, M. A., and Pellman, D. (2004). Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell 6, 815-829.
10. Carvalho, P., Tirnauer, J. S., and Pellman, D. (2003). Surfing on microtubule ends. Trends Cell Biol. 13, 229-237.
11. Caudron, F., Andrieux, A., Job, D., and Boscheron, C. (2008). A new role for kinesin-directed transport of Bik1p (CLIP-170) in Saccharomyces cerevisiae. J. Cell Sci. 121, 1506-1513.
12. Coquelle, F. M., et al. (2002). LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol. Cell. Biol. 22, 3089-3102.
13. Desai, A., and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell. Dev. Biol. 13, 83-117.
14. DeZwaan, T. M., Ellingson, E., Pellman, D., and Roof, D. M. (1997). Kinesinrelated KIP3 of Saccharomyces cerevisiae is required for a distinct step in nuclear migration. J. Cell Biol. 138, 1023-1040.
15. Dietrich, F. S., et al. (2004). The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304, 304-307.
16. Efimov, V. P., Zhang, J., and Xiang, X. (2006). CLIP-170 homologue and NUDE play overlapping roles in NUDF localization in Aspergillus nidulans. Mol. Biol. Cell 17, 2021-2034.
17. Galjart, N., and Perez, F. (2003). A plus-end raft to control microtubule dynamics and function. Curr. Opin. Cell Biol. 15, 48-53.
18. Gardner, M. K., et al. (2008). Chromosome congression by kinesin-5 motormediated disassembly of longer kinetochore microtubules. Cell 135, 894-906.
19. Gladfelter, A., and Berman, J. (2009). Dancing genomes: fungal nuclear positioning. Nat. Rev. Microbiol. 7, 875-886.
20. Gladfelter, A. S., Hungerbuehler, A. K., and Philippsen, P. (2006). Asynchronous nuclear division cycles in multinucleated cells. J. Cell Biol. 172, 347-362.
21. Gupta, M. L., Jr., Carvalho, P., Roof, D. M., and Pellman, D. (2006). Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle. Nat. Cell Biol. 8, 913-923.
22. Hammond, J. W., Cai, D., and Verhey, K. J. (2008). Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20, 71-76.
23. Helfer, H., and Gladfelter, A. S. (2006). AgSwe1p regulates mitosis in response to morphogenesis and nutrients in multinucleated Ashbya gossypii cells. Mol. Biol. Cell 17, 4494-4512.
24. Howard, J., and Hyman, A. A. (2009). Growth, fluctuation and switching at microtubule plus ends. Nat. Rev. Mol. Cell Biol. 10, 569-574.
25. Kaufmann, A. (2009). A plasmid collection for PCR-based gene targeting in the filamentous ascomycete Ashbya gossypii. Fungal Genet. Biol. 46, 595-603.
26. Kohli, M., Galati, V., Boudier, K., Roberson, R. W., and Philippsen, P. (2008). Growth-speed-correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. J. Cell Sci. 121, 3878-3889.
27. Komarova, Y. A., Akhmanova, A. S., Kojima, S., Galjart, N., and Borisy, G. G. (2002). Cytoplasmic linker proteins promote microtubule rescue in vivo. J. Cell Biol. 159, 589-599.
28. Kusch, J., Meyer, A., Snyder, M. P., and Barral, Y. (2002). Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev. 16, 1627-1639.
29. Lang, C., Grava, S., Finlayson, M., Trimble, R., Philippsen, P., and Jaspersen, S. L. (2010b). Structural mutants of the spindle pole body cause distinct alteration of cytoplasmic microtubules and nuclear dynamics in multinucleated hyphae. Mol. Biol. Cell 21, 753-766.
30. Lang, C., Grava, S., van den Hoorn, T., Trimble, R., Philippsen, P., and Jaspersen, S. L. (2010a). Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii. Mol. Biol. Cell 21, 18-28.
31. Lee, L., Klee, S. K., Evangelista, M., Boone, C., and Pellman, D. (1999). Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p. J. Cell Biol. 144, 947-961.
32. Lee, L., Tirnauer, J. S., Li, J., Schuyler, S. C., Liu, J. Y., and Pellman, D. (2000). Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science 287, 2260-2262.
33. Lee, W. L., Oberle, J. R., and Cooper, J. A. (2003). The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J. Cell Biol. 160, 355-364.
34. Lin, H., de Carvalho, P., Kho, D., Tai, C. Y., Pierre, P., Fink, G. R., and Pellman, D. (2001). Polyploids require Bik1 for kinetochore-microtubule attachment. J. Cell Biol. 155, 1173-1184.
35. Miller, R. K., Heller, K. K., Frisen, L., Wallack, D. L., Loayza, D., Gammie, A. E., and Rose, M. D. (1998). The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast. Mol. Biol. Cell 9, 2051-2068.
36. Moore, A., and Wordeman, L. (2004). The mechanism, function and regulation of depolymerizing kinesins during mitosis. Trends Cell Biol. 14, 537-546.
37. Perez, F., Diamantopoulos, G. S., Stalder, R., and Kreis, T. E. (1999). CLIP-170 highlights growing microtubule ends in vivo. Cell 96, 517-527.
38. Shaw, S. L., Yeh, E., Maddox, P., Salmon, E. D., and Bloom, K. (1997). Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J. Cell Biol. 139, 985-994.
39. Sheeman, B., Carvalho, P., Sagot, I., Geiser, J., Kho, D., Hoyt, M. A., and Pellman, D. (2003). Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr. Biol. 13, 364-372.
40. Slep, K. C. (2010). Structural and mechanistic insights into microtubule endbinding proteins. Curr. Opin. Cell Biol. 22, 88-95.
41. Sproul, L. R., Anderson, D. J., Mackey, A. T., Saunders, W. S., and Gilbert, S. P. (2005). Cik1 targets the minus-end kinesin depolymerase kar3 to microtubule plus ends. Curr. Biol. 15, 1420-1427.
42. Tirnauer, J. S., O'Toole, E., Berrueta, L., Bierer, B. E., and Pellman, D. (1999). Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 145, 993-1007. (Pubitemid 29270058)
43. van der Vaart, B., Akhmanova, A., and Straube, A. (2009). Regulation of microtubule dynamic instability. Biochem. Soc. Trans. 37, 1007-1013.
44. Varga, V., Helenius, J., Tanaka, K., Hyman, A. A., Tanaka, T. U., and Howard, J. (2006). Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 8, 957-962.
45. Varga, V., Leduc, C., Bormuth, V., Diez, S., and Howard, J. (2009). Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization. Cell 138, 1174-1183.
46. Wendland, J., Ayad-Durieux, Y., Knechtle, P., Rebischung, C., and Philippsen, P. (2000). PCR-based gene targeting in the filamentous fungus Ashbya gossypii. Gene 242, 381-391.
47. Wendland, J., and Walther, A. (2005). Ashbya gossypii: a model for fungal developmental biology. Nat. Rev. Microbiol. 3, 421-429.
48. Wolyniak, M. J., Blake-Hodek, K., Kosco, K., Hwang, E., You, L., and Huffaker, T. C. (2006). The regulation of microtubule dynamics in Saccharomyces cerevisiae by three interacting plus-end tracking proteins. Mol. Biol. Cell 17, 2789-2798.