Dissecting the involvement of formins in Bud6p-mediated cortical capture of microtubules in S. cerevisiae

Journal of Cell Science

Volumn 121, Issue 22, 2008, Pages 3803-3814

  Delgehyr, Nathalie ^a   Lopes, Cláudia S J ^a   Moir, Catherine A ^a   Huisman, Stephen M ^a   Segal, Marisa ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cytoskeleton; Microtubules; Yeast

Indexed keywords

ACTIN; BINDING PROTEIN; BNI1 PROTEIN; BNR1 PROTEIN; BUD6P PROTEIN; FUNGAL PROTEIN; KAR9P PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL BUDDING; CELL CYCLE REGULATION; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; IN VITRO STUDY; MICROTUBULE ASSEMBLY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; SPINDLE POLE BODY;

CELL DIVISION; CELL POLARITY; CYTOSKELETAL PROTEINS; MICROFILAMENT PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 59549103134     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.036269     Document Type: Article

References (61)

1. Adams, A. E. and Pringle, J. R. (1991). Staining of actin with fluorochrome-conjugated phalloidin. Meth. Enzymol. 194, 729-731.
2. Amberg, D. C., Zahner, J. E., Mulholland, J. W., Pringle, J. R. and Botstein, D. (1997). Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol. Biol. Cell 8, 729-753.
3. Ayscough, K. R., Stryker, J., Pokala, N., Sanders, M., Crews, P. and Drubin, D. G. (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137, 399-416.
4. Beach, D. L., Thibodeaux, J., Maddox, P., Yeh, E. and Bloom, K. (2000). The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr. Biol. 10, 1497-1506.
5. Buttery, S. M., Yoshida, S. and Pellman, D. (2007). Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell 18, 1826-1838.
6. Byers, B. (1981). Cytology of the yeast life cycle. In The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance (ed. J. N. Strathern, E. W. Jones and J. R. Broach), pp. 59-96. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
7. Carminati, J. L. and Stearns, T. (1997). Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J. Cell Biol. 138, 629-641.
8. Chang, F. and Peter, M. (2003). Yeasts make their mark. Nat. Cell Biol. 5, 294-299.
9. Dong, Y., Pruyne, D. and Bretscher, A. (2003). Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J. Cell Biol. 161, 1081-1092.
10. Evangelista, M., Blundell, K., Longtine, M. S., Chow, C. J., Adames, N., Pringle, J. R., Peter, M. and Boone, C. (1997). Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118-122.
11. Evangelista, M., Pruyne, D., Amberg, D. C., Boone, C. and Bretscher, A. (2002). Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4, 260-269.
12. Faix, J. and Grosse, R. (2006). Staying in shape with formins. Dev. Cell 10, 693-706.
13. Feierbach, B., Verde, F. and Chang, F. (2004). Regulation of a formin complex by the microtubule plus end protein tea1p. J. Cell Biol. 165, 697-707.
14. Fujiwara, T., Tanaka, K., Mino, A., Kikyo, M., Takahashi, K., Shimizu, K. and Takai, Y. (1998). Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1221-1233.
15. Fujiwara, T., Tanaka, K., Inoue, E., Kikyo, M. and Takai, Y. (1999). Bni1p regulates microtubule-dependent nuclear migration through the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 8016-8027.
16. Guthrie, C. and Fink, G. R. (1991). Guide to Yeast Genetics and Molecular Biology. San Diego, CA: Academic Press.
17. Huisman, S. M. and Segal, M. (2005). Cortical capture of microtubules and spindle polarity in budding yeast: where's the catch? J. Cell Sci. 118, 463-471.
18. Huisman, S. M., Bales, O. A., Bertrand, M., Smeets, M. F., Reed, S. I. and Segal, M. (2004). Differential contribution of Bud6p and Kar9p to microtubule capture and spindle orientation in S. cerevisiae. J. Cell Biol. 167, 231-244.
19. Huisman, S. M., Smeets, M. F. and Segal, M. (2007). Phosphorylation of Spc110p by Cdc28p-Clb5p kinase contributes to correct spindle morphogenesis in S. cerevisiae. J. Cell Sci. 120, 435-446.
20. Hwang, E., Kusch, J., Barral, Y. and Huffaker, T. C. (2003). Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables. J. Cell Biol. 161, 483-488.
21. Imamura, H., Tanaka, K., Hihara, T., Umikawa, M., Kamei, T., Takahashi, K., Sasaki, T. and Takai, Y. (1997). Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 16, 2745-2755.
22. Infante, C., Ramos-Morales, F., Fedriani, C., Bornens, M. and Rios, R. M. (1999). GMAP-210, A cis-Golgi network-associated protein, is a minus end microtubule-binding protein. J. Cell Biol. 145, 83-98.
23. Irazoqui, J. E., Howell, A. S., Theesfeld, C. L. and Lew, D. J. (2005). Opposing roles for actin in Cdc42p polarization. Mol. Biol. Cell 16, 1296-1304.
24. Jaquenoud, M. and Peter, M. (2000). Gic2p may link activated Cdc42p to components involved in actin polarization, including Bni1p and Bud6p (Aip3p). Mol. Cell. Biol. 20, 6244-6258.
25. Jaspersen, S. L. and Winey, M. (2004). The budding yeast spindle pole body: structure, duplication, and function. Annu. Rev. Cell Dev. Biol. 20, 1-28.
26. Jensen, S., Segal, M., Clarke, D. J. and Reed, S. I. (2001). A novel role of the budding yeast separin Esp1 in anaphase spindle elongation: evidence that proper spindle association of Esp1 is regulated by Pds1. J. Cell Biol. 152, 27-40.
27. Jensen, S., Geymonat, M., Johnson, A. L., Segal, M. and Johnston, L. H. (2002). Spatial regulation of the guanine nucleotide exchange factor Lte1 in Saccharomyces cerevisiae. J. Cell Sci. 115, 4977-4991.
28. Jin, H. and Amberg, D. C. (2000). The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p. Mol. Biol. Cell 11, 647-661.
29. Kikyo, M., Tanaka, K., Kamei, T., Ozaki, K., Fujiwara, T., Inoue, E., Takita, Y., Ohya, Y. and Takai, Y. (1999). An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18, 7046-7054.
30. Korinek, W. S., Copeland, M. J., Chaudhuri, A. and Chant, J. (2000). Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science 287, 2257-2259.
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. Lord, M., Yang, M. C., Mischke, M. and Chant, J. (2000). Cell cycle programs of gene expression control morphogenetic protein localization. J. Cell Biol. 151, 1501-1512.
34. Martin, S. G., Rincon, S. A., Basu, R., Perez, P. and Chang, F. (2007). Regulation of the formin for3p by cdc42p and bud6p. Mol. Biol. Cell 18, 4155-4167.
35. Miller, R. K., Matheos, D. and Rose, M. D. (1999). The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J. Cell Biol. 144, 963-975.
36. Miller, R. K., Cheng, S. C. and Rose, M. D. (2000). Bim1p/Yeb1p mediates the Kar9p-dependent cortical attachment of cytoplasmic microtubules. Mol. Biol. Cell 11, 2949-2959.
37. Moseley, J. B. and Goode, B. L. (2005). Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280, 28023-28033.
38. Moseley, J. B. and Goode, B. L. (2006). The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70, 605-645.
39. Nelson, S. A. and Cooper, J. A. (2007). A novel pathway that coordinates mitotic exit with spindle position. Mol. Biol. Cell 18, 3440-3450.
40. Otomo, T., Otomo, C., Tomchick, D. R., Machius, M. and Rosen, M. K. (2005). Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol. Cell 18, 273-281.
41. Ozaki-Kuroda, K., Yamamoto, Y., Nohara, H., Kinoshita, M., Fujiwara, T., Irie, K. and Takai, Y. (2001). Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 827-839.
42. Pearson, C. G. and Bloom, K. (2004). Dynamic microtubules lead the way for spindle positioning. Nat. Rev. Mol. Cell. Biol. 5, 481-492.
43. Pereira, G., Tanaka, T. U., Nasmyth, K. and Schiebel, E. (2001). Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex. EMBO J. 20, 6359-6370.
44. Pringle, J. R. (1991). Staining of bud scars and other cell wall chitin with calcofluor. Meth. Enzymol. 194, 732-735.
45. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A. and Boone, C. (2002). Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612-615.
46. Pruyne, D., Gao, L., Bi, E. and Bretscher, A. (2004). Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15, 4971-4989.
47. Sagot, I., Klee, S. K. and Pellman, D. (2002). Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4, 42-50.
48. Segal, M., Bloom, K. and Reed, S. I. (2000a). Bud6 directs sequential microtubule interactions with the bud tip and bud neck during spindle morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 11, 3689-3702.
49. Segal, M., Clarke, D. J., Maddox, P., Salmon, E. D., Bloom, K. and Reed, S. I. (2000b). Coordinated spindle assembly and orientation requires Clb5p-dependent kinase in budding yeast. J. Cell Biol. 148, 441-452.
50. Segal, M., Bloom, K. and Reed, S. I. (2002). Kar9p-independent microtubule capture at Bud6p cortical sites primes spindle polarity before bud emergence in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 4141-4155.
51. 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.
52. Sheu, Y. J., Santos, B., Fortin, N., Costigan, C. and Snyder, M. (1998). Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol. 18, 4053-4069.
53. Sheu, Y. J., Barral, Y. and Snyder, M. (2000). Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae. Mol. Cell. Biol. 20, 5235-5247.
54. Sikorski, R. S. and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
55. Straight, A. F., Marshall, W. F., Sedat, J. W. and Murray, A. W. (1997). Mitosis in living budding yeast: anaphase A but no metaphase plate. Science 277, 574-578.
56. Theesfeld, C. L., Irazoqui, J. E., Bloom, K. and Lew, D. J. (1999). The role of actin in spindle orientation changes during the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 146, 1019-1032.
57. Wach, A., Brachat, A., Pohlmann, R. and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
58. Yamashita, Y. M., Mahowald, A. P., Perlin, J. R. and Fuller, M. T. (2007). Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315, 518-521.
59. Yang, S., Ayscough, K. R. and Drubin, D. G. (1997). A role for the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection. J. Cell Biol. 136, 111-123.
60. Yeh, E., Yang, C., Chin, E., Maddox, P., Salmon, E. D., Lew, D. J. and Bloom, K. (2000). Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants. Mol. Biol. Cell 11, 3949-3961.
61. Yin, H., Pruyne, D., Huffaker, T. C. and Bretscher, A. (2000). Myosin V orientates the mitotic spindle in yeast. Nature 406, 1013-1015.