Profilin-mediated competition between capping protein and formin Cdc12p during cytokinesis in fission yeast

Molecular Biology of the Cell

Volumn 16, Issue 5, 2005, Pages 2313-2324

  Kovar, David R ^a   Wu, Jian Qiu ^a   Pollard, Thomas D ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDC12 PROTEIN; METHENAMINE; PROFILIN; PROTEIN; PROTEIN SPCP; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL SEPARATION; CYTOKINESIS; DEPOLYMERIZATION; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; HIGH TEMPERATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; TEMPERATURE SENSITIVITY; YEAST;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; BINDING, COMPETITIVE; CELL CYCLE PROTEINS; CONTRACTILE PROTEINS; CYTOKINESIS; DESTRIN; GENES, FUNGAL; MICE; MICROFILAMENT PROTEINS; MUTATION; PROFILINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCES POMBE;

EID: 18244377374     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-09-0781     Document Type: Article

References (67)

1. Amatruda, J. F., Cannon, J. F., Tatchell, K., Hug, C., and Cooper, J. A. (1990). Disruption of the actin cytoskeleton in yeast capping protein mutants. Nature 344, 352-354.
2. Amatruda, J. F., and Cooper, J. A. (1992). Purification, characterization, and immunofluorescence localization of Saccharomyces cerevisiae capping protein. J. Cell Biol. 117, 1067-1076.
3. Amatruda, J. F., Gattermeir, D. J., Karpova, T. S., and Cooper, J. A. (1992). Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast. J. Cell Biol. 119, 1151-1162.
4. Bahler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P., and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
5. Balasubramanian, M. K., Hirani, B. R., Burke, J. D., and Gould, K. L. (1994). The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125, 1289-1301.
6. Balasubramanian, M. K., McCollum, D., and Gould, K. L. (1997). Cytokinesis in fission yeast Schizosaccharomyces pombe. Methods Enzymol. 283, 494-506.
7. Bi, E., Maddox, P., Lew, D. J., Salmon, E. D., McMillan, J. N., Yeh, E., and Pringle, J. R. (1998). Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142, 1301-1312.
8. Blanchoin, L., and Pollard, T. D. (2002). Hydrolysis of ATP by polymerized actin depends on the bound divalent cation but not profilin. Biochemistry 41, 597-602.
9. Caldwell, J. E., Heiss, S. G., Mermall, V., and Cooper, J. A. (1989). Effects of CapZ, an actin capping protein of muscle, on the polymerization of actin. Biochemistry 28, 8506-8514.
10. Carter, S. B. (1967). Effects of cytochalasins on mammalian cells. Nature 213, 261-264.
11. Chang, F., Drubin, D., and Nurse, P. (1997). cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137, 169-182.
12. Cooper, J. A., and Pollard, T. D. (1985). Effect of capping protein on the kinetics of actin polymerization. Biochemistry 24, 793-799.
13. Cooper, J. A., and Schafer, D. A. (2000). Control of actin assembly and disassembly at filament ends. Curr. Opin. Cell Biol. 12, 97-103.
14. 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.
15. Evangelista, M., Zigmond, S., and Boone, C. (2003). Formins: signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116, 2603-2611.
16. Feierbach, B., and Chang, F. (2001). Roles of the fission yeast formin forSp in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11, 1656-1665.
17. Goode, B. L., Drubin, D. G., and Lappalainen, P. (1998). Regulation of the cortical actin cytoskeleton in budding yeast by twinfilin, a ubiquitous actin monomer-sequestering protein. J. Cell Biol. 342, 723-733.
18. Harris, E. S., Li, F., and Higgs, H. N. (2004). The mouse formin, FRLalpha, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. J. Biol. Chem.
19. Higashida, C., Miyoshi, T., Fujita, A., Oceguera-Yanez, F., Monypenny, J., Andou, Y., Narumiya, S., and Watanabe, N. (2004). Actin polymerization- driven molecular movement of mDia1 in living cells. Science 303, 2007-2010.
20. Higgs, H. N., Blanchoin, L., and Pollard, T. D. (1999). Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38, 15212-15222.
21. Hopmann, R., Cooper, J. A., and Miller, K. G. (1996). Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila. J. Cell Biol. 133, 1293-1305.
22. Hopmann, R., and Miller, K. G. (2003). A balance of capping protein and profilin functions is required to regulate actin polymerization in Drosophila bristle. Mol. Biol. Cell 34, 118-128.
23. Houk, T. W., Jr., and Ue, K. (1974). The measurement of actin concentration in solution: a comparison of methods. Anal. Biochem. 62, 66-74.
24. Huang, S., Blanchoin, L., Kovar, D. R., and Staiger, C. J. (2003). Arabidopsis capping protein (ArCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J. Biol. Chem. 278, 44832-44842.
25. Hug, C., Jay, P. Y., Reddy, I., McNally, J. G., Bridgman, P. C., Elson, E. L., and Cooper, J. A. (1995). Capping protein levels influence actin assembly and cell motility in Dictyostelium. Cell 81, 591-600.
26. Isenberg, G., Aebi, U., and Pollard, T. D. (1980). An actin-binding protein from Acanthamoeba regulates actin filament polymerization and interactions. Nature 288, 455-459.
27. Kang, F., Purich, D. L., and Southwick, F. S. (1999). Profilin promotes barbed-end actin filament assembly without lowering the critical concentration. J. Biol. Chem. 274, 36963-36972.
28. Kiger, A., Baum, B., Jones, S., Jones, M., Coulson, A., Echeverri, C., and Perrimon, N. (2003). A functional genomic analysis of cell morphology using RNA interference. J. Biol. 2, 27.
29. Kim, K., Yamashita, A., Wear, M. A., Maeda, Y., and Cooper, J. A. (2004). Capping protein binding to actin in yeast: biochemical mechanism and physiological relevance. J. Cell Biol. 164, 567-580.
30. Kovar, D. R., Kuhn, J. R., Tichy, A. L., and Pollard, T. D. (2003). The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J. Cell Biol. 161, 875-887.
31. Kovar, D. R., and Pollard, T. D. (2004). Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc. Natl. Acad. Sci. USA 101, 14725-14730.
32. 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.
33. Li, F., and Higgs, H. N. (2003). The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 13, 1335-1340.
34. Li, R., Zheng, Y., and Drubin, D. G. (1995). Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J. Cell Biol. 128, 599-615.
35. Lu, J., and Pollard, T. D. (2001). Profilin binding to poly-L-proline and actin monomers along with ability to catalyze actin nucleotide exchange is required for viability of fission yeast. Mol. Biol. Cell 12, 1161-1175.
36. Marks, J., and Hyams, J. S. (1985). Localization of F-actin through the cell division cycle of Schizosaccharomyces pombe. Eur. J. Cell Biol. 39, 27-32.
37. Maundrell, K. (1990). nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J. Biol. Chem. 265, 10857-10864.
38. Moseley, J. B., Sagot, I., Manning, A. L., Xu, Y., Eck, M. J., Pellman, D., and Goode, B. L. (2004). A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell 15, 896-907.
39. Nakano, K., Imai, J., Arai, R., Toh, E. A., Matsui, Y., and Mabuchi, I. (2002). The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. J. Cell Sci. 115, 4629-4639.
40. Nakano, K., Satoh, K., Morimatsu, A., Ohnuma, M., and Mabuchi, I. (2001). Interactions among a fimbrin, a capping protein, and an actin-depolymerizing factor in organization of the fission yeast actin cytoskeleton. Mol. Biol. Cell 12, 3515-3526.
41. Palmgren, S., Ojala, P. J., Wear, M. A., Cooper, J. A., and Lappalainen, P. (2001). Interactions with PIP2, ADP-actin monomers, and capping protein regulate the activity and localization of yeast twinfilin. J. Cell Biol. 155, 251-260.
42. Pantaloni, D., and Carlier, M. F. (1993). How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell 75, 1007-1014.
43. Pasion, S. G., and Forsburg, S. L. (1999). Nuclear localization of Schizosaccharomyces pombe Mcm2/Cdc19p requires MCM complex assembly. Mol. Biol. Cell 10, 4043-4057.
44. Pelham, R. J., and Chang, F. (2002). Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature 419, 82-86.
45. Petersen, J., Nielsen, O., Egel, R., and Hagan, I. M. (1998a). F-actin distribution and function during sexual differentiation in Schizosaccharomyces pombe. J. Cell Sci. 111, 867-876.
46. Petersen, J., Nielsen, O., Egel, R., and Hagan, I. M. (1998b). FH3, a domain found in formins, targets the fission yeast formin Fus1 to the projection tip during conjugation. J. Cell Biol. 141, 1217-1228.
47. Pollard, T. D., and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
48. Pollard, T. D., and Cooper, J. A. (1984). Quantitative analysis of the etfect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry 23, 6631-6641.
49. 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.
50. Rogers, S. L., Wiedemann, U., Stuurman, N., and Vale, R. D. (2003). Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162, 1079-1088.
51. Romero, S., Le Clainche, C., Didry, D., Egile, C., Pantaloni, D., and Carlier, M. F. (2004). Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119, 419-429.
52. Sagot, I., Rodal, A. A., Moseley, J., Goode, B. L., and Pellman, D. (2002). An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4, 626-631.
53. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
54. Schroeder, T. E. (1970). The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z Zellforsch Mikrosk Anat. 109, 431-449.
55. Schroeder, T. E. (1972). The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol. 53, 419-434.
56. Skop, A. R., Liu, H., Yates, I. J., Meyer, B. J., and Heald, R. (2004). Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 305, 61-66.
57. Soeno, Y., Abe, H., Kimura, S., Maruyama, K., and Obinata, T. (1998). Generation of functional beta-actinin (CapZ) in an E. coli expression system. J. Muscle Res. Cell Motil. 19, 639-646.
58. Tolliday, N., Pitcher, M., and Li, R. (2003). Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II. Mol. Biol. Cell 14, 798-809.
59. Waddle, J. A., Cooper, J. A., and Waterston, R. H. (1994). Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions. Development 120, 2317-2328.
60. Wallar, B. J., and Alberts, A. S. (2003). The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13, 435-446.
61. Watts, F. Z., Shiels, G., and Orr, E. (1987). The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J. 6, 3499-3505.
62. Wear, M. A., Yamashita, A., Kim, K., Maeda, Y., and Cooper, J. A. (2003). How capping protein binds the barbed end of the actin filament. Curr. Biol. 13, 1531-1537.
63. Wu, J. Q., Bahler, J., and Pringle, J. R. (2001). Roles of a fimbrin and an alpha-actinin-like protein in fission yeast cell polarization and cytokinesis. Mol. Biol. Cell 12, 1061-1077.
64. Wu, J. Q., Kuhn, J. R., Kovar, D. R., and Pollard, T. D. (2003). Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 5, 723-734.
65. Yamashita, A., Maeda, K., and Maeda, Y. (2003). Crystal structure of CapZ: structural basis for actin filament barbed end capping. EMBO J. 22, 1529-1538.
66. Young, M. E., Cooper, J. A., and Bridgman, P. C. (2004). Yeast actin patches are networks of branched actin filaments. J. Cell Biol. 166, 629-635.
67. Zigmond, S. H., Evangelista, M., Boone, C., Yang, C., Dar, A. C., Sichert, F., Forkey, J., and Pring, M. (2003). Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13, 1820-1823.