The LIM domain-containing Dbm1 GTPase-activating protein is required for normal cellular morphogenesis in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 16, Issue 4, 1996, Pages 1376-1390

  Chen, Guang Chao ^a   Zheng, Li ^a   Chan, Clarence S M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL GROWTH; CYTOSKELETON; HAPLOIDY; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE;

EID: 0029939188     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.4.1376     Document Type: Article

References (89)

1. Adames, N., K. Blundell, M. N. Ashby, and C. Boone. 1995. Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection. Science 270:464-467.
2. Adams, A. E. M., D. I. Johnson, R. M. Longnecker, B. F. Sloat, and J. R. Pringle. 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 111:131-142.
3. Adams, A. E. M., and J. R. Pringle. 1984. Relationship of actin and tubulin distribution in wild-type and morphogenetic mutant Saccharomyces cerevisiae. J Cell Biol 98:934-945.
4. Archer, V. E. V., J. Breton, I. Sanchez-Garcia, H. Osada, A. Forster, A. J. Thomson, and T. H. Rabbitts. 1994. Cysteine-rich LIM domains of LIM-homeodomain and LIM-only proteins contain zinc but not iron. Proc Natl. Acad. Sci. USA 91:316-320.
5. Bender, A. 1993. Genetic evidence for the roles of the bud-site-selection genes BUD5 and BUD2 in control of the Rsr1p (Bud1p) GTPase in yeast Proc. Natl. Acad. Sci. USA 90:9926-9929.
6. Bender, A., and J. Pringle. 1991. Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol Cell. Biol. 11:1295-1305.
7. Bender, A., and J. R. Pringle. 1989. Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1. Proc. Natl. Acad Sci. USA 86:9976-9980.
8. Benton, B. K., A. H. Tinkelenberg, D. Jean, S. D. Plump, and F. R. Cross. 1993. Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast. EMBO J 12:5267-5275.
9. Bretscher, A., B. Drees, E. Harsay, D. Schott, and T. Wang. 1994. What are the basic functions of microfilaments? Insights from studies in budding yeast J. Cell Biol 126:821-825.
10. Brewster, J. L., and M. C. Gustin. 1994. Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway. Yeast 10:425-439.
11. Chan, C. S. M., and D. Botstein. 1993. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 135: 677-691.
12. Chant, J. 1994. Cell polarity in yeast. Trends Genet. 10:328-333.
13. Chant, J., K. Corrado, J. R. Pringle, and I. Herskowitz. 1991. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 65:1213-1224
14. Chant, J., and I. Herskowitz. 1991. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65:1203-1212.
15. Chant, J., M. Mischke, E. Mitchell, I. Herskowitz, and J. R. Pringle. 1995. Role of Bud3p in producing the axial budding pattern of yeast. J Cell Biol. 129:767-778.
16. Chant, J., and J. R. Pringle. 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol 129:751-765.
17. Chenevert, J., K. Corrado, A. Bender, J. Pringle, and I. Herskowitz. 1992 A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature (London) 356:77-79.
18. Corrado, K. Personal communication.
19. rac. Nature (London) 351:400-402.
20. Doignon, F., N. Biteau, M. Crouzet, and M. Aigle. 1993. The complete sequence of a 19,482 bp segment located on the right arm of chromosome II from Saccharomyces cerevisiae. Yeast 9:189-199.
21. Feuerstein, R., X. Wang, D. Song, N. E. Cooke, and S. A. Liebhaber. 1994. The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc. Natl. Acad. Sci. USA 91:10655-10659.
22. Flescher, E. G., K. Madden, and M. Snyder. 1993. Components required for cytokinesis are important for bud site selection in yeast. J. Cell Biol. 122: 373-386.
23. Ford, S. K., and J. R. Pringle. 1991. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site Dev. Genet. 12:281-292.
24. Friefelder, D. 1960. Bud position in Saccharomyces cerevisiae. J. Bacteriol. 80:567-568.
25. Fujita, A., C. Oka, Y. Arikawa, T. Katagai, A. Tonouchi, S. Kuhara, and Y. Misumi. 1994 A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature (London) 372:567-570.
26. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS Cell 68:1077-1090.
27. Haarer, B. K., and J. R. Pringle. 1987. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol Cell Biol. 7:3678-3687.
28. Hall, A. 1994. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10:31-54.
29. Hayashibe, M., and S. Katohda. 1973. Initiation of budding and chitin-ring. J. Gen. Appl. Microbiol. 19:23-39.
30. Hempe, J. M., and R. J. Cousins. 1991. Cysteine-rich intestinal protein binds zinc during transmucosal zinc transport. Proc Natl Acad. Sci. USA 88:9671-9674.
31. Johnson, D. I., and J. R. Pringle. 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111:143-152.
32. Jones, J. S., and L. Prakash. 1990. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast 6:363-366.
33. Kim, H. B., B. K. Haarer, and J. R. Pringle. 1991 Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. J. Cell Biol. 112:535-544.
34. Kim, Y.-J., L. Francisco, G.-C. Chen, E. Marcotte, and C. S. M. Chan. 1994 Control of cellular morphogenesis by the Ip12/Bem2 GTPase-activating protein. possible role of protein phosphorylation. J. Cell Biol 127:1381-1394.
35. Koerner, T. J., J. E. Hill, A. M. Myers, and A. Tzagoloff. 1991. High-expression vectors with multiple cloning sites for construction of trpE fusion genes: pATH vectors. Methods Enzymol 194:477-490.
36. Kosa, J. L., J. W. Michelsen, H. A. Louis, J. I. Olsen, D. R. Davis, M. C. Beckerle, and D. R. Winge. 1994 Common metal ion coordination in LIM domain proteins. Biochemistry 33:468-477.
37. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987 Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol 154:367-382.
38. Lamarche, N., and A. Hall. 1994. GAPs for rho-related GTPases Trends Genet. 10:436-440
39. Li, P. M., J. Reichert, G. Freyd, H. R. Horvitz, and C. T. Walsh. 1991. The LIM region of a presumptive Caenorhabditis elegans transcription factor is an iron-sulfur- and zinc-containing metallodomain. Proc Natl. Acad Sci. USA 88:9210-9213.
40. Li, R., Y. Zheng, and D. G. Drubin. 1995. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J. Cell Biol 128:599-615.
41. Madaule, P., R. Axel, and A. M. Myers. 1987. Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae. Proc. Natl. Acad Sci. USA 84:779-783.
42. Madden, K., C. Costigan, and M. Snyder. 1992. Cell polarity and morphogenesis in Saccharomyces cerevisiae. Trends Cell Biol. 2:22-29.
43. Madden, K., and M. Snyder. 1992. Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection. Mol Biol. Cell 3:1025-1035.
44. Marmur, J. 1961 A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J. Mol Biol. 3:208-218.
45. Matsui, Y., and A. Toh-e. 1992. Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol. Cell. Biol. 12:5690-5699
46. Michelsen, J. W., K. L. Schmeichel, M. C. Beekerle, and D. R. Winge. 1993. The LIM motif defines a specific zinc-binding protein domain Proc. Natl. Acad. Sci. USA 90:4404-4408.
47. Michelsen, J. W., A. K. Sewell, H. A. Louis, J. I. Olsen, D. R. Davis, D. R. Winge, and M. C. Beckerle. 1994. Mutational analysis of the metal sites in an LIM domain. J. Biol. Chem 269:11108-11113.
48. Molero, G., M. Yuste-Rojas, A. Montesi, A. Vázquez, C. Nombela, and M. Sanchez. 1993. A cdc-like autolytic Saccharomyces cerevisiae mutant altered in budding site selection is complemented by SPO12, a sporulation gene J. Bacteriol. 175:6562-6570.
49. Mulholland, J., D. Preuss, A. Moon, A. Wong, D. Drubin, and D. Botstein. 1994. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol. 125:381-391.
50. Müller, L., G. Xu, R. Wells, C. P. Hollenberg, and W. Piepersberg. 1994. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucleic Acids Res. 22:3151-3154.
51. Nakajima, H., A. Hirata, Y. Ogawa, T. Yonehara, K. Yoda, and M. Yamasaki. 1991. A cytoskeleton-related gene, USO1. is required for intracellular protein transport in Saccharomyces cerevisiae. J. Cell Biol. 113:245-260.
52. Ohya, Y. Personal communication.
53. Ohya, Y., S. Miyamoto, Y. Ohsumi, and Y. Anraku. 1986. Calcium-sensitive cls4 mutant of Saccharomyces cerevisiae with a defect in bud formation. J. Bacteriol. 165:28-33.
54. Ohya, Y., Y. Ohsumi, and Y. Anraku. 1984. Genetic study of the role of calcium ions in the cell division cycle of Saccharomyces cerevisiae: a calcium-dependent mutant and its trifluoperazine-dependent pseudorevertants. Mol. Gen. Genet. 193:389-394.
55. Ohya, Y., H. Qadota, Y. Anraku, J. R. Pringle, and D. Botstein. 1993. Suppression of yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol. Biol. Cell 4:1017-1025.
56. Park, H.-O., J. Chant, and I. Herskowitz. 1993 BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature (London) 365:269-274.
57. Peterson, J., Y. Zheng, L. Bender, A. Myers, R. Cerione, and A. Bender. 1994. Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast. J. Cell Biol 127:1395-1406.
58. Powers, S., E. Gonzales, T. Christensen, J. Cubert, and D. Broek. 1991. Functional cloning of BUD5, a CDC25-related gene from S. cerevisiae that can suppress a dominant-negative RAS2 mutant Cell 65:1225-1231.
59. Pringle, J. R., R. A. Preston, A. Adams, T. Stearns, D. Drubin, B. K. Haarer, and E. Jones. 1989. Fluorescence microscopy methods for yeast. Methods Cell Biol. 31:357-435
60. Ramer, S. W., S. J. Elledge, and R. W. Davis. 1992. Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc. Natl Acad. Sci. USA 89:11589-11593.
61. Ridley, A. J., A. J. Self, F. Kasmi, H. F. Paterson, A. Hall, C. J. Marshall, and C. Ellis. 1993. rho family GTPase activating proteins p190, bcr and rhoGAP show distinct specificities in vitro and in vivo EMBO J 12:5151-5160.
62. Rine, J., and I. Herskowitz. 1987. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae Genetics 116:9-22.
63. Roberts, R. L., and G. R. Fink. 1994. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8:2974-2985.
64. Rose, M. D., P. Novick, J. H. Thomas, D. Botstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237-243.
65. Rose, M. D., F. Winston, and P. Hieter. 1990 Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202-211
67. Sadler, I., A. W. Crawford, J. W. Michelsen, and M. C. Beckerle. 1992. Zyxin and cCRP. two interactive LIM domain proteins associated with the cytoskeleton. J. Cell Biol. 119:1573-1587
68. Sánchez-García, I., H. Osada, A. Forster, and T. H. Rabbitts. 1993 The cysteine-rich LIM domains inhibit DNA binding by the associated homeodomain in Isl-1. EMBO J. 12:4243-4250
69. Sánchez-García, I., and T. H. Rabbits. 1994. The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends Genet. 10:315-320.
70. Schmeichel, K. L., and M. C. Beckerle. 1994. The LIM domain is a modular protein-binding interface. Cell 79:211-219.
71. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
72. Sloat, B. F., A. Adams, and J. R. Pringle. 1981. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 89:395-405
73. Sloat, B. F., and J. R. Pringle. 1978. A mutant of yeast defective in cellular morphogenesis. Science 200:1171-1173.
74. Snyder, M. 1989 The SPA2 protein of yeast localizes to sites of cell growth. J. Cell Biol 108:1419-1429
75. Snyder, M., S. Gehrung, and B. D. Page. 1991. Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J. Cell Biol. 114:515-532
76. Stevenson, B. J., B. Ferguson, C. De Virgilio, E. Bi, J. R. Pringle, G. Ammerer, and G. F. Sprague Jr. 1995. Mutation of RGA1, which encodes a putative GTPase-activating protein for the polarity - establishment protein Cdc42p, activates the pheromone response pathway in the yeast Saccharomyces cerevisiae. Genes Dev. 9:2949-2963.
77. Takai, Y., T. Sasaki, K. Tanaka, and H. Nakanishi. 1995. Rho as a regulator of the cytoskeleton. Trends Biochem. Sci. 20:227-231.
78. Trueblood, C. E., Y. Ohya, and J. Rine. 1993. Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase I in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:4260-4275.
79. Wang, T., and A. Bretscher. 1995. The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast. Mol. Biol. Cell 6:1011-1024.
80. Welch, M. D., D. A. Holtzman, and D. G. Drubin. 1994. The yeast actin cytoskeleton. Curr. Opin. Cell Biol. 6:110-119.
81. Winey, M., M. A. Hoyt, C. Chan, L. Goetsch, D. Botstein, and B. Byers. 1993. NDC1: a nuclear periphery component required for yeast spindle pole body duplication. J. Cell Biol. 122:743-751.
82. Xue, D., Y. Tu, and M. Chalfie. 1993. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science. 261: 1324-1328.
83. Yamochi, W., K. Tanaka, H. Nonaka, A. Maeda, T. Musha, and Y. Takai. 1994. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 125: 1077-1093.
84. Zheng, Y., A. Bender, and R. A. Cerione. 1995. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. J. Biol. Chem. 270:626-630.
85. Zheng, Y., R. Cerione, and A. Bender. 1994. Control of the yeast bud-site assembly GTPase Cdc42: catalysis of guanine-nucleotide exchange by Cdc24 and stimulation of GTPase activity by Bem3. J. Biol. Chem. 269:2369-2372.
86. Zheng, Y., M. J. Hart, K. Shinjo, T. Evans, A. Bender, and R. A. Cerione. 1993. Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins J. Biol. Chem. 268:24629-24634.
87. Ziman, M., and D. I. Johnson. 1994. Genetic evidence for a functional interaction between Saccharomyces cerevisiae CDC24 and CDC42. Yeast. 10:463-474.
88. Ziman, M., J. M. O'Brien, L. A. Ouellette, W. R. Church, and D. I. Johnson. 1991. Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol. Cell. Biol. 11:3537-3544.
89. Ziman, M., D. Preuss, J. Mulholland, J. M. O'Brien, D. Botstein, and D. I. Johnson. 1993. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol. Biol Cell 4:1307-1316