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PMID: 9367979 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae.

Genes & development ·Vol. 11 ·No. 22 ·1997-11-15 ·Pages 2958-71

Chen GC, Kim YJ, Chan CS

Abstract

BEM2 of Saccharomyces cerevisiae encodes a Rho-type GTPase-activating protein that is required for proper bud site selection at 26 degrees C and for bud emergence at elevated temperatures. We show here that the temperature-sensitive growth phenotype of bem2 mutant cells can be suppressed by increased dosage of the GIC1 gene. The Gic1 protein, together with its structural homolog Gic2, are required for cell size and shape control, bud site selection, bud emergence, actin cytoskeletal organization, mitotic spindle orientation/positioning, and mating projection formation in response to mating pheromone. Each protein contains a CRIB (Cdc42/Rac-interactive binding) motif and each interacts in the two-hybrid assay with the GTP-bound form of the Rho-type Cdc42 GTPase, a key regulator of polarized growth in yeast. The CRIB motif of Gic1 and the effector domain of Cdc42 are required for this association. Genetic experiments indicate that Gic1 and Gic2 play positive roles in the Cdc42 signal transduction pathway, probably as effectors of Cdc42. Subcellular localization studies with a functional green fluorescent protein-Gic1 fusion protein indicate that this protein is concentrated at the incipient bud site of unbudded cells, at the bud tip and mother-bud neck of budded cells, and at cortical sites on large-budded cells that may delimit future bud sites in the two progeny cells. The ability of Gic1 to associate with Cdc42 is important for its function but is apparently not essential for its subcellular localization.

MeSH Terms
Adaptor Proteins, Signal Transducing Amino Acid Sequence Binding Sites Carrier Proteins/physiology Cell Compartmentation Cell Cycle Proteins/physiology Cell Division Cell Survival Fungal Proteins/physiology GTP-Binding Proteins/physiology GTPase-Activating Proteins Genes, Fungal Molecular Sequence Data Protein Binding Protein Serine-Threonine Kinases/physiology Saccharomyces cerevisiae/cytology,growth & development Saccharomyces cerevisiae Proteins Sequence Alignment Sequence Homology, Amino Acid cdc42 GTP-Binding Protein, Saccharomyces cerevisiae
Chemicals
Adaptor Proteins, Signal Transducing BEM2 protein, S cerevisiae Carrier Proteins Cell Cycle Proteins Fungal Proteins GIC1 protein, S cerevisiae GIC2 protein, S cerevisiae GTPase-Activating Proteins Saccharomyces cerevisiae Proteins CLA4 protein, S cerevisiae Protein Serine-Threonine Kinases GTP-Binding Proteins cdc42 GTP-Binding Protein, Saccharomyces cerevisiae
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Chen G C
Department of Microbiology, The University of Texas, Austin, Texas 78712, USA.
Kim Y J
Chan C S
References (57)
57 references, click to expand
  1. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity.
    Mol Biol Cell. 1993 Dec;4(12):1307-16 PMID: 8167411
  2. Movement of yeast cortical actin cytoskeleton visualized in vivo.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3886-91 PMID: 8632984
  3. 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. 1994 Jan 28;269(4):2369-72 PMID: 8300560
  4. RSR1, a ras-like gene homologous to Krev-1 (smg21A/rap1A): role in the development of cell polarity and interactions with the Ras pathway in Saccharomyces cerevisiae.
    Mol Cell Biol. 1992 Feb;12(2):758-66 PMID: 1732742
  5. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4463-8 PMID: 9114012
  6. 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. 1991 Mar;11(3):1295-305 PMID: 1996092
  7. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1995 May;129(3):751-65 PMID: 7730409
  8. Characterization of SKM1, a Saccharomyces cerevisiae gene encoding a novel Ste20/PAK-like protein kinase.
    Mol Microbiol. 1997 Feb;23(3):431-44 PMID: 9044278
  9. Associations among PH and SH3 domain-containing proteins and Rho-type GTPases in Yeast.
    J Cell Biol. 1996 May;133(4):879-94 PMID: 8666672
  10. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast.
    J Cell Biol. 1995 Feb;128(4):599-615 PMID: 7860633
  11. The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2.
    Cell. 1997 Feb 21;88(4):531-42 PMID: 9038344
  12. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae.
    J Cell Biol. 1994 Jun;125(5):1077-93 PMID: 8195291
  13. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast.
    Genes Dev. 1997 Nov 15;11(22):2972-82 PMID: 9367980
  14. Selection of polarized growth sites in yeast.
    Trends Cell Biol. 1996 Nov;6(11):434-41 PMID: 15157515
  15. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces.
    J Cell Biol. 1984 Mar;98(3):922-33 PMID: 6365930
  16. The LIM domain-containing Dbm1 GTPase-activating protein is required for normal cellular morphogenesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1376-90 PMID: 8657111
  17. Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast.
    EMBO J. 1993 Dec 15;12(13):5267-75 PMID: 8262069
  18. Interaction mating reveals binary and ternary connections between Drosophila cell cycle regulators.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12980-4 PMID: 7809159
  19. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers.
    Yeast. 1990 Sep-Oct;6(5):363-6 PMID: 2220072
  20. Yeast src homology region 3 domain-binding proteins involved in bud formation.
    J Cell Biol. 1996 May;133(4):865-78 PMID: 8666671
  21. Role for the Rho-family GTPase Cdc42 in yeast mating-pheromone signal pathway.
    Nature. 1995 Aug 24;376(6542):702-5 PMID: 7651520
  22. The SIT4 protein phosphatase functions in late G1 for progression into S phase.
    Mol Cell Biol. 1991 Apr;11(4):2133-48 PMID: 1848673
  23. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization.
    Cell. 1996 Mar 8;84(5):723-34 PMID: 8625410
  24. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases.
    J Biol Chem. 1995 Dec 8;270(49):29071-4 PMID: 7493928
  25. Genetic evidence for a functional interaction between Saccharomyces cerevisiae CDC24 and CDC42.
    Yeast. 1994 Apr;10(4):463-74 PMID: 7941732
  26. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites.
    Mol Biol Cell. 1997 Apr;8(4):729-53 PMID: 9247651
  27. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast.
    Genes Dev. 1995 Aug 1;9(15):1817-30 PMID: 7649470
  28. 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 U S A. 1989 Dec;86(24):9976-80 PMID: 2690082
  29. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity.
    J Cell Biol. 1990 Jul;111(1):143-52 PMID: 2164028
  30. Pheromone signalling in Saccharomyces cerevisiae requires the small GTP-binding protein Cdc42p and its activator CDC24.
    Mol Cell Biol. 1995 Oct;15(10):5246-57 PMID: 7565673
  31. Assay of yeast mating reaction.
    Methods Enzymol. 1991;194:77-93 PMID: 2005823
  32. Improved green fluorescence.
    Nature. 1995 Feb 23;373(6516):663-4 PMID: 7854443
  33. One-step gene disruption in yeast.
    Methods Enzymol. 1983;101:202-11 PMID: 6310324
  34. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast.
    Genetics. 1993 Nov;135(3):677-91 PMID: 8293973
  35. The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast.
    Mol Biol Cell. 1995 Aug;6(8):1011-24 PMID: 7579704
  36. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  37. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae.
    J Cell Biol. 1984 Mar;98(3):934-45 PMID: 6365931
  38. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1.
    Cell. 1991 Jun 28;65(7):1213-24 PMID: 1905981
  39. Gene splicing by overlap extension.
    Methods Enzymol. 1993;217:270-9 PMID: 8474334
  40. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins.
    J Cell Biol. 1993 Mar;120(6):1305-20 PMID: 8449978
  41. Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast.
    J Cell Biol. 1994 Dec;127(5):1395-406 PMID: 7962098
  42. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1981 Jun;89(3):395-405 PMID: 7019215
  43. 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. 1995 Dec 1;9(23):2949-63 PMID: 7498791
  44. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2.
    Cell. 1993 Nov 19;75(4):791-803 PMID: 8242750
  45. Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins. Delineation of a limit Cdc42 GTPase-activating protein domain.
    J Biol Chem. 1993 Nov 25;268(33):24629-34 PMID: 8227021
  46. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway.
    Cell. 1991 Jun 28;65(7):1203-12 PMID: 2065354
  47. ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Oct;16(10):5264-75 PMID: 8816439
  48. 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. 1991 Jul;11(7):3537-44 PMID: 1904541
  49. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis.
    Science. 1997 Apr 4;276(5309):118-22 PMID: 9082982
  50. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1857-70 PMID: 8657162
  51. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae.
    J Biol Chem. 1995 Jan 13;270(2):626-30 PMID: 7822288
  52. 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. 1997 Apr 21;137(2):399-416 PMID: 9128251
  53. Role of Bud3p in producing the axial budding pattern of yeast.
    J Cell Biol. 1995 May;129(3):767-78 PMID: 7730410
  54. Control of cellular morphogenesis by the Ip12/Bem2 GTPase-activating protein: possible role of protein phosphorylation.
    J Cell Biol. 1994 Dec;127(5):1381-94 PMID: 7962097
  55. A mutant of yeast defective in cellular morphogenesis.
    Science. 1978 Jun 9;200(4346):1171-3 PMID: 349694
  56. Fluorescence microscopy methods for yeast.
    Methods Cell Biol. 1989;31:357-435 PMID: 2476649
  57. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1990 Jul;111(1):131-42 PMID: 2195038
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
1997-11-15
Pages
2958-71
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC316704
Subset
IM
Grants
NIGMS NIH HHS · GM45185 · United States
Databases
GENBANK
U00061, U28374
Analysis Services
Analysis Services

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