The Saccharomyces homolog of mammalian RACK1, Cpc2/Asc1p, is required for FLO11-dependent adhesive growth and dimorphism

Molecular and Cellular Proteomics

Volumn 6, Issue 11, 2007, Pages 1968-1979

  Valerius, Oliver ^a   Kleinschmidt, Malte ^a   Rachfall, Nicole ^a   Schulze, Florian ^a   Marín, Sarai López ^a   Hoppert, Michael ^a   Streckfuss Bömeke, Katrin ^a   Fischer, Claudia ^a,b   Braus, Gerhard H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b DSMZ German Collection of Microorganisms and Cell Cultures ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYCLIC AMP; NITROGEN; PROTEIN ASC1P; PROTEIN CPC2; PROTEIN FLO11; PROTEOME; RECEPTOR FOR ACTIVATED C KINASE 1; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 2ALPHA; TRANSCRIPTION FACTOR ELF 4A; UNCLASSIFIED DRUG;

ARTICLE; CELL INTERACTION; CELL WALL; CONTROLLED STUDY; FUNGAL CELL; GENE DELETION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; RIBOSOME; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSLATION INITIATION;

AMINO ACID SEQUENCE; AMINO ACIDS; CELL ADHESION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EUKARYOTIC INITIATION FACTOR-2; GENE DELETION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE INITIATION FACTORS; PHOSPHOPROTEINS; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEX CHARACTERISTICS;

EUKARYOTA; MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 36749020117     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700184-MCP200     Document Type: Article

References (83)

1. Roberts, R. L., and Fink, G. R. (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
2. Guo, B., Styles, C. A., Feng, Q., and Fink, G. R. (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc. Natl. Acad. Sci. U S. A. 97, 12158-12163
3. Gimeno, C. J., Ljungdahl, P. O., Styles, C. A., and Fink, G. R. (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68, 1077-1090
4. Mösch, H. U., and Fink, G. R. (1997) Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145, 671-684
5. Cullen, P. J., and Sprague, G. F., Jr. (2000) Glucose depletion causes haploid invasive growth in yeast. Proc. Natl. Acad. Sci. U. S. A. 97, 13619-13624
6. Robertson, L. S., and Fink, G. R. (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc. Natl. Acad. Sci. U. S. A. 95, 13783-13787
7. Pan, X., and Heitman, J. (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 4874-4887
8. Lo, W. S., and Dranginis, A. M. (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9, 161-171
9. Lengeler, K. B., Davidson, R. C., D'Souza, C., Harashima, T., Shen, W. C., Wang, P., Pan, X., Waugh, M., and Heitman, J. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64, 746-785
10. Elion, E. A., Qi, M., and Chen, W. (2005) Signal transduction. Signaling specificity in yeast. Science 307, 687-688
11. Mösch, H. U., Kübler, E., Krappmann, S., Fink, G. R., and Braus, G. H. (1999) Grosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol. Biol. Cell 10, 1325-1335
12. Rupp, S., Summers, E., Lo, H. J., Madhani, H., and Fink, G. (1999) MAP kiase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18, 1257-1269
13. van Dyk, D., Pretorius, I. S., and Bauer, F. F. (2005) Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae. Genetics 169, 91-106
14. Braus, G. H., Grundmann, O., Brückner, S., and Mösch, H. U. (2003) Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 4272-4284
15. Hinnebusch, A. G., and Natarajan, K. (2002) Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1, 22-32
16. Dever, T. E., and Hinnebusch, A. G. (2005) GCN2 whets the appetite for amino acids. Mol. Cell 18, 141-142
17. Natarajan, K., Meyer, M. R., Jackson, B. M., Slade, D., Roberts, C., Hinnebusch, A. G., and Marton, M. J. (2001) Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21, 4347-4368
18. Kleinschmidt, M., Grundmann, O., Blüthgen, N., Mösch, H. U., and Braus, G. H. (2005) Transcriptional profiling of Saccharomyces cerevisiae cells under adhesion-inducing conditions. Mol. Genet. Genomics 273, 382-393
19. Yin, Z., Stead, D., Selway, L., Walker, J., Riba-Garcia, I., McLnerney, T., Gaskell, S., Oliver, S. G., Cash, P., and Brown, A. J. (2004) Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae. Proteomics 4, 2425-2436
20. Wek, S. A., Zhu, S., and Wek, R. C. (1995) The histidyl-tRNA synthetase-related sequence in the elF-2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15, 4497-4506
21. Dever, T. E., Feng, L., Wek, R. C., Cigan, A. M., Donahue, T. F., and Hinnebusch, A. G. (1992) Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68, 585-596
22. Zhu, S., Sobolev, A. Y., and Wek, R. C. (1996) Histidyl-tRNA synthetase-related sequences in GCN2 protein kinase regulate in vitro phosphorylation of eIF-2. J. Biol. Chem. 271, 24989-24994
23. Hao, S., Sharp, J. W., Ross-Inta, C. M., McDaniel, B. J., Anthony, T. G., Wek, R. C., Cavener, D. R., McGrath, B. C., Rudell, J. B., Koehnle, T. J., and Gietzen, D. W. (2005) Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 307, 1776-1778
24. Hinnebusch, A. G. (1997) Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272, 21661-21664
25. Komitzer, D., Raboy, B., Kulka, R. G., and Fink, G. R. (1994) Regulated degradation of the transcription factor Gcn4. EMBO J. 13, 6021-6030
26. Pries, R., Bömeke, K., Imiger, S., Grundmann, O., and Braus, G. H. (2002) Amino acid-dependent Gcn4p stability regulation occurs exclusively in the yeast nucleus. Eukaryot. Cell 1, 663-672
27. Bömeke, K., Pries, R., Korte, V., Scholz, E., Herzog, B., Schulze, F., and Braus, G. H. (2006) Yeast Gcn4p stabilization is initiated by the dissociation of the nuclear Pho85p/Pcl5p complex. Mol. Biol. Cell 17, 2952-2962
28. Hoffmann, B., Mösch, H. U., Sattlegger, E., Barthelmess, I. B., Hinnebusch, A., and Braus, G. H. (1999) The WD protein Cpc2p is required for repression of Gcn4 protein activity in yeast in the absence of amino-acid starvation. Mol. Microbiol. 31, 807-822
29. Chantrel, Y., Gaisne, M., Lions, C., and Verdiere, J. (1998) The transcriptional regulator Hap1p (Cyp1p) is essential for anaerobic or heme-deficient growth of Saccharomyces cerevisiae: Genetic and molecular characterization of an extragenic suppressor that encodes a WD repeat protein. Genetics 148, 559-569
30. Gerbasi, V. R., Weaver, C. M., Hill, S., Friedman, D. B., and Link, A. J. (2004) Yeast Asc1p and mammalian RACK1 are functionally orthologous core 40S ribosomal proteins that repress gene expression. Mol. Cell. Biol. 24, 8276-8287
31. Krüger, D., Koch, J., and Barthelmess, I. B. (1990) cpc-2, a new locus involved in general control of amino acid synthetic enzymes in Neurospora crassa. Curr. Genet. 18, 211-215
32. Müller, F., Kruger, D., Sattlegger, E., Hoffmann, B., Ballario, P., Kanaan, M., and Barthelmess, I. B. (1995) The cpc-2 gene of Neurospora crassa encodes a protein entirely composed of WD-repeat segments that is involved in general amino acid control and female fertility. Mol. Gen. Genet. 248, 162-173
33. Ron, D., Chen, C. H., Caldwell, J., Jamieson, L., Orr, E., and Mochly-Rosen, D. (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. Proc. Natl. Acad. Sci. U. S. A. 91, 839-843
34. Kleinschmidt, M., Schulz, R., and Braus, G. H. (2006) The yeast CPC2/ ASC1 gene is regulated by the transcription factors Fhl1p and Ifh1p. Curr. Genet. 49, 218-228
35. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168
36. Wessel, D., and Flügge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
37. Yan, J. X., Devenish, A. T., Wait, R., Stone, T., Lewis, S., and Fowler, S. (2002) Fluorescence two-dimensional difference gel electrophoresis and mass spectrometry based proteomic analysis of Escherichia coli. Proteomics 2, 1682-1698
38. Ray, R., and Haystead, T. A. (2003) Phosphoproteome analysis in yeast. Methods Enzymol. 366, 95-103
39. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
40. Eng, J. K., McCormack, A. L., and Yates, J. R., III (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989
41. Link, A. J., Eng, J., Schieltz, D. M., Carmack, E., Mize, G. J., Morris, D. R., Garvik, B. M., and Yates, J. R., III (1999) Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17, 676-682
42. Spurr, A. R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43
43. Venable, J. H., and Coggeshall, R. (1965) A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407-408
44. Hoppert, M., and Holzenburg, A. (2003) Electron Microscopy in Microbiology, pp. 11-18, Springer, New York
45. Cross, F. R., and Tinkelenberg, A. H. (1991) A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle. Cell 65, 875-883
46. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
47. Rose, M., and Botstein, D. (1983) Construction and use of gene fusions to lacZ (β-galactosidase) that are expressed in yeast. Methods Enzymol. 101, 167-180
48. Chang, M. Y., Hartl, F. U., Martin, J., Pollock, R. A., Kalousek, F., Neupert, W., Hallberg, E. M., Hallberg, R. L., and Horwich, A. L. (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620-625
49. Johnson, R. B., Fearon, K., Mason, T., and Jindal, S. (1989) Cloning and characterization of the yeast chaperonin HSP60 gene. Gene (Amst.) 84, 295-302
50. Krietsch, W. K. (1975) Triosephosphate isomerase from yeast. Methods Enzymol. 41, 434-438
51. Liu, H. P., and Bretscher, A. (1989) Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57, 233-242
52. Futcher, B., Latter, G. I., Monardo, P., McLaughlin, C. S., and Garrels, J. I. (1999) A sampling of the yeast proteome. Mol. Cell. Biol. 19, 7357-7368
53. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., and Brown, P. O. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257
54. Causton, H. C., Ren, B., Koh, S. S., Harbison, C. T., Kanin, E., Jennings, E. G., Lee, T. I., True, H. L., Lander, E. S., and Young, R. A. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12, 323-337
55. Brückner, S., Köhler, T., Braus, G. H., Heise, B., Bolte, M., and Mösch, H. U. (2004) Differential regulation of Tec1 by Fus3 and Kss1 confers signaling specificity in yeast development. Curr. Genet. 46, 331-342
56. Volschenk, H., Viljoen, M., Grobler, J., Petzold, B., Bauer, F., Subden, R. E., Young, R. A., Lonvaud, A., Denayrolles, M., and van Vuuren, H. J. (1997) Engineering pathways for malate degradation in Saccharomyces cerevisiae. Nat. Biotechnol. 15, 253-257
57. Pan, X., and Heitman, J. (2002) Protein kinase A operates a molecular switch that governs yeast pseudohyphal differentiation. Mol. Cell. Biol. 22, 3981-3993
58. Chasse, S. A., Flanary, P., Parnell, S. C., Hao, N., Cha, J. Y., Siderovski, D. P., and Dohlman, H. G. (2006) Genome-scale analysis reveals Sst2 as the principal regulator of mating pheromone signaling in the yeast Saccharomyces cerevisiae. Eukaryot. Cell 5, 330-346
59. Rosdahl, J. A., Mourton, T. L., and Brady-Kalnay, S. M. (2002) Protein kinase C δ (PKCδ) is required for protein tyrosine phosphatase A (PTP μ)-dependent neurite outgrowth. Mol. Cell. Neurosci. 19, 292-306
60. Hermanto, U., Zong, C. S., Li, W., and Wang, L. H. (2002) RACK1, an insulin-like growth factor 1 (IGF-1) receptor-interacting protein, modulates IGF-1-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol. Cell. Biol. 22, 2345-2365
61. Chang, B. Y., Conroy, K. B., Machleder, E. M., and Cartwright, C. A. (1998) RACK1, a receptor for activated C kinase and a homolog of the β subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18, 3245-3256
62. Gruhler, A., Olsen, J. V., Mohammed, S., Mortensen, P., Faergeman, N. J., Mann, M., and Jensen, O. N. (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell. Proteomics 4, 310-327
63. Gavin, A. C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L. J., Bastuck, S., Dumpelfeld, B., Edelmann, A., Heurtier, M. A., Hoffman, V., Hoefert, C., Klein, K., Hudak, M., Michon, A. M., Schelder, M., Schirle, M., Remor, M., Rudi, T., Hooper, S., Bauer, A., Bouwmeester, T., Casari, G., Drewes, G., Neubauer, G., Rick, J. M., Kuster, B., Bork, P., Russell, R. B., and Superti-Furga, G. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636
64. Chang, B. Y., Harte, R. A., and Cartwright, C. A. (2002) RACK1: a novel substrate for the Src protein-tyrosine kinase. Oncogene 21, 7619-7629
65. Liliental, J., and Chang, D. D. (1998) Rack1, a receptor for activated protein kinase C, interacts with integrin β subunit. J. Biol. Chem. 273, 2379-2383
66. Buensuceso, C. S., Woodside, D., Huff, J. L., Plopper, G. E., and O'Toole, T. E. (2001) The WD protein Rack1 mediates protein kinase C and integrin-dependent cell migration. J. Cell Sci. 114, 1691-1698
67. McCahill, A., Warwicker, J., Bolger, G. B., Houslay, M. D., and Yarwood, S. J. (2002) The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol. Pharmacol. 62, 1261-1273
68. Nilsson, J., Sengupta, J., Frank, J., and Nissen, P. (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep. 5, 1137-1141
69. Levin, D. E., and Bartlett-Heubusch, E. (1992) Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116, 1221-1229
70. Hoffmann, B., Wanke, C., Lapaglia, S. K., and Braus, G. H. (2000) c-Jun and RACK1 homologues regulate a control point for sexual development in Aspergillus nidulans. Mol. Microbiol. 37, 28-41
71. Jeong, H. T., Oowatari, Y., Abe, M., Tanaka, K., Matsuda, H., and Kawamukai, M. (2004) Interaction between a negative regulator (Msa2/ Nrd1) and a positive regulator (Cpc2) of sexual differentiation in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 68, 1621-1626
72. Palmer, D. A., Thompson, J. K., Li. L., Prat, A., and Wang, P. (2006) Gib2, a novel Gig-like/RACK1 homolog, functions as a Gβ subunit in cAMP signaling and is essential in Cryptococcus neoformans. J. Biol. Chem. 281, 32596-32605
73. Rothberg, K. G., Burdette, D. L., Pfannstiel, J., Jetton, N., Singh, R., and Ruben, L. (2006) The RACK1 homologue from Trypanosoma brucei is required for the onset and progression of cytokinesis. J. Biol. Chem. 281, 9781-9790
74. Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L. A., Offenhauser, N., Marchisio, P. C., and Biffo, S. (2003) Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426, 579-584
75. Smith, M. R., Jaramillo, M., Tuazon, P. T., Traugh, J. A., Liu, Y. L., Sonenberg, N., and Kung, H. F. (1991) Modulation of the mitogenic activity of eukaryotic translation initiation factor-4E by protein kinase C. New Biol. 3, 601-607
76. Linder, P. (2003) Yeast RNA helicases of the DEAD-box family involved in translation initiation. Biol. Cell 95, 157-167
77. op den Camp, R. G., and Kuhlemeier, C. (1998) Phosphorylation of tobacco eukaryotic translation initiation factor 4A upon pollen tube germination. Nucleic. Acids Res. 26, 2058-2062
78. Ibrahimo, S., Holmes, L. E., and Ashe, M. P. (2006) Regulation of translation initiation by the yeast eIF4E binding proteins is required for the pseudohyphal response. Yeast 23, 1075-1088
79. Park, Y. U., Hur, H., Ka, M., and Kim, J. (2006) Identification of translational regulation target genes during filamentous growth in Saccharomyces cerevisiae: regulatory role of Caf2O and Dhh1. Eukaryot. Cell 5, 2120-2127
80. Zeller, C. E., Parnell, S. C., and Dohlman, H. G. (2007) The RACK1 ortholog Asc1 functions as a G protein β subunit coupled to glucose responsiveness in yeast. J. Biol. Chem. 282, 25168-25176
81. McCarthy, J., Hopwood, F., Oxley, D., Laver, M., Castagna, A., Righetti, P. G., Williams, K., and Herbert, B. (2003) Carbamylation of proteins in 2-D electrophoresis-myth or reality? J. Proteome Res. 2, 239-242
82. Strittmatter, A. W., Fischer, C., Kleinschmidt, M., and Braus, G. H. (2006) FLO11 mediated filamentous growth of the yeast Saccharomyces cerevisiae depends on the expression of the ribosomall RPS26 genes. Mol. Genet. Genomics 276, 113-125
83. 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