The β subunit of the heterotrimeric G protein triggers the Kluyveromyces lactis pheromone response pathway in the absence of the γ subunit

Molecular Biology of the Cell

Volumn 21, Issue 3, 2010, Pages 489-498

  Navarro Olmos, Rocío ^a   Kawasaki, Laura ^a   Domínguez Ramírez, Lenin ^b   Ongay Larios, Laura ^a   Pérez Molina, Rosario ^a   Coria, Roberto ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; MUTANT PROTEIN; PHEROMONE; PROTEIN SUBUNIT;

ARTICLE; BETA CHAIN; KLUYVEROMYCES; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; GTP-BINDING PROTEIN ALPHA SUBUNITS; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; KLUYVEROMYCES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHEROMONES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

EID: 76049085127     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-06-0472     Document Type: Article

References (49)

1. Alspaugh, J. A., Perfect, J. R., and Heitman, J. (1997). Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 11, 3206-3217.
2. Bennett, R. J., and Johnson, A. D. (2006). The role of nutrient regulation and the Gpa2 protein in the mating pheromone response of C. albicans. Mol. Microbiol. 62, 100-119.
3. Blumer, K. J., and Thorner, J. (1990). β and γ subunits of a yeast guanine nucleotide-binding protein are not essential for membrane association of the α subunit but are required for receptor coupling. Proc. Natl. Acad. Sci. USA 87, 4363-4367.
4. Breitkreutz, A., Boucher, L., and Tyers, M. (2001). MAPK specificity in the yeast pheromone response independent of transcriptional activation. Curr. Biol. 11, 1266-1271.
5. Clapham, D. E., and Neer, E. J. (1993). New roles for G-protein beta gammadimers in transmembrane signalling. Nature 365, 403-406.
6. Dietzel, C., and Kurjan, J. (1987). The yeast Scg1 gene: a Gα-like protein implicated in the a- and α-factor response pathway. Cell 50, 1001-1010.
7. Dignard, D., André, D., and Whiteway, M. (2008). Heterotrimeric G-protein subunit function in Candida albicans: both the α and β subunits of the pheromone response G protein are required for mating. Eukaryot. Cell 7, 1591-1599.
8. Dohlman, H. G., and Thorner, J. W. (2001). Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu. Rev. Biochem. 70, 703-754.
9. Elion, E. A., Satterberg, B., and Kranz, J. E. (1993). FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol. Biol. Cell 4, 495-510.
10. Goddard, A., Ladds, G., Forfar, R., and Davey, J. (2006). Identification of Gnr1p, a negative regulator of Gα signalling in Schizosaccharomyces pombe, and its complementation by human Gβ subunits. Fungal Genet. Biol. 43, 840-851.
11. Golemis, E. A., Serebriiskii, I., Gyuris, J., and Brent, R. (1997). Interaction trap/two-hybrid system to identify interacting proteins. Curr. Protoc. Neurosci. Chapter 4, 4.4.1-4.4.36.
12. Grishin, A. V., Weiner, J. L., and Blumer, K. L. (1994). Biochemical and genetic analysis of dominant-negative mutations affecting a yeast G-proteins γ subunit. Mol. Cell. Biol. 14, 4571-4578.
13. Harashima, T., and Heitman, J. (2002). The Gα protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gβ subunits. Mol. Cell 10, 163-173.
14. Hirschman, J. E., De Zutter, G. S., Simonds, W. F., and Jenness, D. D. (1997). The Gβγ complex of the yeast pheromone response pathway. J. Biol. Chem. 272, 240-248.
15. Hirschman, J. E., and Jenness. D. D. (1999). Dual lipid modification of the yeast Gγ subunit Ste18p determines membrane localization of Gβγ. Mol. Cell. Biol. 19, 7705-7711.
16. Hsueh, Y.-P., Xue, C., and Heitman, J. (2007). G protein signaling governing cell fate decisions involves opposing Gα subunits in Cryptococcus neoformans. Mol. Biol. Cell 18, 3237-3249.
17. Inouye, C., Dhillon, N., and Thorner, J. (1997). Ste5 RING-H2 domain: role in Ste4-promoted oligomerization for yeast pheromone signaling. Science 278, 103-106.
18. Kawasaki, L., Saviñón-Tejeda, A. L., Ongay-Larios, L., Ramírez, J., and Coria, R. (2005). The Gβ(KlSte4p) subunit of the heterotrimeric G protein has a positive and essential role in the induction of mating in the yeast Kluyveromyces lactis. Yeast 22, 947-956.
19. Kawasaki, L., Castañeda-Bueno, M., Sánchez-Paredes, E., Velázquez-Zavala, N., Torres-Quiroz, F., Ongay-Larios, L., and Coria, R. (2008). Protein kinases involved in mating and osmotic stress in the yeast Kluyveromyces lactis. Eukaryot. Cell 7, 78-85.
20. Ladds, G., Goddard, A., and Davey, J. (2005). Functional analysis of heterologous GPCR signalling pathways in yeast. Trends Biotechnol. 23, 367-373.
21. Landry, S., Pettit, M., Apolinario, A., and Hoffman, C. S. (2000). The fission yeast git5 gene encodes a Gβ subunit required for glucose-triggered adenylate cyclase activation. Genetics 154, 1463-1471.
22. Landry, S., and Hoffman, C. S. (2001). The git5 Gβ and git11 Gγ form an atypical Gβγ dimer acting in the fission yeast glucose/cAMP pathway. Genetics 157, 1159-1168.
23. Leberer, E., Dignard, D., Thomas, D. Y., and Leeuw, T. A. (2000). A conserved Gβ binding (GBB) sequence motif in Ste20p/PAK family protein kinases. Biol. Chem. 381, 427-431.
24. Li, L., Shen, G., Zhang, Z. G., Wang, Y. L., Thompson, J. K., and Wang, P. (2007). Canonical heterotrimeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol. Biol. Cell 18, 4201-4209.
25. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003). Structure validation by C-alpha geometry: phi, psi, and C-beta deviation. Proteins 50: 437-450.
26. Manahan, C. L., Patnana, M., Blumer, K. J., and Linder, M. E. (2000). Dual lipid modification motifs in Gα and Gγ subunits are required for full activity of the pheromone response pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 957-968.
27. Marti-Renom, M. A., Stuart, A., Fiser, A., Sánchez, R., Melo, F., and Sali, A. (2000). Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29, 291-325.
28. Miyajima, I., Nakafuku, M., Nakayama, N., Brenner, C., Miyajima, A., Kaibuchi, K., Arai, K., Kaziro, Y., and Matsumoto, K. (1987). GPA1, a haploid-specific essential gene, encodes a yeast homolog of mammalian G protein which may be involved in mating factor signal transduction. Cell 50, 1011-1019.
29. Michaelson, D., Ahearn, I., Bergo, M., Young, S., and Philips, M. (2002). Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and golgi. Mol. Biol. Cell 13, 3294-3302.
30. Neer, E. J. (1995). Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80, 249-257.
31. Olson, K. A., Nelson, C., Tai, G., Hung, W., Yong, C., Astell, C., and Sadowski, I. (2000). Two regulators of Ste12p inhibit pheromone-responsive transcription by separate mechanisms. Mol. Cell. Biol. 20, 4199-4209.
32. Ongay-Larios, L., Saviñón-Tejeda, A., Williamson, M., Durán-Avelar, M. J., and Coria, R. (2000). The Leu132 of the Ste4(Gβ) subunit is essential for proper coupling of the G protein with the Ste2 α-factor receptor during the mating pheromone response in yeast. FEBS Lett. 467, 22-26.
33. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004). UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
34. Saviñón-Tejeda, A., Ongay-Larios, L., Ramírez, J., and Coria, R. (1996). Isolation of a gene encoding a G protein α subunit involved in the regulation of cAMP levels in the yeast Kluyveromyces lactis. Yeast 12, 1125-1133.
35. Saviñón-Tejeda, A., Ongay-Larios, L., Valdés- Rodríguez, J., and Coria, R. (2001). The KlGpa1 gene encodes a G-protein α subunit that is a positive control element in the mating pathway of the budding yeast Kluyveromyces lactis. J. Bacteriol. 183, 229-234.
36. Scannell, D. R., Butler, G., and Wolfe, K. H. (2007). Yeast genome evolutionthe origin of species. Yeast 24, 929-942.
37. Schmidt, C. J., and Neer, E. J. (1991). In vitro synthesis of G protein βγ dimers. J. Biol. Chem. 266, 4538-4544.
38. Shpakov, A., and Pertseva, M. N. (2008). Signaling systems of lower eukaryotes and their evolution. Int. Rev. Cell. Mol. Biol. 269, 151-282.
39. Sondek, J., Bohm, A., Lambright, D. J., Hamm, H. E., and Sigler, P. B. (1996). Crystal structure of a G-protein βγ dimer at 2.1 Å resolution. Nature 379, 369-374.
40. Wall, M. A., Coleman, D. E., Lee, E., Iñiguez-Lluhi, J. A., Posner, B. A., Gilman, A. G., and Sprang, S. R. (1995). The structure of the G protein heterotrimer Giα1β1γ2. Cell 83, 1047-1058.
41. Wang, P., Perfect, J. R., and Heitman, J. (2000). The G-protein beta subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell. Biol. 20, 352-362.
42. Welton, R. M., and Hoffman, C. S. (2000). Glucose monitoring in fission yeast via the gpa2 Gα, the git5 Gβ, and the git3 putative glucose receptor. Genetics 156, 513-521.
43. Westfall, P. J., Patterson, J. C., Chen, R. E., and Thorner, J. (2008). Stress resistance and signal fidelity independent of nuclear MAPK function. Proc. Natl. Acad. Sci. USA 105, 12212-12217.
44. Whiteway, M., Hougan, L., Dignard, D., Thomas, D. Y., Bell, L., Saari, G. C., Grant, F. J., O'Hara, P., and MacKay, V. L. (1989). The Ste4 and Ste18 genes of yeast encode potential β and γ subunits of the mating factor receptor-coupled G protein. Cell 56, 467-477.
45. Whiteway, M., and Thomas, D. Y. (1994). Site-directed mutations altering the CAAX box of Ste18, the yeast pheromone-response pathway Gγ subunit. Genetics 137, 967-976.
46. Whiteway, M., Clark, K. L., Leberer, E., Dignard, D., and Thomas, D. Y. (1994). Genetic identification of residues involved in association of α and β G-protein subunits. Mol. Cell. Biol. 14, 3223-3229.
47. Whiteway, M., Wu, C., Leeuw, T., Clark, K., Fourest-Lieuvin, A., Thomas, D. Y., and Leberer, E. (1995). Association of the yeast pheromone response G protein βγ subunits with the MAP Kinase scaffold Ste5p. Science 269, 1572-1575.
48. Zhang, F. L., and Casey, P. J. (1996). Influence of metal ions on substrate binding and catalytic activity of mammalian protein geranylgeranyltransferase type-I. Biochem J. 320, 925-932.
49. Zheng, Y., Cerione, R., and Bender, A. (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.