Guanine nucleotide-binding protein (Gα) endocytosis by a cascade of ubiquitin binding domain proteins is required for sustained morphogenesis and proper mating in yeast

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 15052-15063

  Dixit, Gauri ^a   Baker, Rachael ^a   Sacks, Carly M ^b   Torres, Matthew P ^c   Dohlman, Henrik G ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; ENZYME ACTIVITY; MOLECULAR BIOLOGY; MORPHOLOGY; SIGNAL TRANSDUCTION; YEAST;

CELL SURFACE RECEPTORS; CELLULAR MORPHOGENESIS; ENDOMEMBRANE COMPARTMENTS; GENE DELETION MUTANTS; GUANINE NUCLEOTIDE-BINDING PROTEINS; HETEROTRIMERIC G PROTEINS; POST-TRANSLATIONAL MODIFICATIONS; SIGNALING PROTEINS;

PROTEINS;

BUL1 PROTEIN; CELL PROTEIN; DDI1 PROTEIN; EDE1 PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT 1; PHEROMONE; RUP1 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; GENE DELETION; MATING SYSTEM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; UBIQUITINATION; YEAST;

ENDOCYTOSIS; G PROTEINS; PROTEIN DOMAINS; PROTEIN PURIFICATION; UBIQUITINATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CARRIER PROTEINS; CROSSES, GENETIC; ENDOCYTOSIS; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; IMMUNOBLOTTING; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TIME-LAPSE IMAGING; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84901425427     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.566117     Document Type: Article

References (73)

1. Sprang, S. R. (1997) G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66, 639-678 (Pubitemid 27274670)
2. Ross, E. M., and Wilkie, T. M. (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGSlike proteins. Annu. Rev. Biochem. 69, 795-827
3. Berman, D. M., Wilkie, T. M., and Gilman, A. G. (1996) GAIP and RGS4 Are GTPase-activating proteins for the Gi subfamily of G protein subunits. Cell 86, 445-452 (Pubitemid 26272084)
4. Dohlman, H. G., and Jones, J. C. (2012) Signal activation and inactivation by the Gα helical domain: a long-neglected partner in G protein signaling. Sci. Signal. 5, re2
5. Mixon, M. B., Lee, E., Coleman, D. E., Berghuis, A. M., Gilman, A. G., and Sprang, S. R. (1995) Tertiary and quaternary structural changes in Giα induced by GTP hydrolysis. Science 270, 954-960
6. Westfield, G. H., Rasmussen, S. G., Su, M., Dutta, S., DeVree, B. T., Chung, K. Y., Calinski, D., Velez-Ruiz, G., Oleskie, A. N., Pardon, E., Chae, P. S., Liu, T., Li, S., Woods, V. L., Jr., Steyaert, J., Kobilka, B. K., Sunahara, R. K., and Skiniotis, G. (2011) Structural flexibility of the Gαsα-helical domain in the β2-adrenoceptor Gs complex. Proc. Natl. Acad. Sci. U.S.A. 108, 16086-16091
7. Van Eps, N., Preininger, A. M., Alexander, N., Kaya, A. I., Meier, S., Meiler, J., Hamm, H. E., and Hubbell, W. L. (2011) Interaction of a G protein with an activated receptor opens the interdomain interface in the α subunit. Proc. Natl. Acad. Sci. U.S.A. 108, 9420-9424
8. Wedegaertner, P. B. (2012) G protein trafficking. In GPCR Signalling Complexes-Synthesis, Assembly, Trafficking, and Specificity (Dupré, D. J., Hébert, T. E., and Jockers, R., eds.) pp. 193-223, Springer, The Netherlands
9. qα mediates long-term adaptation in Drosophila photoreceptors. J. Neurosci. 27, 5571-5583 (Pubitemid 350021065)
10. Chisari, M., Saini, D. K., Kalyanaraman, V., and Gautam, N. (2007) Shuttling of G protein subunits between the plasma membrane and intracellular membranes. J. Biol. Chem. 282, 24092-24098 (Pubitemid 47328053)
11. sα. Mol. Biol. Cell 7, 1225-1233
12. Slessareva, J. E., Routt, S. M., Temple, B., Bankaitis, V. A., and Dohlman, H. G. (2006) Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein α subunit at the endosome. Cell 126, 191-203
13. Backer, J. M. (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem. J. 410, 1-17 (Pubitemid 351300321)
14. Irannejad, R., Tomshine, J. C., Tomshine, J. R., Chevalier, M., Mahoney, J. P., Steyaert, J., Rasmussen, S. G., Sunahara, R. K., El-Samad, H., Huang, B., and von Zastrow, M. (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534-538
15. Murphy, J. E., Padilla, B. E., Hasdemir, B., Cottrell, G. S., and Bunnett, N. W. (2009) Endosomes: a legitimate platform for the signaling train. Proc. Natl. Acad. Sci. U.S.A. 106, 17615-17622
16. Hicke, L., and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287
17. Hicke, L. (1999) Gettin' down with ubiquitin: turning off cell-surface receptors, transporters, and channels. Trends Cell Biol. 9, 107-112 (Pubitemid 29151787)
18. Zhu, M., Torres, M. P., Kelley, J. B., Dohlman, H. G., and Wang, Y. (2011) Pheromone- and RSP5-dependent ubiquitination of the G protein β subunit Ste4 in yeast. J. Biol. Chem. 286, 27147-27155
19. Shaw, J. D., Cummings, K. B., Huyer, G., Michaelis, S., and Wendland, B. (2001) Yeast as a model system for studying endocytosis. Exp. Cell Res. 271, 1-9 (Pubitemid 33070987)
20. Tardiff, D. F., Jui, N. T., Khurana, V., Tambe, M. A., Thompson, M. L., Chung, C. Y., Kamadurai, H. B., Kim, H. T., Lancaster, A. K., Caldwell, K. A., Caldwell, G. A., Rochet, J.-C., Buchwald, S. L., and Lindquist, S. (2013) Yeast reveal a "Druggable" Rsp5/Nedd4 network that ameliorates α-synuclein toxicity in neurons. Science 342, 979-983
21. Shih, S. C., Sloper-Mould, K. E., and Hicke, L. (2000) Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J. 19, 187-198 (Pubitemid 30042701)
22. Sloper-Mould, K. E., Jemc, J. C., Pickart, C. M., and Hicke, L. (2001) Distinct functional surface regions on ubiquitin. J. Biol. Chem. 276, 30483-30489
23. Husnjak, K., and Dikic, I. (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322
24. Dohlman, H. G., and Thorner, J. (2001) Regulation of G protein initiated signal transduction in yeast: paradigms and principles. Annu. Rev. Biochem. 70, 703-754 (Pubitemid 32662223)
25. Wang, Y., Marotti, L. A., Jr., Lee, M. J., and Dohlman, H. G. (2005) Differential regulation of G protein α subunit trafficking by mono- and polyubiquitination, J. Biol. Chem. 280, 284-291 (Pubitemid 40164991)
26. Torres, M. P., Lee, M. J., Ding, F., Purbeck, C., Kuhlman, B., Dokholyan, N. V., and Dohlman, H. G. (2009) G protein mono-ubiquitination by the Rsp5 ubiquitin ligase. J. Biol. Chem. 284, 8940-8950
27. Dunn, R., and Hicke, L. (2001) Domains of the Rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis. Mol. Biol. Cell 12, 421-435 (Pubitemid 33051585)
28. Marotti, L. A., Jr., Newitt, R., Wang, Y., Aebersold, R., and Dohlman, H. G. (2002) Direct identification of a G protein ubiquitination site by mass spectrometry. Biochemistry 41, 5067-5074 (Pubitemid 34411660)
29. Cappell, S. D., Baker, R., Skowyra, D., and Dohlman, H. G. (2010) Systematic analysis of essential genes reveals important regulators of G protein signaling. Mol. Cell 38, 746-757
30. Li, X., Gerber, S. A., Rudner, A. D., Beausoleil, S. A., Haas, W., Villén, J., Elias, J. E., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of β-factor-arrested Saccharomyces cerevisiae. J. Proteome Res. 6, 1190-1197 (Pubitemid 46480484)
31. Torres, M. P., Clement, S. T., Cappell, S. D., and Dohlman, H. G. (2011) Cell cycle-dependent phosphorylation and ubiquitination of aGprotein α subunit. J. Biol. Chem. 286, 20208-20216
32. Coleman, D. E., Berghuis, A. M., Lee, E., Linder, M. E., Gilman, A. G., and Sprang, S. R. (1994) Structures of active conformations of Gi α1 and the mechanism of GTP hydrolysis. Science 265, 1405-1412
33. Hoffman, G. A., Garrison, T. R., and Dohlman, H. G. (2002) Analysis of RGS proteins in Saccharomyces cerevisiae. Methods Enzymol. 344, 617-631
34. Song, J., Hirschman, J., Gunn, K., and Dohlman, H. G. (1996) Regulation of membrane and subunit interactions by N-myristoylation of a G protein α subunit in yeast. J. Biol. Chem. 271, 20273-20283 (Pubitemid 26281792)
35. Clarke, T. F., 4th, and Clark, P. L. (2008) Rare codons cluster. PLoS ONE 3, e3412
36. Isom, D. G., Sridharan, V., Baker, R., Clement, S. T., Smalley, D. M., and Dohlman, H. G. (2013) Protons as second messenger regulators of G protein signaling. Mol. Cell 51, 531-538
37. Isom, D. G., Marguet, P. R., Oas, T. G., and Hellinga, H. W. (2011) A miniaturized technique for assessing protein thermodynamics and function using fast determination of quantitative cysteine reactivity. Proteins 79, 1034-1047
38. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 (Pubitemid 28062863)
39. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808
40. Lee, M. J., and Dohlman, H. G. (2008) Coactivation of G protein signaling by cell-surface receptors and an intracellular exchange factor. Curr. Biol. 18, 211-215 (Pubitemid 351192317)
41. Dohlman, H. G., Goldsmith, P., Spiegel, A. M., and Thorner, J. (1993) Pheromone action regulates G-protein α-subunit myristoylation in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 90, 9688-9692 (Pubitemid 23315851)
42. Hao, N., Nayak, S., Behar, M., Shanks, R. H., Nagiec, M. J., Errede, B., Hasty, J., Elston, T. C., and Dohlman, H. G. (2008) Regulation of cell signaling dynamics by the protein kinase-scaffold Ste5. Mol. Cell 30, 649-656 (Pubitemid 351755062)
43. Sprague, G. F., Jr. (1991) Assay of yeast mating reaction. Methods Enzymol. 194, 77-93
44. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R. R., Mohan, A., Heyen, J. W., Goebl, M. G., and Iakoucheva, L. M. (2010) Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78, 365-380
45. Jones, J. C., Jones, A. M., Temple, B. R., and Dohlman, H. G. (2012) Differences in intradomain and interdomain motion confer distinct activation properties to structurally similar Gα proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 7275-7279
46. Higashijima, T., Ferguson, K. M., Sternweis, P. C., Ross, E. M., Smigel, M. D., and Gilman, A. G. (1987) The effect of activating ligands on the intrinsic fluorescence of guanine nucleotide-binding regulatory proteins. J. Biol. Chem. 262, 752-756 (Pubitemid 17005248)
47. Hurley, J. H., and Stenmark, H. (2011) Molecular mechanisms of ubiquitin- dependent membrane traffic. Annu. Rev. Biophys. 40, 119-142
48. Hicke, L., Schubert, H. L., and Hill, C. P. (2005) Ubiquitin-binding domains. Nat. Rev. Mol. Cell. Biol. 6, 610-621 (Pubitemid 41081265)
49. Dikic, I., Wakatsuki, S., and Walters, K. J. (2009) Ubiquitin-binding domains: from structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671
50. Winzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., Chu, A. M., Connelly, C., Davis, K., Dietrich, F., Dow, S. W., El Bakkoury, M., Foury, F., Friend, S. H., Gentalen, E., Giaever, G., Hegemann, J. H., Jones, T., Laub, M., Liao, H., Liebundguth, N., Lockhart, D. J., Lucau-Danila, A., Lussier, M., M'Rabet, N., Menard, P., Mittmann, M., Pai, C., Rebischung, C., Revuelta, J. L., Riles, L., Roberts, C. J., Ross-MacDonald, P., Scherens, B., Snyder, M., Sookhai-Mahadeo, S., Storms, R. K., Véronneau, S., Voet, M., Volckaert, G., Ward, T. R., Wysocki, R., Yen, G. S., Yu, K., Zimmermann, K., Philippsen, P., Johnston, M., and Davis, R. W. (1999) Functional characterization of the S. Cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906 (Pubitemid 29381993)
51. Hurley, J. H. (2010) The ESCRT complexes. Crit. Rev. Biochem. Mol. Biol. 45, 463-487
52. MacGurn, J. A., Hsu, P.-C., and Emr, S. D. (2012) Ubiquitin and membrane protein turnover: from cradle to grave. Annu. Rev. Biochem. 81, 231-259
53. Donaldson, K. M., Yin, H., Gekakis, N., Supek, F., and Joazeiro, C. A. (2003) Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262 (Pubitemid 36178306)
54. Betz, W. J., Mao, F., and Smith, C. B. (1996) Imaging exocytosis and endocytosis. Curr. Opin. Neurobiol. 6, 365-371 (Pubitemid 26235686)
55. Yashiroda, H., Oguchi, T., Yasuda, Y., Toh-E. A., and Kikuchi, Y. (1996) Bul1, a new protein that binds to the Rsp5 ubiquitin ligase in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 3255-3263
56. Gagny, B., Wiederkehr, A., Dumoulin, P., Winsor, B., Riezman, H., and Haguenauer-Tsapis, R. (2000) A novel EH domain protein of Saccharomyces cerevisiae, Ede1p, involved in endocytosis. J. Cell Sci. 113, 3309-3319
57. Liu, Y., and Xiao, W. (1997) Bidirectional regulation of two DNA-damageinducible genes, MAG1 and DDI1, from Saccharomyces cerevisiae. Mol. Microbiol. 23, 777-789 (Pubitemid 27072938)
58. Lam, M. H., and Emili, A. (2013) Ubp2 regulates Rsp5 ubiquitination activity in vivo and in vitro. PLoS ONE 8, e75372
59. Pruyne, D., and Bretscher, A. (2000) Polarization of cell growth in yeast. J. Cell Sci. 113, 571-585
60. Tanaka, H., and Yi, T.-M. (2010) The effects of replacing Sst2 with the heterologous RGS4 on polarization and mating in yeast. Biophys. J. 99, 1007-1017
61. Abe, F., and Iida, H. (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol. Cell. Biol. 23, 7566-7584 (Pubitemid 37271457)
62. Hiraki, T., and Abe, F. (2010) Overexpression of Sna3 stabilizes tryptophan permease Tat2, potentially competing for theWWdomain of Rsp5 ubiquitin ligase with its binding protein Bul1. FEBS Lett. 584, 55-60
63. Gabriely, G., Kama, R., Gelin-Licht, R., and Gerst, J. E. (2008) Different domains of the UBL-UBA ubiquitin receptor, Ddi1/Vsm1, are involved in its multiple cellular roles. Mol. Biol. Cell 19, 3625-3637
64. Dores, M. R., Schnell, J. D., Maldonado-Baez, L., Wendland, B., and Hicke, L. (2010) The function of yeast epsin and Ede1 ubiquitin-binding domains during receptor internalization. Traffic 11, 151-160
65. Shih, S. C., Katzmann, D. J., Schnell, J. D., Sutanto, M., Emr, S. D., and Hicke, L. (2002) Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389-393 (Pubitemid 34521036)
66. Clement, S. T., Dixit, G., and Dohlman, H. G. (2013) Regulation of yeast G protein signaling by the kinases that activate theAMPKhomolog Snf1. Sci. Signal. 6, ra78
67. Sokolov, M., Lyubarsky, A. L., Strissel, K. J., Savchenko, A. B., Govardovskii, V. I., Pugh, E. N., Jr., and Arshavsky, V. Y. (2002) Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation. Neuron 34, 95-106 (Pubitemid 34270701)
68. Rojas, A. M., Fuentes, G., Rausell, A., and Valencia, A. (2012) The Ras protein superfamily: evolutionary tree and role of conserved amino acids. J. Cell Biol. 196, 545
69. Zong, H., Kaibuchi, K., and Quilliam, L. A. (2001) The insert region of RhoA is essential for Rho kinase activation and cellular transformation. Mol. Cell. Biol. 21, 5287-5298 (Pubitemid 32702434)
70. Visvikis, O., Lorès, P., Boyer, L., Chardin, P., Lemichez, E., and Gacon, G. (2008) Activated Rac1, but not the tumorigenic variant Rac1b, is ubiquitinated on Lys-147 through a JNK-regulated process. FEBS J. 275, 386-396
71. Sasaki, A. T., Carracedo, A., Locasale, J. W., Anastasiou, D., Takeuchi, K., Kahoud, E. R., Haviv, S., Asara, J. M., Pandolfi, P. P., and Cantley, L. C. (2011) Ubiquitination of K-Ras enhances activation and facilitates binding to select downstream effectors. Sci. Signal. 4, ra13
72. Baker, R., Wilkerson, E. M., Sumita, K., Isom, D. G., Sasaki, A. T., Dohlman, H. G., and Campbell, S. L. (2013) Differences in the regulation of K-Ras and H-Ras isoforms by monoubiquitination. J. Biol. Chem. 288, 36856-36862
73. Baker, R., Lewis, S. M., Sasaki, A. T., Wilkerson, E. M., Locasale, J. W., Cantley, L. C., Kuhlman, B., Dohlman, H. G., and Campbell, S. L. (2013) Site-specific monoubiquitination activates Ras by impeding GTPase-activating protein function. Nat. Struct. Mol. Biol. 20, 46-52