The Phosducin-Like Protein PhLP1 Is Essential for Gβγ Dimer Formation in Dictyostelium discoideum

REFERENCES

• Aloy, P., B. Bottcher, H. Ceulemans, C. Leutwein, C. Mellwig, S. Fischer, A. C. Gavin, P. Bork, G. Superti-Furga, L. Serrano, and R. B. Russell. 2004. Structure-based assembly of protein complexes in yeast. Science 303:2026–2029.
   PubMed Web of Science ®Google Scholar
• Bauer, P. H., S. Muller, M. Puzicha, S. Pippig, B. Obermaier, E. J. Helmreich, and M. J. Lohse. 1992. Phosducin is a protein kinase A-regulated G-protein regulator. Nature 358:73–76.
   PubMedGoogle Scholar
• Blaauw, M., J. C. Knol, A. Kortholt, J. Roelofs, R. Engel, M. Postma, A. J. Visser, and P. J. van Haastert. 2003. Phosducin-like proteins in Dictyostelium discoideum: implications for the phosducin family of proteins. EMBO J. 22:5047–5057.
   PubMedGoogle Scholar
• Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604–1607.
   PubMed Web of Science ®Google Scholar
• Brock, R., G. Vamosi, G. Vereb, and T. M. Jovin. 1999. Rapid characterization of green fluorescent protein fusion proteins on the molecular and cellular level by fluorescence correlation microscopy. Proc. Natl. Acad. Sci. USA 96:10123–10128.
   PubMedGoogle Scholar
• Clapham, D. E., and E. J. Neer. 1997. G protein beta gamma subunits. Annu. Rev. Pharmacol. Toxicol. 37:167–203.
   PubMed Web of Science ®Google Scholar
• Dues, G., S. Muller, and N. Johnsson. 2001. Detection of a conformational change in G gamma upon binding G beta in living cells. FEBS Lett. 505:75–80.
   PubMedGoogle Scholar
• Feldman, D. E., V. Thulasiraman, R. G. Ferreyra, and J. Frydman. 1999. Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol. Cell 4:1051–1061.
   PubMed Web of Science ®Google Scholar
• Flanary, P. L., P. R. DiBello, P. Estrada, and H. G. Dohlman. 2000. Functional analysis of Plp1 and Plp2, two homologues of phosducin in yeast. J. Biol. Chem. 275:18462–18469.
   PubMed Web of Science ®Google Scholar
• Frydman, J. 2001. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 70:603–647.
   PubMed Web of Science ®Google Scholar
• Garcia-Higuera, I., J. Fenoglio, Y. Li, C. Lewis, M. P. Panchenko, O. Reiner, T. F. Smith, and E. J. Neer. 1996. Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein beta subunit. Biochemistry 35:13985–13994.
   PubMedGoogle Scholar
• Garcia-Higuera, I., C. Gaitatzes, T. F. Smith, and E. J. Neer. 1998. Folding a WD repeat propeller. Role of highly conserved aspartic acid residues in the G protein beta subunit and Sec13. J. Biol. Chem. 273:9041–9049.
   PubMed Web of Science ®Google Scholar
• Gaudet, R., A. Bohm, and P. B. Sigler. 1996. Crystal structure at 2.4 angstroms resolution of the complex of transducin betagamma and its regulator, phosducin. Cell 87:577–588.
   PubMed Web of Science ®Google Scholar
• Graber, S. G., R. A. Figler, V. K. Kalman-Maltese, J. D. Robishaw, and J. C. Garrison. 1992. Expression of functional G protein beta gamma dimers of defined subunit composition using a baculovirus expression system. J. Biol. Chem. 267:13123–13126.
   PubMed Web of Science ®Google Scholar
• Gutsche, I., L. O. Essen, and W. Baumeister. 1999. Group II chaperonins: new TRiC(k)s and turns of a protein folding machine. J. Mol. Biol. 293:295–312.
   PubMedGoogle Scholar
• Hansen, W. J., M. Ohh, J. Moslehi, K. Kondo, W. G. Kaelin, and W. J. Welch. 2002. Diverse effects of mutations in exon II of the von Hippel-Lindau (VHL) tumor suppressor gene on the interaction of pVHL with the cytosolic chaperonin and pVHL-dependent ubiquitin ligase activity. Mol. Cell. Biol. 22:1947–1960.
   PubMed Web of Science ®Google Scholar
• Hartl, F. U., and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858.
   PubMed Web of Science ®Google Scholar
• Hawes, B. E., K. Touhara, H. Kurose, R. J. Lefkowitz, and J. Inglese. 1994. Determination of the G beta gamma-binding domain of phosducin. A regulatable modulator of G beta gamma signaling. J. Biol. Chem. 269:29825–29830.
   PubMedGoogle Scholar
• Hekman, M., P. H. Bauer, P. Sohlemann, and M. J. Lohse. 1994. Phosducin inhibits receptor phosphorylation by the beta-adrenergic receptor kinase in a PKA-regulated manner. FEBS Lett. 343:120–124.
   PubMedGoogle Scholar
• Hess, S. T., S. Huang, A. A. Heikal, and W. W. Webb. 2002. Biological and chemical applications of fluorescence correlation spectroscopy: a review. Biochemistry 41:697–705.
   PubMed Web of Science ®Google Scholar
• Higgins, J. B., and P. J. Casey. 1994. In vitro processing of recombinant G protein gamma subunits. Requirements for assembly of an active beta gamma complex. J. Biol. Chem. 269:9067–9073.
   PubMedGoogle Scholar
• Higgins, J. B., and P. J. Casey. 1996. The role of prenylation in G-protein assembly and function. Cell. Signal. 8:433–437.
   PubMed Web of Science ®Google Scholar
• Hink, M. A., J. W. Borst, and A. J. Visser. 2003. Fluorescence correlation spectroscopy of GFP fusion proteins in living plant cells. Methods Enzymol. 361:93–112.
   PubMedGoogle Scholar
• Hirschman, J. E., G. S. De Zutter, W. F. Simonds, and D. D. Jenness. 1997. The G beta gamma complex of the yeast pheromone response pathway. Subcellular fractionation and protein-protein interactions. J. Biol. Chem. 272:240–248.
   PubMedGoogle Scholar
• Humrich, J., C. Bermel, M. Bunemann, L. Harmark, R. Frost, U. Quitterer, and M. J. Lohse. 2005. Phosducin-like protein regulates G-protein βγ folding by interaction with tailless complex polypeptide-1α: dephosphorylation or splicing of PhLP turns the switch toward regulation of Gβγ folding. J. Biol. Chem. 280:20042–20050.
   PubMed Web of Science ®Google Scholar
• Janetopoulos, C., T. Jin, and P. Devreotes. 2001. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 291:2408–2411.
   PubMed Web of Science ®Google Scholar
• Jin, T., N. Zhang, Y. Long, C. A. Parent, and P. N. Devreotes. 2000. Localization of the G protein betagamma complex in living cells during chemotaxis. Science 287:1034–1036.
   PubMed Web of Science ®Google Scholar
• Justice, J. M., J. J. Murtagh, Jr., J. Moss, and M. Vaughan. 1995. Hydrophobicity and subunit interactions of rod outer segment proteins investigated using Triton X-114 phase partitioning. J. Biol. Chem. 270:17970–17976.
   PubMedGoogle Scholar
• Kasahara, S., P. Wang, and D. L. Nuss. 2000. Identification of bdm-1, a gene involved in G protein beta-subunit function and alpha-subunit accumulation. Proc. Natl. Acad. Sci. USA 97:412–417.
   PubMed Web of Science ®Google Scholar
• Kim, S. A., and P. Schwille. 2003. Intracellular applications of fluorescence correlation spectroscopy: prospects for neuroscience. Curr. Opin. Neurobiol. 13:583–590.
   PubMedGoogle Scholar
• Lacefield, S., and F. Solomon. 2003. A novel step in beta-tubulin folding is important for heterodimer formation in Saccharomyces cerevisiae. Genetics 165:531–541.
   PubMed Web of Science ®Google Scholar
• Lee, R. H., B. S. Lieberman, and R. N. Lolley. 1987. A novel complex from bovine visual cells of a 33,000-dalton phosphoprotein with beta- and gamma-transducin: purification and subunit structure. Biochemistry 26:3983–3990.
   PubMedGoogle Scholar
• Lee, R. H., T. D. Ting, B. S. Lieberman, D. E. Tobias, R. N. Lolley, and Y. K. Ho. 1992. Regulation of retinal cGMP cascade by phosducin in bovine rod photoreceptor cells. Interaction of phosducin and transducin. J. Biol. Chem. 267:25104–25112.
   PubMedGoogle Scholar
• Leroux, M. R., and F. U. Hartl. 2000. Protein folding: versatility of the cytosolic chaperonin TRiC/CCT. Curr. Biol. 10:R260–R264.
   PubMedGoogle Scholar
• Li, W. Z., P. Lin, J. Frydman, T. R. Boal, T. S. Cardillo, L. M. Richard, D. Toth, M. A. Lichtman, F. U. Hartl, F. Sherman, et al. 1994. Tcp20, a subunit of the eukaryotic TRiC chaperonin from humans and yeast. J. Biol. Chem. 269:18616–18622.
   PubMedGoogle Scholar
• Lilly, P., L. Wu, D. L. Welker, and P. N. Devreotes. 1993. A G-protein beta-subunit is essential for Dictyostelium development. Genes Dev. 7:986–995.
   PubMedGoogle Scholar
• Linskens, M. H., P. D. Grootenhuis, M. Blaauw, B. Huisman-de Winkel, A. Van Ravestein, P. J. Van Haastert, and J. C. Heikoop. 1999. Random mutagenesis and screening of complex glycoproteins: expression of human gonadotropins in Dictyostelium discoideum. FASEB J. 13:639–645.
   PubMedGoogle Scholar
• Loew, A., Y. K. Ho, T. Blundell, and B. Bax. 1998. Phosducin induces a structural change in transducin beta gamma. Structure 6:1007–1019.
   PubMedGoogle Scholar
• Lukov, G. L., T. Hu, J. N. McLaughlin, H. E. Hamm, and B. M. Willardson. 2005. Phosducin-like protein acts as a molecular chaperone for G protein betagamma dimer assembly. EMBO J. 24:1965–1975.
   PubMed Web of Science ®Google Scholar
• Martin-Benito, J., S. Bertrand, T. Hu, P. J. Ludtke, J. N. McLaughlin, B. M. Willardson, J. L. Carrascosa, and J. M. Valpuesta. 2004. Structure of the complex between the cytosolic chaperonin CCT and phosducin-like protein. Proc. Natl. Acad. Sci. USA 101:17410–17415.
   PubMedGoogle Scholar
• McLaughlin, J. N., C. D. Thulin, S. M. Bray, M. M. Martin, T. S. Elton, and B. M. Willardson. 2002. Regulation of angiotensin II-induced G protein signaling by phosducin-like protein. J. Biol. Chem. 277:34885–34895.
   PubMedGoogle Scholar
• McLaughlin, J. N., C. D. Thulin, S. J. Hart, K. A. Resing, N. G. Ahn, and B. M. Willardson. 2002. Regulatory interaction of phosducin-like protein with the cytosolic chaperonin complex. Proc. Natl. Acad. Sci. USA 99:7962–7967.
   PubMed Web of Science ®Google Scholar
• Medina, M. A., and P. Schwille. 2002. Fluorescence correlation spectroscopy for the detection and study of single molecules in biology. Bioessays 24:758–764.
   PubMed Web of Science ®Google Scholar
• Mende, U., C. J. Schmidt, F. Yi, D. J. Spring, and E. J. Neer. 1995. The G protein gamma subunit. Requirements for dimerization with beta subunits. J. Biol. Chem. 270:15892–15898.
   PubMedGoogle Scholar
• Muntz, K. H., P. C. Sternweis, A. G. Gilman, and S. M. Mumby. 1992. Influence of gamma subunit prenylation on association of guanine nucleotide-binding regulatory proteins with membranes. Mol. Biol. Cell 3:49–61.
   PubMedGoogle Scholar
• Murzin, A. G. 1992. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 14:191–201.
   PubMedGoogle Scholar
• Neer, E. J., C. J. Schmidt, R. Nambudripad, and T. F. Smith. 1994. The ancient regulatory-protein family of WD-repeat proteins. Nature 371:297–300.
   PubMed Web of Science ®Google Scholar
• Neer, E. J., and T. F. Smith. 2000. A groovy new structure. Proc. Natl. Acad. Sci. USA 97:960–962.
   PubMedGoogle Scholar
• Ormo, M., A. B. Cubitt, K. Kallio, L. A. Gross, R. Y. Tsien, and S. J. Remington. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273:1392–1395.
   PubMed Web of Science ®Google Scholar
• Postma, M., J. Roelofs, J. Goedhart, T. W. J. Gadella, A. J. W. G. Visser, and P. J. M. Van Haastert. 2003. Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia. Mol. Biol. Cell 14:5019–5027.
   PubMedGoogle Scholar
• Pronin, A. N., and N. Gautam. 1993. Proper processing of a G protein gamma subunit depends on complex formation with a beta subunit. FEBS Lett. 328:89–93.
   PubMedGoogle Scholar
• Ruchira, M. A. Hink, L. Bosgraaf, P. J. van Haastert, and A. J. Visser. 2004. Pleckstrin homology domain diffusion in Dictyostelium cytoplasm studied using fluorescence correlation spectroscopy. J. Biol. Chem. 279:10013–10019.
   PubMedGoogle Scholar
• Savage, J. R., J. N. McLaughlin, N. P. Skiba, H. E. Hamm, and B. M. Willardson. 2000. Functional roles of the two domains of phosducin and phosducin-like protein. J. Biol. Chem. 275:30399–30407.
   PubMedGoogle Scholar
• Schagger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368–379.
   PubMed Web of Science ®Google Scholar
• Schmidt, C. J., and E. J. Neer. 1991. In vitro synthesis of G protein beta gamma dimers. J. Biol. Chem. 266:4538–4544.
   PubMedGoogle Scholar
• Schmidt, C. J., T. C. Thomas, M. A. Levine, and E. J. Neer. 1992. Specificity of G protein beta and gamma subunit interactions. J. Biol. Chem. 267:13807–13810.
   PubMed Web of Science ®Google Scholar
• Schroder, S., K. Bluml, C. Dees, and M. J. Lohse. 1997. Identification of a C-terminal binding site for G-protein betagamma-subunits in phosducin-like protein. FEBS Lett. 401:243–246.
   PubMedGoogle Scholar
• Schroder, S., and M. J. Lohse. 1996. Inhibition of G-protein betagamma-subunit functions by phosducin-like protein. Proc. Natl. Acad. Sci. USA 93:2100–2104.
   PubMedGoogle Scholar
• Siegers, K., B. Bolter, J. P. Schwarz, U. M. Bottcher, S. Guha, and F. U. Hartl. 2003. TRiC/CCT cooperates with different upstream chaperones in the folding distinct protein classes. EMBO J. 22:5230–5240.
   PubMedGoogle Scholar
• Simonds, W. F., J. E. Butrynski, N. Gautam, C. G. Unson, and A. M. Spiegel. 1991. G-protein beta gamma dimers. Membrane targeting requires subunit coexpression and intact gamma C-A-A-X domain. J. Biol. Chem. 266:5363–5366.
   PubMedGoogle Scholar
• Skakun, V. V., M. A. Hink, A. V. Digris, E. R., E. G. Novikov, V. V. Apanasovic, and A. J. W. G. Visser. 2005. Global analysis of fluorescence fluctuation data. Eur. Biophys. J. 34:323–334.
   PubMedGoogle Scholar
• Smith, T. F., C. Gaitatzes, K. Saxena, and E. J. Neer. 1999. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:181–185.
   PubMed Web of Science ®Google Scholar
• Sondek, J., A. Bohm, D. G. Lambright, H. E. Hamm, and P. B. Sigler. 1996. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379:369–374.
   PubMed Web of Science ®Google Scholar
• Thibault, C., M. W. Sganga, and M. F. Miles. 1997. Interaction of phosducin-like protein with G protein betagamma subunits. J. Biol. Chem. 272:12253–12256.
   PubMedGoogle Scholar
• Ursic, D., and M. R. Culbertson. 1991. The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol. Cell. Biol. 11:2629–2640.
   PubMedGoogle Scholar
• Valpuesta, J. M., J. Martin-Benito, P. Gomez-Puertas, J. L. Carrascosa, and K. R. Willison. 2002. Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett. 529:11–16.
   PubMedGoogle Scholar
• Wang, Q., B. K. Mullah, and J. D. Robishaw. 1999. Ribozyme approach identifies a functional association between the G protein beta1gamma7 subunits in the beta-adrenergic receptor signaling pathway. J. Biol. Chem. 274:17365–17371.
   PubMed Web of Science ®Google Scholar
• Wu, L., R. Valkema, P. J. Van Haastert, and P. N. Devreotes. 1995. The G protein beta subunit is essential for multiple responses to chemoattractants in Dictyostelium. J. Cell Biol. 129:1667–1675.
   PubMedGoogle Scholar
• Xu, J., D. Wu, V. Z. Slepak, and M. I. Simon. 1995. The N terminus of phosducin is involved in binding of beta gamma subunits of G protein. Proc. Natl. Acad. Sci. USA 92:2086–2090.
   PubMedGoogle Scholar
• Zhang, F. L., and P. J. Casey. 1996. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65:241–269.
   PubMed Web of Science ®Google Scholar