Monitoring the Diffusion of Single Heterotrimeric G Proteins in Supported Cell-membrane Sheets Reveals their Partitioning into Microdomains

Journal of Molecular Biology

Volumn 363, Issue 5, 2006, Pages 918-930

  Perez, Jean Baptiste ^a   Segura, Jean Manuel ^a   Abankwa, Daniel ^a   Piguet, Joachim ^a   Martinez, Karen L ^a   Vogel, Horst ^a  

^a EPFL   (Switzerland)

Author keywords

G protein; membrane anchors; microdomains; single molecule microscopy

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DIFFUSION; EMBRYO; HUMAN; HUMAN CELL; LIPID BILAYER; MONITORING; PRIORITY JOURNAL; PROTEIN DOMAIN;

EID: 33750009848     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.08.036     Document Type: Article

References (61)

1. Azpiazu I., and Gautam N. A fluorescence resonance energy transfer-based sensor indicates that receptor access to a G protein is unrestricted in a living mammalian cell. J. Biol. Chem. 279 (2004) 27709-27718
2. Bunemann M., Frank M., and Lohse M.J. Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. U S A 100 (2003) 16077-16082
3. Gibson S.K., and Gilman A.G. Gialpha and Gbeta subunits both define selectivity of G protein activation by alpha2-adrenergic receptors. Proc. Natl. Acad. Sci. U S A 103 (2006) 212-217
4. Levitzki A. From epinephrine to cyclic AMP. Science 241 (1988) 800-806
5. Ostrom R.S., and Insel P.A. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br. J. Pharmacol. 143 (2004) 235-245
6. Holst B., Hastrup H., Raffetseder U., Martini L., and Schwartz T.W. Two active molecular phenotypes of the tachykinin NK1 receptor revealed by G-protein fusions and mutagenesis. J. Biol. Chem. 276 (2001) 19793-19799
7. Neubig R.R. Membrane organization in G-protein mechanisms. FASEB J. 8 (1994) 939-946
8. Rebois R.V., and Hebert T.E. Protein complexes involved in heptahelical receptor-mediated signal transduction. Recept. Chann. 9 (2003) 169-194
9. Pike L.J. Lipid rafts: bringing order to chaos. J. Lipid Res. 44 (2003) 655-667
10. Simons K., and Toomre D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell. Biol. 1 (2000) 31-39
11. Simons K., and Vaz W.L. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 269-295
12. Oh P., and Schnitzer J.E. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol. Biol. Cell 12 (2001) 685-698
13. Nair K.S., Balasubramanian N., and Slepak V.Z. Signal-dependent translocation of transducin, RGS9-1-Gb5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr. Biol. 12 (2002) 421-425
14. Seno K., Kishimoto M., Abe M., Higuchi Y., Mieda M., Owada Y., et al. Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J. Biol. Chem. 276 (2001) 20813-20816
15. Moffett S., Brown D.A., and Linder M.E. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275 (2000) 2191-2198
16. Rotblat B., Prior I., Muncke C., Parton R., Kloog Y., Henis Y., and Hancock J. Three separable domains regulate GTP-dependent association of H-ras with the plasma membrane. Mol. Cell. Biol. 24 (2004) 6799-6810
17. Prior I.A., Harding A., Yan J., Sluimer J., Parton R.G., and Hancock J.F. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nature Cell. Biol. 3 (2001) 368-375
18. Lommerse P.H., Snaar-Jagalska B.E., Spaink H.P., and Schmidt T. Single-molecule diffusion measurements of H-Ras at the plasma membrane of live cells reveal microdomain localization upon activation. J. Cell Sci. 118 (2005) 1799-1809
19. Murakoshi H., Iino R., Kobayashi T., Fujiwara T., Ohshima C., Yoshimura A., and Kusumi A. Single-molecule imaging analysis of Ras activation in living cells. Proc. Natl Acad. Sci. U S A 101 (2004) 7317-7322
20. Lommerse P.H., Spaink H.P., and Schmidt T. In vivo plasma membrane organization: results of biophysical approaches. Biochim. Biophys. Acta 1664 (2004) 119-1131
21. Meyer B.H., Segura J.-M., Martinez K.L., Hovius R., George N., Johnsson K., and Vogel H. FRET imaging reveals that functional neurokinin-1 receptors are monomeric and reside in membrane microdomains of live cells. Proc. Natl Acad. Sci. U S A 103 (2006) 2138-2143
22. Ianoul A., Grant D.D., Rouleau Y., Bani-Yaghoub M., Johnston L.J., and Pezacki J.P. Imaging nanometer domains of beta-adrenergic receptor complexes on the surface of cardiac myocytes. Nature Chem. Biol. 1 (2005) 196-202
23. Cezanne L., Lecat S., Lagane B., Millot C., Vollmer J.Y., Matthes H., et al. Dynamic confinement of NK2 receptors in the plasma membrane. Improved FRAP analysis and biological relevance. J. Biol. Chem. 279 (2004) 45057-45067
24. Daumas F., Destainville N., Millot C., Lopez A., Dean D., and Salome L. Confined diffusion without fences of a G-protein-coupled receptor as revealed by single particle tracking. Biophys. J. 84 (2003) 356-366
25. Lill Y., Martinez K.L., Lill M.A., Meyer B.H., Vogel H., and Hecht B. Kinetics of the initial steps of G protein-coupled receptor-mediated cellular signaling revealed by single-molecule imaging. Chemphyschem. 6 (2005) 1633-1640
26. Serge A., Fourgeaud L., Hemar A., and Choquet D. Receptor activation and homer differentially control the lateral mobility of metabotropic glutamate receptor 5 in the neuronal membrane. J. Neurosci. 22 (2002) 3910-3920
27. Prummer M., Meyer B.H., Franzini R., Segura J.M., George N., Johnsson K., and Vogel H. Post-translational covalent labeling reveals heterogeneous mobility of individual G protein-coupled receptors in living cells. Chembiochem. 7 (2006) 908-911
28. Kwon G., Axelrod D., and Neubig R.R. Lateral mobility of tetramethylrhodamine (TMR) labelled G protein alpha and beta gamma subunits in NG 108-15 cells. Cell Signal. 6 (1994) 663-679
29. Wang T.Y., Leventis R., and Silvius J.R. Fluorescence-based evaluation of the partitioning of lipids and lipidated peptides into liquid-ordered lipid microdomains: a model for molecular partitioning into "lipid rafts". Biophys. J. 79 (2000) 919-933
30. Bieri C., Ernst O.P., Heyse S., Hofmann K.P., and Vogel H. Micropatterned immobilization of a G protein-coupled receptor and direct detection of G protein activation. Nature Biotechnol. 17 (1999) 1105-1108
31. Hong Y., Webb B.L., Su H., Mozdy E.J., Fang Y., Wu Q., et al. Functional GPCR microarrays. J. Am. Chem. Soc. 127 (2005) 15350-15351
32. Yamazaki V., Sirenko O., Schafer R.J., and Groves J.T. Lipid mobility and molecular binding in fluid lipid membranes. J. Am. Chem. Soc. 127 (2005) 2826-2827
33. Heyse S., Ernst O.P., Dienes Z., Hofmann K.P., and Vogel H. Incorporation of rhodopsin in laterally structured supported membranes: observation of transducin activation with spatially and time-resolved surface plasmon resonance. Biochemistry 37 (1998) 507-522
34. Huang C., Hepler J.R., Chen L.T., Gilman A.G., Anderson R.G., and Mumby S.M. Organization of G proteins and adenylyl cyclase at the plasma membrane. Mol. Biol. Cell. 8 (1997) 2365-2378
35. Prior I., Muncke C., Parton R., and Hancock J. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell. Biol. 160 (2003) 165-170
36. Danelon C., Perez J.B., Santschi C., Brugger J., and Vogel H. Cell membranes suspended across nanoaperture arrays. Langmuir 22 (2006) 22-25
37. Martinez K.L., Meyer B.H., Hovius R., Lundstrom K., and Vogel H. Ligand binding to G protein-coupled receptors in tethered cell membranes. Langmuir 19 (2003) 10925-10929
38. Scheuring S., Rigaud J.L., and Sturgis J.N. Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum. EMBO J. 23 (2004) 4127-4133
39. Fotiadis D., Liang Y., Filipek S., Saperstein D.A., Engel A., and Palczewski K. Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421 (2003) 127-128
40. Perez J.-B., Martinez K.L., Segura J.-M., and Vogel H. Supported cell-membrane sheets for functional fluorescence imaging of membrane proteins. Adv. Funct. Mater. 16 (2006) 306-312
41. Hughes T.E., Zhang H., Logothetis D.E., and Berlot C.H. Visualization of a functional Gαq-green fluorescent protein fusion in living cells. Association with the plasma membrane is disrupted by mutational activation and by elimination of palmitoylation sites, but not be activation mediated by receptors or AlF4. J. Biol. Chem. 276 (2001) 4227-4235
42. Michaelson D., Ahearn I., Bergo M., Young S., and Philips M. Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol. Biol. Cell 13 (2002) 3294-3302
43. Evanko D.S., Thiyagarajan M.M., and Wedegaertner P.B. Interaction with Gβγ is required for membrane targeting and palmitoylation of Gα(s) and Gα(q). J. Biol. Chem. 275 (2000) 1327-1336
44. Leaney J.L., Benians A., Graves F.M., and Tinker A. A novel strategy to engineer functional fluorescent inhibitory G-protein alpha subunits. J. Biol. Chem. 277 (2002) 28803-28809
45. Meyer, B.H. (2005). Thesis 3272. Investigation of the Neurokinin-1 Receptor by Fluorescence Techniques. EPFL, Lausanne.
46. Saxton M.J. Single-particle tracking: the distribution of diffusion coefficients. Biophys. J. 72 (1997) 1744-1753
47. Vrljic M., Nishimura S.Y., Brasselet S., Moerner W.E., and McConnell H.M. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83 (2002) 2681-2692
48. van Rheenen J., Achame E.M., Janssen H., Calafat J., and Jalink K. PIP2 signaling in lipid domains: a critical re-evaluation. EMBO J. 24 (2005) 1664-1673
49. Milosevic I., Sorensen J.B., Lang T., Krauss M., Nagy G., Haucke V., et al. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25 (2005) 2557-2565
50. Anderson R.G., and Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296 (2002) 1821-1825
51. Cha S.H., Jung N.H., Kim B.R., Kim H.W., and Kwak J.O. Evidence for cyclooxygenase-1 association with caveolin-1 and -2 in cultured human embryonic kidney (HEK 293) cells. IUBMB Life 56 (2004) 221-227
52. Niv H., Gutman O., Kloog Y., and Henis Y.I. Activated K-Ras and H-Ras display different interactions with saturable non-raft sites at the surface of live cells. J. Cell. Biol. 157 (2002) 865-872
53. Stanasila L., Perez J.-B., Vogel H., and Cotecchia S. Oligomerization of the α1a- and α1b-adrenergic receptor subtypes. Potential implications in receptor internalization. J. Biol. Chem. 278 (2003) 40239-40251
54. Griesbeck O., Baird G.S., Campbell R.E., Zacharias D.A., and Tsien R.Y. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276 (2001) 29188-29194
55. Zhang J., Campbell R.E., Ting A.Y., and Tsien R.Y. Creating new fluorescent probes for cell biology. Nature Rev. Mol. Cell. Biol. 3 (2002) 906-918
56. Feder T.J., Brust-Mascher I., Slattery J.P., Baird B., and Webb W.W. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70 (1996) 2767-2773
57. Schreiter C., Gjoni M., Hovius R., Martinez K.L., Segura J.-M., and Vogel H. Reversible sequential-binding probe receptor-ligand interactions in single cells. Chembiochem. 6 (2005) 2187-2194
58. Schmidt T., Schutz G.J., Baumgartner W., Gruber H.J., and Schindler H. Characterization of photophysics and mobility of single molecules in a fluid lipid-membrane. J. Phys .Chem. 99 (1995) 17662-17668
59. Qian H., Sheetz M.P., and Elson E.L. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60 (1991) 910-921
60. Simson R., Sheets E.D., and Jacobson K. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys. J. 69 (1995) 989-993
61. Saxton M.J. Lateral diffusion in an archipelago. Single-particle diffusion. Biophys. J. 64 (1993) 1766-1780