Quantitative morphological analysis of arrestin2 clustering upon G protein-coupled receptor stimulation by super-resolution microscopy

Journal of Structural Biology

Volumn 184, Issue 2, 2013, Pages 329-334

  Truan, Zinnia ^a   Tarancón Díez, Laura ^a   Bönsch, Claudia ^a   Malkusch, Sebastian ^b   Endesfelder, Ulrike ^b   Munteanu, Mihaela ^a   Hartley, Oliver ^a   Heilemann, Mike ^b   Fürstenberg, Alexandre ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Arrestin; Clustering; G protein coupled receptor; Single molecule fluorescence microscopy; Super resolution microscopy

Indexed keywords

ARRESTIN2 PROTEIN; CHEMOKINE RECEPTOR CCR5; CYTOCHALASIN D; G PROTEIN COUPLED RECEPTOR; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MEMBRANE PROTEIN; NANOBODY; NOCODAZOLE; RANTES; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CLUSTER ANALYSIS; CONFOCAL MICROSCOPY; ENZYME ACTIVATION; FEMALE; FLUORESCENCE MICROSCOPY; INTERNALIZATION; MICROSCOPY; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SUPER RESOLUTION MICROSCOPY; WIDE FIELD MICROSCOPY;

ARRESTIN; CLUSTERING; G-PROTEIN COUPLED RECEPTOR; SINGLE-MOLECULE FLUORESCENCE MICROSCOPY; SUPER-RESOLUTION MICROSCOPY;

ACTIN CYTOSKELETON; ANIMALS; ARRESTINS; CATTLE; CHEMOKINE CCL5; CHEMOKINES, CC; CHO CELLS; CRICETINAE; CRICETULUS; CYTOCHALASIN D; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; NOCODAZOLE; PROTEIN TRANSPORT; RECEPTORS, CCR5; RECOMBINANT FUSION PROTEINS; SINGLE-DOMAIN ANTIBODIES; TUBULIN MODULATORS;

EID: 84887240137     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.09.019     Document Type: Article

References (35)

1. Cordes T., Strackharn M., Stahl S.W., Summerer W., Steinhauer C., Forthmann C., Puchner E.M., Vogelsang J., Gaub H.E., Tinnefeld P. Resolving single-molecule assembled patterns with superresolution blink-microscopy. Nano Lett. 2010, 10:645-651.
2. Endesfelder U., Finan K., Holden S.J., Cook P.R., Kapanidis A.N., Heilemann M. Multi-scale spatial organization of RNA polymerase in Escherichia coli. Biophys. J. 2013, 105:172-181.
3. Escola J.-M., Kuenzi G., Gaertner H., Foti M., Hartley O. CC chemokine receptor 5 (CCR5) desensitization - cycling receptors accumulate in the trans-Golgi network. J. Biol. Chem. 2010, 285:41772-41780.
4. Fürstenberg A., Heilemann M. Single-molecule localization microscopy - near-molecular spatial resolution in light microscopy with photoswitchable fluorophores. Phys. Chem. Chem. Phys. 2013, 15:14919-14930.
5. Gaertner H., Lebeau O., Borlat I., Cerini F., Dufour B., Kuenzi G., Melotti A., Fish R.J., Offord R., Springael J.Y., Parmentier M., Hartley O. Highly potent HIV inhibition: engineering a key anti-HIV structure from PSC-RANTES into MIP-1 beta/CCL4. Protein Eng. Des. Sel. 2008, 21:65-72.
6. Gaertner H., Cerini F., Escola J.-M., Kuenzi G., Melotti A., Offord R., Rossitto-Borlat I., Nedellec R., Salkowitz J., Gorochov G., Mosier D., Hartley O. Highly potent, fully recombinant anti-HIV chemokines: reengineering a low-cost microbicide. Proc. Natl. Acad. Sci. USA 2008, 105:17706-17711.
7. Hartley O., Gaertner H., Wilken J., Thompson D., Fish R., Ramos A., Pastore C., Dufour B., Cerini F., Melotti A., Heveker N., Picard L., Alizon M., Mosier D., Kent S., Offord R. Medicinal chemistry applied to a synthetic protein: development of highly potent HIV entry inhibitors. Proc. Natl. Acad. Sci. USA 2004, 101:16460-16465.
8. Heilemann M., van de Linde S., Mukherjee A., Sauer M. Super-resolution imaging with small organic fluorophores. Angew. Chem. Int. Ed. 2009, 48:6903-6908.
9. Kamiyama D., Huang B. Development in the STORM. Dev. Cell 2012, 23:1103-1110.
10. Kenakin T.P. Cellular assays as portals to seven-transmembrane receptor-based drug discovery. Nat. Rev. Drug Discov. 2009, 8:617-626.
11. Kobilka B.K., Deupi X. Conformational complexity of G-protein-coupled receptors. Trends Pharmacol. Sci. 2007, 28:397-406.
12. Lando D., Endesfelder U., Berger H., Subramanian L., Dunne P.D., McColl J., Klenerman D., Carr A.M., Sauer M., Allshire R.C., Heilemann M., Laue E.D. Quantitative single-molecule microscopy reveals that CENP-A(Cnp1) deposition occurs during G2 in fission yeast. Open Biol. 2012, 2:120078.
13. Laporte S.A., Oakley R.H., Holt J.A., Barak L.S., Caron M.G. The interaction of beta-arrestin with the AP-2 adaptor is required for the clustering of beta(2)-adrenergic receptor into clathrin-coated pits. J. Biol. Chem. 2000, 275:23120-23126.
14. Lederman M.M., Veazey R.S., Offord R., Mosier D.E., Dufour J., Mefford M., Piatak M., Lifson J.D., Salkowitz J.R., Rodriguez B., Blauvelt A., Hartley O. Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 2004, 306:485-487.
15. Lee S.F., Vérolet Q., Fürstenberg A. Improved super-resolution microscopy with oxazine fluorophores in heavy water. Angew. Chem. Int. Ed. 2013, 52:8948-8951.
16. Lefkowitz R.J., Shenoy S.K. Transduction of receptor signals by beta-arrestins. Science 2005, 308:512-517.
17. Luttrell L.M., Gesty-Palmer D. Beyond desensitization: physiological relevance of arrestin-dependent signaling. Pharmacol. Rev. 2010, 62:564.
18. Malkusch S., Muranyi W., Muller B., Krausslich H.G., Heilemann M. Single-molecule coordinate-based analysis of the morphology of HIV-1 assembly sites with near-molecular spatial resolution. Histochem. Cell Biol. 2013, 139:173-179.
19. Mennella V., Keszthelyi B., McDonald K.L., Chhun B., Kan F., Rogers G.C., Huang B., Agard D.A. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 2012, 14:1159-1168.
20. Moerner W.E. Microscopy beyond the diffraction limit using actively controlled single molecules. J. Microsc. 2012, 246:213-220.
21. Moore C.A.C., Milano S.K., Benovic J.L. Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 2007, 69:451-482.
22. Muranyi W., Malkusch S., Muller B., Heilemann M., Krausslich H.G. Super-resolution microscopy reveals specific recruitment of HIV-1 envelope proteins to viral assembly sites dependent on the envelope C-terminal tail. PLoS Pathog. 2013, 9:e1003198.
23. Oakley R.H., Laporte S.K., Holt J.A., Caron M.G., Barak L.S. Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem. 2000, 275:17201-17210.
24. Peterson P. F2PY: a tool for connecting Fortran and Python programs. Int. J. Comput. Sci. Eng. 2009, 4:296-305.
25. Reiter E., Ahn S., Shukla A.K., Lefkowitz R.J. Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 2012, 52:179-197.
26. Ries J., Kaplan C., Platonova E., Eghlidi H., Ewers H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 2012, 9:582-584.
27. Ripley B.D. Modelling spatial patterns. J. R. Stat. Soc. 1977, 39:172-212.
28. Rosenbaum D.M., Rasmussen S.G.F., Kobilka B.K. The structure and function of G-protein-coupled receptors. Nature 2009, 459:356-363.
29. Santini F., Gaidarov I., Keen J.H. G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol. 2002, 156:665-676.
30. Sengupta P., Jovanovic-Talisman T., Skoko D., Renz M., Veatch S.L., Lippincott-Schwartz J. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat. Methods 2011, 8:969-975.
31. Spudich J.A., Sivaramakrishnan S. Myosin VI: an innovative motor that challenged the swinging lever arm hypothesis. Nat. Rev. Mol. Cell Biol. 2010, 11:128-137.
32. van de Linde S., Sauer M., Heilemann M. Subdiffraction-resolution fluorescence imaging of proteins in the mitochondrial inner membrane with photoswitchable fluorophores. J. Struct. Biol. 2008, 164:250-254.
33. Williamson D.J., Owen D.M., Rossy J., Magenau A., Wehrmann M., Gooding J.J., Gaus K. Pre-existing clusters of the adaptor lat do not participate in early T cell signaling events. Nat. Immunol. 2011, 12:655-662.
34. Wolter S., Schuttpelz M., Tscherepanow M., Van de Linde S., Heilemann M., Sauer M. Real-time computation of subdiffraction-resolution fluorescence images. J. Microsc. 2010, 237:12-22.
35. Zidar D.A. Endogenous ligand bias by chemokines: implications at the front lines of infection and leukocyte trafficking. Endocr. Metab. Immun. Disord. Drug Targets 2011, 11:120-131.