A G protein-coupled receptor dimerization interface in human cone opsins

Biochemistry

Volumn 56, Issue 1, 2017, Pages 61-72

  Jastrzebska, Beata ^a   Comar, William D ^b   Kaliszewski, Megan J ^b   Skinner, Kevin C ^b   Torcasio, Morgan H ^b   Esway, Anthony S ^b   Jin, Hui ^a   Palczewski, Krzysztof ^a   Smith, Adam W ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF AKRON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CELL SIGNALING; COLOR VISION; PROTEINS;

BINDING INTERFACE; CELLULAR PLASMA MEMBRANES; CHEMICAL SIGNALS; G PROTEIN COUPLED RECEPTORS; MUTAGENESIS EXPERIMENT; QUATERNARY INTERACTIONS; TIME-RESOLVED FLUORESCENCE; TRANSMEMBRANE HELICES;

DIMERIZATION;

AMINO ACID DERIVATIVE; CONE OPSIN; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ARTICLE; BINDING AFFINITY; COLOR VISION; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE; HUMAN; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; RETINA CONE; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; CONFOCAL MICROSCOPY; COS CELL LINE; FLUORESCENCE MICROSCOPY; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECTROFLUOROMETRY;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CONE OPSINS; COS CELLS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MUTATION; PROTEIN MULTIMERIZATION; RECEPTORS, G-PROTEIN-COUPLED; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE;

EID: 85009346224     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.6b00877     Document Type: Article

References (75)

1. Endres, N. F., Barros, T., Cantor, A. J., and Kuriyan, J. (2014) Emerging concepts in the regulation of the EGF receptor and other receptor tyrosine kinases. Trends Biochem. Sci. 39, 437-446.
2. Groves, J. T., and Kuriyan, J. (2010) Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17, 659-665.
3. Khelashvili, G., Dorff, K., Shan, J., Camacho-Artacho, M., Skrabanek, L., Vroling, B., Bouvier, M., Devi, L. A., George, S. R., Javitch, J. A., Lohse, M. J., Milligan, G., Neubig, R. R., Palczewski, K., Parmentier, M., Pin, J.-P., Vriend, G., Campagne, F., and Filizola, M. (2010) GPCR-OKB: the G Protein Coupled Receptor Oligomer Knowledge Base. Bioinformatics 26, 1804-1805.
4. Lambert, N. A. (2010) GPCR Dimers Fall Apart. Sci. Signaling 3, pe12.
5. Milligan, G. (2013) The Prevalence, Maintenance, and Relevance of G Protein-Coupled Receptor Oligomerization. Mol. Pharmacol. 84, 158-169.
6. Lodowski, D. T., Salom, D., Le Trong, I., Teller, D. C., Ballesteros, J. A., Palczewski, K., and Stenkamp, R. E. (2007) Crystal packing analysis of Rhodopsin crystals. J. Struct. Biol. 158, 455-462.
7. Wu, H., Wacker, D., Mileni, M., Katritch, V., Han, G. W., Vardy, E., Liu, W., Thompson, A. A., Huang, X.-P., Carroll, F. I., Mascarella, S. W., Westkaemper, R. B., Mosier, P. D., Roth, B. L., Cherezov, V., and Stevens, R. C. (2012) Structure of the human β-opioid receptor in complex with JDTic. Nature 485, 327-332.
8. Huang, J., Chen, S., Zhang, J. J., and Huang, X. Y. (2013) Crystal structure of oligomeric beta1-adrenergic G protein-coupled receptors in ligand-free basal state. Nat. Struct. Mol. Biol. 20, 419-425.
9. Wu, B., Chien, E. Y. T., Mol, C. D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F. C., Hamel, D. J., Kuhn, P., Handel, T. M., Cherezov, V., and Stevens, R. C. (2010) Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists. Science 330, 1066-1071.
10. Manglik, A., Kruse, A. C., Kobilka, T. S., Thian, F. S., Mathiesen, J. M., Sunahara, R. K., Pardo, L., Weis, W. I., Kobilka, B. K., and Granier, S. (2012) Crystal structure of the μ-opioid receptor bound to a morphinan antagonist. Nature 485, 321-326.
11. Periole, X., Knepp, A. M., Sakmar, T. P., Marrink, S. J., and Huber, T. (2012) Structural Determinants of the Supramolecular Organization of G Protein-Coupled Receptors in Bilayers. J. Am. Chem. Soc. 134, 10959-10965.
12. Simpson, L. M., Taddese, B., Wall, I. D., and Reynolds, C. A. (2010) Bioinformatics and molecular modelling approaches to GPCR oligomerization. Curr. Opin. Pharmacol. 10, 30-37.
13. Nemoto, W., and Toh, H. (2005) Prediction of interfaces for oligomerizations of G-protein coupled receptors. Proteins: Struct., Funct., Genet. 58, 644-660.
14. Filizola, M., and Weinstein, H. (2002) Structural models for dimerization of G-protein coupled receptors: The opioid receptor homodimers. Biopolymers 66, 317-325.
15. Jastrzebska, B., Chen, Y., Orban, T., Jin, H., Hofmann, L., and Palczewski, K. (2015) Disruption of Rhodopsin Dimerization with Synthetic Peptides Targeting an Interaction Interface. J. Biol. Chem. 290, 25728.
16. Harikumar, K. G., Dong, M., Cheng, Z., Pinon, D. I., Lybrand, T. P., and Miller, L. J. (2006) Transmembrane Segment Peptides Can Disrupt Cholecystokinin Receptor Oligomerization without affecting Receptor Function. Biochemistry 45, 14706-14716.
17. Hayashi, R., Osada, S., Yoshiki, M., Sugiyama, D., Fujita, I., Hamasaki, Y., and Kodama, H. (2006) Superoxide production in human neutrophils is enhanced by treatment with transmembrane peptides derived from human formyl peptide receptor. J. Biochem. 139, 981-988.
18. Wang, J., He, L., Combs, C. A., Roderiquez, G., and Norcross, M. A. (2006) Dimerization of CXCR4 in living malignant cells: control of cell migration by a synthetic peptide that reduces homologous CXCR4 interactions. Mol. Cancer Ther. 5, 2474-2483.
19. Baneres, J.-L., and Parello, J. (2003) Structure-based Analysis of GPCR Function: Evidence for a Novel Pentameric Assembly between the Dimeric Leukotriene B4 Receptor BLT1 and the G-protein. J. Mol. Biol. 329, 815-829.
20. Hebert, T. E., Moffett, S., Morello, J.-P., Loisel, T. P., Bichet, D. G., Barret, C., and Bouvier, M. (1996) A Peptide Derived from a β2-Adrenergic Receptor Transmembrane Domain Inhibits Both Receptor Dimerization and Activation. J. Biol. Chem. 271, 16384-16392.
21. Xue, L., Rovira, X., Scholler, P., Zhao, H., Liu, J., Pin, J.-P., and Rondard, P. (2014) Major ligand-induced rearrangement of the heptahelical domain interface in a GPCR dimer. Nat. Chem. Biol. 11, 134-140.
22. Dong, M., Pinon, D. I., Bordner, A. J., and Miller, L. J. (2010) Elucidation of the active conformation of the amino terminus of receptor-bound secretin using intramolecular disulfide bond constraints. Bioorg. Med. Chem. Lett. 20, 6040-6044.
23. Mancia, F., Assur, Z., Herman, A. G., Siegel, R., and Hendrickson, W. A. (2008) Ligand sensitivity in dimeric associations of the serotonin 5HT2c receptor. EMBO Rep. 9, 363-369.
24. Kota, P., Reeves, P. J., RajBhandary, U. L., and Khorana, H. G. (2006) Opsin is present as dimers in COS1 cells: Identification of amino acids at the dimeric interface. Proc. Natl. Acad. Sci. U. S. A. 103, 3054-3059.
25. Guo, W., Shi, L., and Javitch, J. A. (2003) The Fourth Transmembrane Segment Forms the Interface of the Dopamine D2 Receptor Homodimer. J. Biol. Chem. 278, 4385-4388.
26. Marsango, S., Caltabiano, G., Pou, C., Varela Liste, M. J., and Milligan, G. (2015) Analysis of Human Dopamine D3 Receptor Quaternary Structure. J. Biol. Chem. 290, 15146-15162.
27. Gorinski, N., Kowalsman, N., Renner, U., Wirth, A., Reinartz, M. T., Seifert, R., Zeug, A., Ponimaskin, E., and Niv, M. Y. (2012) Computational and Experimental Analysis of the Transmembrane Domain 4/5 Dimerization Interface of the Serotonin 5-HT1A Receptor. Mol. Pharmacol. 82, 448-463.
28. McMillin, S. M., Heusel, M., Liu, T., Costanzi, S., and Wess, J. (2011) Structural Basis of M3Muscarinic Receptor Dimer/Oligomer Formation. J. Biol. Chem. 286, 28584-28598.
29. Harikumar, K. G., Pinon, D. I., and Miller, L. J. (2007) Transmembrane Segment IV Contributes a Functionally Important Interface for Oligomerization of the Class II G Protein-coupled Secretin Receptor. J. Biol. Chem. 282, 30363-30372.
30. Salahpour, A., Angers, S., Mercier, J.-F., Lagace, M., Marullo, S., and Bouvier, M. (2004) Homodimerization of the β2-Adrenergic Receptor as a Prerequisite for Cell Surface Targeting. J. Biol. Chem. 279, 33390-33397.
31. Hernanz-Falcon, P., Rodriguez-Frade, J. M., Serrano, A., Juan, D., del Sol, A., Soriano, S. F., Roncal, F., Gomez, L., Valencia, A., Martinez-A, C., and Mellado, M. (2004) Identification of amino acid residues crucial for chemokine receptor dimerization. Nat. Immunol. 5, 216-223.
32. Dorsch, S., Klotz, K.-N., Engelhardt, S., Lohse, M. J., and Bunemann, M. (2009) Analysis of receptor oligomerization by FRAP microscopy. Nat. Methods 6, 225-230.
33. Hern, J. A., Baig, A. H., Mashanov, G. I., Birdsall, B., Corrie, J. E. T., Lazareno, S., Molloy, J. E., and Birdsall, N. J. M. (2010) Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc. Natl. Acad. Sci. U. S. A. 107, 2693-2698.
34. Fonseca, J. M., and Lambert, N. A. (2009) Instability of a Class A G Protein-Coupled Receptor Oligomer Interface. Mol. Pharmacol. 75, 1296-1299.
35. Rashid, A. J., So, C. H., Kong, M. M. C., Furtak, T., El-Ghundi, M., Cheng, R., O'Dowd, B. F., and George, S. R. (2007) D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc. Natl. Acad. Sci. U. S. A. 104, 654-659.
36. Frederick, A. L., Yano, H., Trifilieff, P., Vishwasrao, H. D., Biezonski, D., Meszaros, J., Urizar, E., Sibley, D. R., Kellendonk, C., Sonntag, K. C., Graham, D. L., Colbran, R. J., Stanwood, G. D., and Javitch, J. A. (2015) Evidence against dopamine D1/D2 receptor heteromers. Mol. Psychiatry 20, 1373-1385.
37. Lan, T.-H., Liu, Q., Li, C., Wu, G., Steyaert, J., and Lambert, N. A. (2015) BRET evidence that β2 adrenergic receptors do not oligomerize in cells. Sci. Rep. 5, 10166.
38. Angers, S., Salahpour, A., Joly, E., Hilairet, S., Chelsky, D., Dennis, M., and Bouvier, M. (2000) Detection of β2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. U. S. A. 97, 3684-3689.
39. Hofmann, L., and Palczewski, K. (2015) Advances in understanding the molecular basis of the first steps in color vision. Prog. Retinal Eye Res. 49, 46-66.
40. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Trong, I. L., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal Structure of Rhodopsin: A G Protein-Coupled Receptor. Science 289, 739-745.
41. Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2003) Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421, 127-128.
42. Mansoor, S. E., Palczewski, K., and Farrens, D. L. (2006) Rhodopsin self-associates in asolectin liposomes. Proc. Natl. Acad. Sci. U. S. A. 103, 3060-3065.
43. Jastrzebska, B., Ringler, P., Palczewski, K., and Engel, A. (2013) The rhodopsin-transducin complex houses two distinct rhodopsin molecules. J. Struct. Biol. 182, 164-172.
44. Gunkel, M., Schoneberg, J., Alkhaldi, W., Irsen, S., Noe, F., Kaupp, U. B., and Al-Amoudi, A. (2015) Higher-Order Architecture of Rhodopsin in Intact Photoreceptors and Its Implication for Phototransduction Kinetics. Structure 23, 628-638.
45. Comar, W. D., Schubert, S. M., Jastrzebska, B., Palczewski, K., and Smith, A. W. (2014) Time-Resolved Fluorescence Spectroscopy Measures Clustering and Mobility of a G Protein-Coupled Receptor Opsin in Live Cell Membranes. J. Am. Chem. Soc. 136, 8342-8349.
46. Fotiadis, D., Jastrzebska, B., Philippsen, A., Muller, D. J., Palczewski, K., and Engel, A. (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr. Opin. Struct. Biol. 16, 252-259.
47. Stenkamp, R. E., Filipek, S., Driessen, C. A. G. G., Teller, D. C., and Palczewski, K. (2002) Crystal structure of rhodopsin: a template for cone visual pigments and other G protein-coupled receptors. Biochim. Biophys. Acta, Biomembr. 1565, 168-182.
48. Zhang, T., Cao, L.-H., Kumar, S., Enemchukwu, N. O., Zhang, N., Lambert, A., Zhao, X., Jones, A., Wang, S., Dennis, E. M., Fnu, A., Ham, S., Rainier, J., Yau, K.-W., and Fu, Y. (2016) Dimerization of visual pigments in vivo. Proc. Natl. Acad. Sci. U. S. A. 113, 9093-9098.
49. Zhang, T., and Fu, Y. (2013) A Phe-rich region in shortwavelength sensitive opsins is responsible for their aggregation in the absence of 11-cis-retinal. FEBS Lett. 587, 2430-2434.
50. Sambrook, J., and Russell, D. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
51. Marita, M., Wang, Y., Kaliszewski, M. J., Skinner, K. C., Comar, W. D., Shi, X., Dasari, P., Zhang, X., and Smith, A. W. (2015) Class A Plexins Are Organized as Preformed Inactive Dimers on the Cell Surface. Biophys. J. 109, 1937-1945.
52. Smith, A. W. (2015) Detection of rhodopsin dimerization in situ by PIE-FCCS, a time-resolved fluorescence spectroscopy. Methods Mol. Biol. 1271, 205-219.
53. Boussif, O., Lezoualc'h, F., Zanta, M. A., Mergny, M. D., Scherman, D., Demeneix, B., and Behr, J. P. (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. U. S. A. 92, 7297-7301.
54. Chen, Y., and Tang, H. (2015) High-throughput screening assays to identify small molecules preventing photoreceptor degeneration caused by the rhodopsin P23H mutation. Methods Mol. Biol. 1271, 369-390.
55. Ulbrich, M. H., and Isacoff, E. Y. (2007) Subunit counting in membrane-bound proteins. Nat. Methods 4, 319-321.
56. Di Rienzo, C., Gratton, E., Beltram, F., and Cardarelli, F. (2013) Fast spatiotemporal correlation spectroscopy to determine protein lateral diffusion laws in live cell membranes. Proc. Natl. Acad. Sci. U. S. A. 110, 12307-12312.
57. Wawrezinieck, L., Rigneault, H., Marguet, D., and Lenne, P.-F. (2005) Fluorescence Correlation Spectroscopy Diffusion Laws to Probe the Submicron Cell Membrane Organization. Biophys. J. 89, 4029-4042.
58. Naji, A., Levine, A. J., and Pincus, P. A. (2007) Corrections to the Saffman-Delbruck Mobility for Membrane Bound Proteins. Biophys. J. 93, L49-L51.
59. Chung, I., Akita, R., Vandlen, R., Toomre, D., Schlessinger, J., and Mellman, I. (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464, 783-787.
60. Bacia, K., Kim, S. A., and Schwille, P. (2006) Fluorescence crosscorrelation spectroscopy in living cells. Nat. Methods 3, 83-89.
61. Muller, B. K., Zaychikov, E., Brauchle, C., and Lamb, D. C. (2005) Pulsed Interleaved Excitation. Biophys. J. 89, 3508-3522.
62. Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y., Pelton, J. G., Shan, Y., Shaw, D. E., Wemmer, D. E., Groves, J. T., and Kuriyan, J. (2013) Conformational Coupling across the Plasma Membrane in Activation of the EGF Receptor. Cell 152, 543-556.
63. Nathans, J., Thomas, D., and Hogness, D. S. (1986) Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232, 193-202.
64. Weisz, O., Swift, A., and Machamer, C. (1993) Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J. Cell Biol. 122, 1185-1196.
65. Soulie, S., Denoroy, L., Caer, J.-P. L., Hamasaki, N., Groves, J. D., and Maire, M. L. (1998) Treatment with Crystalline Ultra-Pure Urea Reduces the Aggregation of Integral Membrane Proteins without Inhibiting N-Terminal Sequencing. J. Biochem. 124, 417-420.
66. Javitch, J. A. (2004) The Ants Go Marching Two by Two: Oligomeric Structure of G-Protein-Coupled Receptors. Mol. Pharmacol. 66, 1077-1082.
67. Asenjo, A. B., Rim, J., and Oprian, D. D. (1994) Molecular determinants of human red/green color discrimination. Neuron 12, 1131-1138.
68. Neitz, J., and Neitz, M. (2011) The genetics of normal and defective color vision. Vision Res. 51, 633-651.
69. Srinivasan, S., Cordomí, A., Ramon, E., and Garriga, P. (2016) Beyond spectral tuning: human cone visual pigments adopt different transient conformations for chromophore regeneration. Cell. Mol. Life Sci. 73, 1253-1263.
70. Jastrzebska, B., Debinski, A., Filipek, S., and Palczewski, K. (2011) Role of membrane integrity on G protein-coupled receptors: Rhodopsin stability and function. Prog. Lipid Res. 50, 267-277.
71. Baylor, D. A., Lamb, T. D., and Yau, K. W. (1979) Responses of retinal rods to single photons. J. Physiol. 288, 613-634.
72. Rieke, F., and Baylor, D. A. (1998) Origin of Reproducibility in the Responses of Retinal Rods to Single Photons. Biophys. J. 75, 1836-1857.
73. Zhang, N., Kolesnikov, A. V., Jastrzebska, B., Mustafi, D., Sawada, O., Maeda, T., Genoud, C., Engel, A., Kefalov, V. J., and Palczewski, K. (2013) Autosomal recessive retinitis pigmentosa E150K opsin mice exhibit photoreceptor disorganization. J. Clin. Invest. 123, 121-137.
74. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies. Trends Biochem. Sci. 26, 318-324.
75. Kefalov, V., Fu, Y., Marsh-Armstrong, N., and Yau, K.-W. (2003) Role of visual pigment properties in rod and cone phototransduction. Nature 425, 526-531.