Calorimetric studies of bovine rod outer segment disk membranes support a monomeric unit for both rhodopsin and opsin

Biophysical Journal

Volumn 95, Issue 6, 2008, Pages 2859-2866

  Edrington V, Thomas C ^a   Bennett, Michael ^b   Albert, Arlene D ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS LINKING REAGENT; OPSIN; RHODOPSIN;

ANIMAL; ARTICLE; CATTLE; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; DIFFERENTIAL SCANNING CALORIMETRY; DIMERIZATION; KINETICS; METABOLISM; PROTEIN DENATURATION; PROTEIN TERTIARY STRUCTURE; RETINA ROD OUTER SEGMENT; TRANSITION TEMPERATURE;

ANIMALS; CALORIMETRY, DIFFERENTIAL SCANNING; CATTLE; CELL MEMBRANE; CROSS-LINKING REAGENTS; DIMERIZATION; KINETICS; OPSIN; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; RHODOPSIN; ROD OUTER SEGMENTS; TRANSITION TEMPERATURE;

EID: 55549105791     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.128868     Document Type: Article

References (41)

1. Pierce, K. L., R. T. Premont, and R. J. Lefkowitz. 2002. Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3:639-650.
2. Insel, P. A., C. M. Tang, I. Hahntow, and M. C. Michel. 2007. Impact of GPCRs in clinical medicine: monogenic diseases, genetic variants and drug targets. Biochim. Biophys. Acta. 1768:994-1005.
3. Javitch, J. A. 2004. The ants go marching two by two: oligomeric structure of G-protein-coupled receptors. Mol. Pharmacol. 66:1077-1082.
4. Terrillon, S., and M. Bouvier. 2004. Roles of G-protein-coupled receptor dimerization. EMBO Rep. 5:30-34.
5. Park, P. S., S. Filipek, J. W. Wells, and K. Palczewski. 2004. Oligomerization of G protein-coupled receptors: past, present, and future. Biochemistry. 43:15643-15656.
6. Prinster, S. C., C. Hague, and R. A. Hall. 2005. Heterodimerization of G protein-coupled receptors: specificity and functional significance. Pharmacol. Rev. 57:289-298.
7. Chabre, M., and M. le Maire. 2005. Monomeric G-protein-coupled receptor as a functional unit. Biochemistry. 44:9395-9403.
8. Davies, M. N., D. E. Gloriam, A. Secker, A. A. Freitas, M. Mendao, J. Timmis, and D. R. Flower. 2007. Proteomic applications of automated GPCR classification. Proteomics. 7:2800-2814.
9. Papermaster, D. S., and W. J. Dreyer. 1974. Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. Biochemistry. 13:2438-2444.
10. Baylor, D. 1996. How photons start vision. Proc. Natl. Acad. Sci. USA. 93:560-565.
11. Palczewski, K. 2006. G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75:743-767.
12. Fotiadis, D., B. Jastrzebska, A. Philippsen, D. J. Muller, K. Palczewski, and A. Engel. 2006. Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr. Opin. Struct. Biol. 16:252-259.
13. Ridge, K. D., and K. Palczewski. 2007. Visual rhodopsin sees the light: structure and mechanism of G protein signaling. J. Biol. Chem. 282:9297-9301.
14. Liang, Y., D. Fotiadis, S. Filipek, D. A. Saperstein, K. Palczewski, and A. Engel. 2003. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278:21655-21662.
15. Suda, K., S. Filipek, K. Palczewski, A. Engel, and D. Fotiadis. 2004. The supramolecular structure of the GPCR rhodopsin in solution and native disc membranes. Mol. Membr. Biol. 21:435-446.
16. Jastrzebska, B., T. Maeda, L. Zhu, D. Fotiadis, S. Filipek, A. Engel, R. E. Stenkamp, and K. Palczewski. 2004. Functional characterization of rhodopsin monomers and dimers in detergents. J. Biol. Chem. 279:54663-54675.
17. Filipek, S., K. A. Krzysko, D. Fotiadis, Y. Liang, D. A. Saperstein, A. Engel, and K. Palczewski. 2004. A concept for G protein activation by G protein-coupled receptor dimers: the transducin/rhodopsin interface. Photochem. Photobiol. Sci. 3:628-638.
18. Khan, S. M., W. Bolen, P. A. Hargrave, M. M. Santoro, and J. H. McDowell. 1991. Differential scanning calorimetry of bovine rhodopsin in rod-outer-segment disk membranes. Eur. J. Biochem. 200:53-59.
19. Shnyrov, V. L., and A. L. Berman. 1988. Calorimetric study of thermal denaturation of vertebrate visual pigments. Biomed. Biochim. Acta. 47:355-362.
20. Landin, J. S., M. Katragadda, and A. D. Albert. 2001. Thermal destabilization of rhodopsin and opsin by proteolytic cleavage in bovine rod outer segment disk membranes. Biochemistry. 40:11176-11183.
21. Polozova, A., and B. J. Litman. 2000. Cholesterol dependent recruitment of di22:6-PC by a G-protein-coupled receptor into lateral domains. Biophys. J. 79:2632-2643.
22. Albert, A. D., K. Boesze-Battaglia, Z. Paw, A. Watts, and R. M. Epand. 1996. Effect of cholesterol on rhodopsin stability in disk membranes. Biochim. Biophys. Acta. 1297:77-82.
23. Smith, H. G., Jr., G. W. Stubbs, and B. J. Litman. 1975. The isolation and purification of osmotically intact discs from retinal rod outer segments. Exp. Eye Res. 20:211-217.
24. Sanchez-Ruiz, J. M., J. L. Lopez-Lacomba, M. Cortijo, and P. L. Mateo. 1988. Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry. 27:1648-1652.
25. Medina, R., D. Perdomo, and J. Bubis. 2004. The hydrodynamic properties of dark- and light-activated states of n-dodecyl beta-D-maltoside- solubilized bovine rhodopsin support the dimeric structure of both conformations. J. Biol. Chem. 279:39565-39573.
26. Dzwolak, W., R. Ravindra, J. Lendermann, and R. Winter. 2003. Aggregation of bovine insulin probed by DSC/PPC calorimetry and FTIR spectroscopy. Biochemistry. 42:11347-11355.
27. van Teeffelen, A. M., M. B. Meinders, and H. H. de Jongh. 2005. Identification of pitfalls in the analysis of heat capacity changes of beta-lactoglobulin A. Int. J. Biol. Macromol. 37:28-34.
28. Rochu, D., N. Beaufet, F. Renault, N. Viguie, and P. Masson. 2002. The wild type bacterial Co(2+)/Co(2+)-phosphotriesterase shows a middle-range thermostability. Biochim. Biophys. Acta. 1594:207-218.
29. Lohner, K., and A. F. Esser. 1991. Thermal unfolding and aggregation of human complement protein C9: a differential scanning calorimetry study. Biochemistry. 30:6620-6625.
30. Fotiadis, D., Y. Liang, S. Filipek, D. A. Saperstein, A. Engel, and K. Palczewski. 2003. Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature. 421:127-128.
31. Miljanich, G. P., M. F. Brown, S. Mabrey-Gaud, E. A. Dratz, and J. M. Sturtevant. 1985. Thermotropic behavior of retinal rod membranes and dispersions of extracted phospholipids. J. Membr. Biol. 85:79-86.
32. Downer, N. W. 1985. Cross-linking of dark-adapted frog photoreceptor disk membranes. Evidence for monomeric rhodopsin. Biophys. J. 47:285-293.
33. Shnyrov, V. L., and P. L. Mateo. 1993. Thermal transitions in the purple membrane from Halobacterium halobium. FEBS Lett. 324:237-240.
34. Jackson, M. B., and J. M. Sturtevant. 1978. Phase transitions of the purple membranes of Halobacterium halobium. Biochemistry. 17:911-915.
35. Stubbs, G. W., and B. J. Litman. 1978. Effect of alterations in the amphipathic microenvironment on the conformational stability of bovine opsin. 1. Mechanism of solubilization of disk membranes by the nonionic detergent, octyl glucoside. Biochemistry. 17:215-219.
36. Botelho, A. V., T. Huber, T. P. Sakmar, and M. F. Brown. 2006. Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes. Biophys. J. 91:4464-4477.
37. Periole, X., T. Huber, S. J. Marrink, and T. P. Sakmar. 2007. G protein-coupled receptors self-assemble in dynamics simulations of model bilayers. J. Am. Chem. Soc. 129:10126-10132.
38. Bayburt, T. H., A. J. Leitz, G. Xie, D. D. Oprian, and S. G. Sligar. 2007. Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 282:14875-14881.
39. Whorton, M. R., M. P. Bokoch, S. G. Rasmussen, B. Huang, R. N. Zare, B. Kobilka, and R. K. Sunahara. 2007. A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. USA. 104:7682-7687.
40. Dell'Orco, D., M. Seeber, and F. Fanelli. 2007. Monomeric dark rhodopsin holds the molecular determinants for transducin recognition: insights from computational analysis. FEBS Lett. 581:944-948.
41. Yeagle, P. L., and A. D. Albert. 2003. A conformational trigger for activation of a G protein by a G protein-coupled receptor. Biochemistry. 42:1365-1368.