The bilayer enhances rhodopsin kinetic stability in bovine rod outer segment disk membranes

Biophysical Journal

Volumn 100, Issue 12, 2011, Pages 2946-2954

  Corley, Scott C ^a   Sprangers, Peter ^b   Albert, Arlene D ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINAE;

EID: 79960331052     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.05.015     Document Type: Article

References (51)

1. Sanchez-Ruiz, J. M. 2010. Protein kinetic stability. Biophys. Chem. 148:1-15.
2. Sanchez-Ruiz, J. M. 1992. Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys. J. 61:921-935.
3. Plaza del Pino, I. M., B. Ibarra-Molero, and J. M. Sanchez-Ruiz. 2000. Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases. Proteins. 40:58-70. (Pubitemid 30368582)
4. Freire, E., W. W. van Osdol, ..., J. M. Sanchez-Ruiz. 1990. Calorimetrically determined dynamics of complex unfolding transitions in proteins. Annu. Rev. Biophys. Biophys. Chem. 19:159-188. (Pubitemid 20205622)
5. Jaswal, S. S., J. L. Sohl, ..., D. A. Agard. 2002. Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability. Nature. 415:343-346. (Pubitemid 34087558)
6. Lee, C., S. H. Park, ..., M. H. Yu. 2000. Regulation of protein function by native metastability. Proc. Natl. Acad. Sci. USA. 97:7727-7731. (Pubitemid 30460715)
7. Huber, R., and R. W. Carrell. 1989. Implications of the three-dimensional structure of alpha 1-antitrypsin for structure and function of serpins. Biochemistry. 28:8951-8966. (Pubitemid 19283457)
8. Carr, C. M., and P. S. Kim. 1993. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell. 73:823-832. (Pubitemid 23159019)
9. Bullough, P. A., F. M. Hughson, ..., D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371:37-43. (Pubitemid 24277462)
10. Chan, D. C., F. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell. 89:263-273. (Pubitemid 27199898)
11. Orosz, A., J. Wisniewski, and C. Wu. 1996. Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization. Mol. Cell. Biol. 16:7018-7030. (Pubitemid 26389761)
12. 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. (Pubitemid 32847986)
13. Edrington, 5th, T. C., M. Bennett, and A. D. Albert. 2008. Calorimetric studies of bovine rod outer segment disk membranes support a monomeric unit for both rhodopsin and opsin. Biophys. J. 95:2859-2866.
14. Morin, P. E., D. Diggs, and E. Freire. 1990. Thermal stability of membrane-reconstituted yeast cytochrome c oxidase. Biochemistry. 29:781-788. (Pubitemid 20041964)
15. Galisteo, M. L., and J. M. Sanchez-Ruiz. 1993. Kinetic study into the irreversible thermal denaturation of bacteriorhodopsin. Eur. Biophys. J. 22:25-30. (Pubitemid 23233151)
16. Epand, R. F., R. M. Epand, and C. Y. Jung. 1999. Glucose-induced thermal stabilization of the native conformation of GLUT 1. Biochemistry. 38:454-458. (Pubitemid 29035716)
17. Lepock, J. R., A. M. Rodahl, ..., K. H. Cheng. 1990. Thermal denaturation of the Ca2(+)-ATPase of sarcoplasmic reticulum reveals two thermodynamically independent domains. Biochemistry. 29:681-689. (Pubitemid 20041949)
18. 2+ -ATPase from sarcoplasmic reticulum membranes. Biochim. Biophys. Acta. 1420:203-213.
19. Zhadan, G. G., C. Cobaleda, ..., V. L. Shnyrov. 1997. Protein involvement in thermally induced structural transitions of pig erythrocyte ghosts. Biochem. Mol. Biol. Int. 42:11-20. (Pubitemid 28173820)
20. Helenius, A., and K. Simons. 1975. Solubilization of membranes by detergents. Biochim. Biophys. Acta. 415:29-79.
21. 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. (Pubitemid 8270203)
22. 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.
23. Hubbard, R. 1958. The thermal stability of rhodopsin and opsin. J. Gen. Physiol. 42:259-280.
24. Shnyrov, V. L., and A. L. Berman. 1988. Calorimetric study of thermal denaturation of vertebrate visual pigments. Biomed. Biochim. Acta. 47:355-362.
25. Khan, S. M., W. Bolen, ..., J. H. McDowell. 1991. Differential scanning calorimetry of bovine rhodopsin in rod-outer-segment disk membranes. Eur. J. Biochem. 200:53-59.
26. Albert, A. D., J. E. Young, and P. L. Yeagle. 1996. Rhodopsin-cholesterol interactions in bovine rod outer segment disk membranes. Biochim. Biophys. Acta. 1285:47-55. (Pubitemid 26388752)
27. Miljanich, G. P., M. F. Brown, ..., J. M. Sturtevant. 1985. Thermotropic behavior of retinal rod membranes and dispersions of extracted phospholipids. J. Membr. Biol. 85:79-86. (Pubitemid 15033400)
28. Stubbs, G. W., H. G. Smith, Jr., and B. J. Litman. 1976. Alkyl glucosides as effective solubilizing agents for bovine rhodopsin. A comparison with several commonly used detergents. Biochim. Biophys. Acta. 426:46-56.
29. Jackson, M. L., and B. J. Litman. 1982. Rhodopsin-phospholipid reconstitution by dialysis removal of octyl glucoside. Biochemistry. 21:5601-5608.
30. Smith, Jr., H. G., 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.
31. Sánchez-Ruiz, J. M., J. L. López-Lacomba, ..., P. L. Mateo. 1988. Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry. 27:1648-1652.
32. Rodriguez-Larrea, D., S. Minning, ..., J. M. Sanchez-Ruiz. 2006. Role of solvation barriers in protein kinetic stability. J. Mol. Biol. 360:715-724. (Pubitemid 43975108)
33. Stubbs, G. W., and B. J. Litman. 1978. Effect of alterations in the amphipathic microenvironment on the conformational stability of bovine opsin. 2. Rate of loss of opsin regenerability. Biochemistry. 17:220-225. (Pubitemid 8270204)
34. Shinoda, H., T. Yamaguchi, and R. Hori. 1961. The surface tension and the critical micelle concentration in aqueous solution of β-D-alkyl glucosides and their mixtures. Bull. Chem. Soc. Jpn. 34:237-241.
35. Lumry, R., and H. Eyring. 1954. Conformation changes of proteins. J. Phys. Chem. 58:110-120.
36. Albert, A. D., K. Boesze-Battaglia, ..., R. M. Epand. 1996. Effect of cholesterol on rhodopsin stability in disk membranes. Biochim. Biophys. Acta. 1297:77-82. (Pubitemid 26298175)
37. Lee, A. G. 2003. Lipid-protein interactions in biological membranes: a structural perspective. Biochem. Biophys. Acta. 1612:1-40. (Pubitemid 36555684)
38. Watts, A., I. D. Volotovski, ..., D. Marsh. 1982. Spin-label studies of rhodopsin-lipid interactions. Biophys. J. 37:94-95.
39. Albert, A. D., P. Yeagle, and B. J. Litman. 1982. P NMR investigation of rhodopsin-phospholipid interactions in bovine rod outer segment disk membranes. Biophys. J. 37:34-36. (Pubitemid 12150007)
40. Wenk, M. R., T. Alt, ..., J. Seelig. 1997. Octyl-beta-D-glucopyranoside partitioning into lipid bilayers: thermodynamics of binding and structural changes of the bilayer. Biophys. J. 72:1719-1731. (Pubitemid 27133111)
41. Almog, S., B. J. Litman, ..., D. Lichtenberg. 1990. States of aggregation and phase transformations in mixtures of phosphatidylcholine and octyl glucoside. Biochemistry. 29:4582-4592. (Pubitemid 20172674)
42. Andersen, O. S., and R. E. Koeppe 2nd. 2007. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36:107-130. (Pubitemid 46998112)
43. Mitchell, D. C., M. Straume, ..., B. J. Litman. 1990. Modulation of metarhodopsin formation by cholesterol-induced ordering of bilayer lipids. Biochemistry. 29:9143-9149. (Pubitemid 20320878)
44. Straume, M., and B. J. Litman. 1987. Equilibrium and dynamic structure of large, unilamellar, unsaturated acyl chain phosphatidylcholine vesicles. Higher order analysis of 1, 6-diphenyl-1, 3, 5-hexatriene and 1-[4-(trimethylammonio) phenyl]- 6-phenyl-1, 3, 5-hexatriene anisotropy decay. Biochemistry. 26:5113-5120.
45. Straume, M., and B. J. Litman. 1987. Influence of cholesterol on equilibrium and dynamic bilayer structure of unsaturated acyl chain phosphatidylcholine vesicles as determined from higher order analysis of fluorescence anisotropy decay. Biochemistry. 26:5121-5126.
46. Straume, M., and B. J. Litman. 1988. Equilibrium and dynamic bilayer structural properties of unsaturated acyl chain phosphatidylcholinecholesterol- rhodopsin recombinant vesicles and rod outer segment disk membranes as determined from higher order analysis of fluorescence anisotropy decay. Biochemistry. 27:7723-7733.
47. Straume, M., D. C. Mitchell, ..., B. J. Litman. 1990. Interconversion of metarhodopsins I and II: a branched photointermediate decay model. Biochemistry. 29:9135-9142. (Pubitemid 20320877)
48. Sakmar, T. P. 2002. Structure of rhodopsin and the superfamily of seven-helical receptors: the same and not the same. Curr. Opin. Cell Biol. 14:189-195. (Pubitemid 34219508)
49. McKibbin, C., N. A. Farmer, ..., P. J. Booth. 2007. Opsin stability and folding: modulation by phospholipid bicelles. J. Mol. Biol. 374:1319- 1332. (Pubitemid 350122546)
50. Bennett, M. P., and D. C. Mitchell. 2008. Regulation of membrane proteins by dietary lipids: effects of cholesterol and docosahexaenoic acid acyl chain-containing phospholipids on rhodopsin stability and function. Biophys. J. 95:1206-1216.
51. Albert, A. D., P. L. Yeagle, ..., R. Epand. 1994. Effect of cholesterol on retinal rod outer segment disk membranes. Invest. Ophthalmol. Vis. Sci. 35:1461.