Arginine-82 regulates the pK(a) of the group responsible for the light- driven proton release in bacteriorhodopsin

Biophysical Journal

Volumn 71, Issue 2, 1996, Pages 1011-1023

  Govindjee, Rajni ^a   Misra, Saurav ^a   Balashov, Sergei P ^a   Ebrey, Thomas G ^a   Crouch, Rosalie K ^b   Menick, Donald R ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIORHODOPSIN; SCHIFF BASE;

ARTICLE; BACTERIUM MUTANT; HALOBACTERIUM; LIGHT; NONHUMAN; PH; PKA; PROTON TRANSPORT;

BACTERIA (MICROORGANISMS); HALOBACTERIUM; MUS;

EID: 0029737389     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79302-5     Document Type: Article

References (59)

1. Alexiev, U. R. Mollaaghababa, P. Scherrer, H. G. Khorana, and M. P. Heyn. 1995. Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk. Proc. Natl. Acad. Sci. USA. 92:372-376.
2. Ames, J. B., and R. A. Mathies. 1990. The role of back-reactions and proton uptake during the N → O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study. Biochemistry. 29: 7181-7190.
3. Balashov, S. P., R. Govindjee, and T. G. Ebrey. 1991. Red shift of the purple membrane absorption band and the deprotonation of tyrosine residues at high pH. Biophys. J. 60:475-490.
4. a's of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry. 34:8820-8834.
5. Balashov, S. P., R. Govindjee, M. Kono, E. Imasheva, E. Lukashev, T. G. Ebrey, R. K. Crouch, D. R. Menick, and Y. Feng. 1993. Effect of the arginine-82 to alanine mutation in bacteriorhodopsin on dark adaptation, proton release, and the photochemical cycle. Biochemistry. 32: 10331-10343.
6. Balashov, S. P., R. Govindjee, M. Kono, E. Lukashev, T. G. Ebrey, Y. Feng, R. K. Crouch, and D. R. Menick. 1992. Arg82Ala mutant of bacteriorhodopsin expressed in H. halobium: drastic decrease in the rate of proton release and effect on dark adaptation. In Structures and Functions of Retinal Proteins. J. L. Rigaud, editor. John Libbey Eurotext Ltd., Montrouge, France. 115-118.
7. Bulashov, S. P., E. S. Imasheva, R. Govindjee, and T. G. Ebrey. 1996. Titration of aspartate-85 in bacteriorhodopsin: what it says about chromophore isomerization and proton release. Biophys. J. 70:473-481.
8. Braiman, M. S., T. Mogi, T. Marti, L. J. Stern, H. G. Khorana, and K. J. Rothschild. 1988. Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation changes of aspartic acid residues 85, 96, and 212. Biochemistry. 27:8516-8520.
9. Brown, L. S., L. Bonet, R. Needleman, and J. K. Lanyi. 1993. Estimated acid dissociation constants of the Schiff base, Asp-85, and Arg-82 during the bacteriorhodopsin photocycle. Biophys. J. 65:124-130.
10. Brown, L. S., J. Sasaki, H. Kandori, A. Maeda, R. Needleman, and J. K. Lanyi. 1995a. Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol Chem. 270: 27,122-27,126.
11. Brown, L. S., G. Váró, M. Hatanaka, J. Sasaki, H. Kandori, A. Maeda, N. Friedman, M. Sheves, R. Needleman, and J. K. Lanyi. 1995b. The complex extracellular domain regulates the deprotonation and reprotonation of the retinal Schiff base during the bacteriorhodopsin photocycle. Biochemistry. 34:12,903-12,911.
12. Cao, Y., L. S. Brown, R. Needleman, and J. K. Lanyi. 1993. Relationship of proton uptake on the cytoplasmic surface and the reisomerization of the retinal in the bacteriorhodopsin photocycle: an attempt to study the complex kinetics of the protons and the N and O intermediates. Biochemistry. 32:10,239-10,248.
13. Cao, Y., G. Váró, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1991. Water is required for proton transfer from aspartate 96 to the bacteriorhodopsin Schiff base. Biochemistry. 30:10,972-10,979.
14. Chernavskii, D. S., I. V. Chizhov, R. H. Lozier, T. M. Murina, A. M. Prokhorov, and B. V. Zubov. 1989. Kinetic model of bacteriorhodopsin photocycle: pathway from M state to bR. Photochem. Photobiol. 49: 649-653.
15. Der, A., P. Hargittai, and J. Simon. 1985. Time-resolved photoelectric and absorption signals from oriented purple membranes immobilized in gel. J. Biochem. Biophys. Methods. 10:259-300.
16. + release and uptake, and electric events in bacteriorhodopsin. FEBS Lett. 178:331-335.
17. Druckmann, S., M. P. Heyn, J. K. Lanyi, M. Ottolenghi, and L. Zimanyi. 1993. Thermal equilibration between the M and N intermediates in the photocycle of bacteriorhodopsin. Biophys. J. 65:1231-1234.
18. Ebrey, T. G. Light energy transduction in bacteriorhodopsin. In Thermodynamics of Membranes. Receptors and Channels. M. Jackson, editor. CRC Press, Boca Raton, FL. 353-387.
19. Gerwert, K., G. Souvignier, and B. Hess. 1990. Simultaneous monitoring of light-induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy. Proc. Natl. Acad. Sci. USA. 87:9774-9778.
20. Govindjee, R., S. P. Balashov, and T. G. Ebrey. 1990. Quantum efficiency of the photochemical cycle of bacteriorhodopsin. Biophys. J. 58: 597-608.
21. a of the chromophore's Schiff base can restore its light-induced deprotonation in the inactive Tyr-57->Asn mutant of bacteriorhodopsin. J. Biol. Chem. 269:14353-14354.
22. Govindjee, R., T. G. Ebrey, and A. R. Crofts. 1980. The quantum efficiency of proton pumping by the purple membrane of Halobacterium halobium. Biophys. J. 30:231-242.
23. Govindjee, R., M. Kono, S. P. Balashov, E. Imasheva, M. Sheves, and T. G. Ebrey. 1995. Effects of substitution of tyrosine 57 with asparagine and phenylalanine on the properties of bacteriorhodopsin. Biochemistry. 34:4828-4838.
24. Gutman, M., and E. Nachliel. 1995. The dynamics of proton exchange between bulk and surface groups. Biochim. Biophys. Acta. 1231: 123-138.
25. Heberle, J., and N. A. Dencher. 1992. Surface-bound probes monitor proton translocation and surface potential changes during the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 89:5996-6000.
26. Henderson, R., J. M. Baldwin, T. A. Ceska, F. Zemlin, E. Beckmann, and K. H. Downing. 1990. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213: 899-929.
27. Humphrey, W., I. Logunov, K. Schulten, and M. Sheves. 1994. Molecular dynamics study of bacteriorhodopsin and artificial pigments. Biochemistry: 33:3668-3678.
28. Keszthelyi, L., and P. Ormos. 1980. Electric signals associated with the photocycle of bacteriorhodopsin. FEBS Lett. 109:189-193.
29. Khorana, H. G. 1993. Two light-transducing membrane proteins: bacteriorhodopsin and the mammalian rhodopsin. Proc. Natl. Acad. Sci. USA. 90:1166-1171.
30. Kono, M., S. Misra, and T. G. Ebrey. 1993. pH dependence of light-induced proton release by bacteriorhodopsin. FEBS Lett. 331:31-34.
31. Lanyi, J. K. 1993. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta Bioenergetics. 1183:241-261.
32. Li, Q.-Q., R. Govindjee, and T. G. Ebrey. 1984. A correlation between proton pumping and the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 81:7079-7082.
33. Liu, S. Y. 1990. Light-induced currents from oriented purple membrane. I. Correlation of the microsecond component (B2) with the L-M photocycle transition. Biophys. J. 57:943-950.
34. Liu, S. Y., and T. G. Ebrey. 1988. Photocurrent measurements of the purple membrane oriented in a polyacrylamide gel. Biophys. J. 54:321-329.
35. Lozier, R. H., R. A. Bogomolni, and W. Stoeckenius. 1975. Bacteriorhodopsin: a light-driven proton pump in Halobacterium halobium. Biophys. J. 15:955-962.
36. Maeda, A., J. Sasaki, Y. Yamazaki. R. Needleman, and J. K. Lanyi. 1994. Interaction of aspartate-85 with a water molecule and the protonated Schiff base in the L intermediate of bacteriorhodopsin - a Fourier-transform infrared spectroscopic study. Biochemistry. 33:1713-1717.
37. Miercke, L. J. W., M. C. Betlach, A. K. Mitra, R. F. Shand, S. K. Fong, and R. M. Stroud. 1991. Wild-type and mutant bacteriorhodopsins D85N, D96N, and R82Q: purification to homogeneity. pH dependence of pumping, and electron diffraction. Biochemistry. 30:3088-3098.
38. Misra, S., S. P. Balashov, T. G. Ebrey, Y. Feng, R. K. Crouch, and D. R. Menick. 1996. Charge movements in the 13-cis photocycles of the bacteriorhodopsin mutants Arg82Lys and Arg82Gln. Biophys. J. 70: A108.
39. Oesterhelt, D., J. Tittor, and E. Bamberg. 1992. A unifying concept for ion translocation by retinal proteins. J. Bioenerg. Biomembr. 24:181-191.
40. Otto, H., T. Marti, M. Holz, T. Mogi, M. Lindau, H. G. Khorana, and M. P. Heyn. 1989. Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 86:9228-9232.
41. Otto, H., T. Marti, M. Holz, T. Mogi, L. J. Stern, F. Engle, H. G. Khorana, and M. P. Heyn. 1990. Substitution of amino acids Asp-85. Asp-212, and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base. Proc. Natl. Acad. Sci. USA. 87:1018-1022.
42. a's of Asp-85 and Glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry. 35:4054-4062.
43. Rothschild, K. J. 1992. FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J. Bioenerg. Biomembr. 24:147-167.
44. Sampogna, R. V., and B. Honig. 1994. Environmental effects on the protonation states of active site residues in bacteriorhodopsin. Biophys. J. 66:1341-1352.
45. Sampogna, R. V., and B. Honig. 1996. Electrostatic coupling between retinal isomerization and the ionization state of Glu-204: a general mechanism for proton release in bacteriorhodopsin. Biophys. J. In press.
46. 96 → Asn bacteriorhodopsin. J. Biol. Chem. 267:20,782-20,786.
47. Scharnagl, C., J. Hettenkofer, and S. F. Fischer. 1994. Proton release pathway in bacteriorhodopsin: molecular dynamics and electrostatic calculations, Intl. J. Quantum Chem. S21:33-56.
48. Scharnagl, C., J. Hettenkofer, and S. F. Fischer. 1995. Electrostatic and conformational effects on the proton translocation steps in bacteriorhodopsin: analysis of multiple M structures. J. Phys. Chem. 99:7787-7800.
49. Scherrer, P., U. Alexiev, H. Otto, M. P. Heyn, T. Marti, and H. G. Khorana. 1992. Proton movement and surface charge in bacteriorhodopsin detected by selectively attached pH-indicators. In Structures and Functions of Retinal Proteins. J. L. Rigaud, editor. John Libbey Eurotext Ltd., Montrouge, France. 205-211.
50. Siebert, F., W. Mäntele, and W. Kreutz. 1982. Evidence for the protonation of two internal carboxylic groups during the photocycle of bacteriorhodopsin. FEBS Lett. 141:82-87.
51. Souvignier, G., and K. Gerwert. 1992. Proton uptake mechanism of bacteriorhodopsin as determined by time-resolved stroboscopic-FTIR-spectroscopy. Biophys. J. 63:1393-1405.
52. Stern, L. J., and H. G. Khorana. 1989. Structure-function studies on bacteriorhodopsin: X. Individual substitutions of arginine residues by glutamine affect chromophore formation, photocycle, and proton translocation. J. Biol. Chem. 264:14,202-14,208.
53. Subramaniam, S., M. Gerstein, D. Oesterhelt, and R. Henderson. 1993. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12:1-8.
54. Subramaniam, S., T. Marti, and H. G. Khorana. 1990. Protonation state of Asp (Glu)-85 regulates the purple-to-blue transition in bacteriorhodopsin mutants Arg-82 → Ala and Asp-85 → Glu: the blue form is inactive in proton translocation. Proc. Natl Acad. Sci. USA. 87:1013-1017.
55. Thorgeirsson, T. E., S. J. Milder, L. J. W. Miercke, M. C. Betlach, R. F. Shand, R. M. Stroud, and D. S. Kliger. 1991. Effects of Asp-96 → Asn, Asp-85 → Asn, and Arg82 → Gln single-site substitutions on the photocycle of bacteriorhodopsin. Biochemistry. 30:9133-9142.
56. Trissl, H.-W. 1990. Photoelectric measurement of purple membranes. Photochem. Photobiol. 51:793-818.
57. Váró, G., and J. K. Lanyi. 1990. Pathways of the rise and decay of the M photointermediate of bacteriorhodopsin. Biochemistry. 29:2241-2250.
58. Zhou, F., A. Windemuth, and K. Schulten. 1993. Molecular dynamics study of the proton pump cycle of bacteriorhodopsin. Biochemistry. 32:2291-2306.
59. Zimdnyi, L., G. Váró, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1992. Pathways of proton release in the bacteriorhodopsin photocycle. Biochemistry. 31:8535-8543.