Chemical and physical evidence for multiple functional steps comprising the M state of the bacteriorhodopsin photocycle.

In the photocycle of bacteriorhodopsin (bR), light-induced transfer of a proton from the Schiff base to an acceptor group located in the extracellular half of the protein, followed by reprotonation from the cytoplasmic side, are key steps in vectorial proton pumping. Between the deprotonation and reprotonation events, bR is in the M state. Diverse experiments undertaken to characterize the M state support a model in which the M state is not a static entity, but rather a progression of two or more functional substates. Structural changes occurring in the M state and in the entire photocycle of wild-type bR can be understood in the context of a model which reconciles the chloride ion-pumping phenotype of mutants D85S and D85T with the fact that bR creates a transmembrane proton-motive force.

[1]  J. Lanyi,et al.  Understanding structure and function in the light-driven proton pump bacteriorhodopsin. , 1998, Journal of structural biology.

[2]  J. Lanyi,et al.  Distortions in the photocycle of bacteriorhodopsin at moderate dehydration. , 1991, Biophysical journal.

[3]  B. Hess,et al.  The photochemical reaction of the 412 nm chromophore of bacteriorhodopsin , 1977, FEBS letters.

[4]  D. Oesterhelt,et al.  The tertiary structural changes in bacteriorhodopsin occur between M states: X‐ray diffraction and Fourier transform infrared spectroscopy , 1997, The EMBO journal.

[5]  D. Oesterhelt,et al.  Rhodopsin-like protein from the purple membrane of Halobacterium halobium. , 1971, Nature: New biology.

[6]  Karl Edman,et al.  High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle , 1999, Nature.

[7]  W. W. Parson,et al.  Flash-induced volume changes of bacteriorhodopsin-containing membrane fragments and their relationship to proton movements and absorbance transients. , 1978, The Journal of biological chemistry.

[8]  R. Glaeser,et al.  Characterization of the conformational change in the M1 and M2 substates of bacteriorhodopsin by the combined use of visible and infrared spectroscopy. , 1992, Journal of structural biology.

[9]  U. Lachish,et al.  TIME RESOLUTION OF A BACK PHOTOREACTION IN BACTERIORHODOPSIN , 1978 .

[10]  R. Callender,et al.  A DETAILED RESONANCE RAMAN STUDY OF THE M412 INTERMEDIATE IN THE BACTERIORHODOPSIN PHOTOCYCLE , 1985, Photochemistry and photobiology.

[11]  R. Shrager,et al.  Influence of excitation energy on the bacteriorhodopsin photocycle. , 1994, Biochemistry.

[12]  J. Lanyi,et al.  The back photoreaction of the M intermediate in the photocycle of bacteriorhodopsin: mechanism and evidence for two M species , 1992, Photochemistry and photobiology.

[13]  Proton uptake mechanism of bacteriorhodopsin as determined by time-resolved stroboscopic-FTIR-spectroscopy. , 1992, Biophysical journal.

[14]  B. Honig,et al.  Environmental effects on formation and photoreaction of the M412 photoproduct of bacteriorhodopsin: implications for the mechanism of proton pumping. , 1981, Biochemistry.

[15]  F. Siebert,et al.  Time-resolved step-scan Fourier transform infrared spectroscopy reveals differences between early and late M intermediates of bacteriorhodopsin. , 1999, Biophysical journal.

[16]  R. Glaeser,et al.  The bacteriorhodopsin photocycle: direct structural study of two substrates of the M-intermediate. , 1994, Biophysical journal.

[17]  J. Lanyi,et al.  Pathways of proton release in the bacteriorhodopsin photocycle. , 1992, Biochemistry.

[18]  H Luecke,et al.  Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. , 1999, Science.

[19]  B. Hess,et al.  Kinetic interaction between aromatic residues and the retinal chromophore of bacteriorhodopsin during the photocycle , 1979, FEBS letters.

[20]  J. Nagle,et al.  PHOTOCYCLE KINETICS: ANALYSIS OF RAMAN DATA FROM BACTERIORHODOPSIN * , 1991, Photochemistry and photobiology.

[21]  R. Govindjee,et al.  The quantum efficiency of proton pumping by the purple membrane of Halobacterium halobium. , 1980, Biophysical journal.

[22]  Miss A.O. Penney.  (b) , 1974, The New Yale Book of Quotations.

[23]  J. Lanyi,et al.  Conformational change of helix G in the bacteriorhodopsin photocycle: investigation with heavy atom labeling and x-ray diffraction. , 1999, Biophysical journal.

[24]  R. Henderson,et al.  Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. , 1990, Journal of molecular biology.

[25]  R. Callender,et al.  Resonance Raman studies of the purple membrane. , 1977, Biochemistry.

[26]  M. Saraste,et al.  FEBS Lett , 2000 .

[27]  D. Oesterhelt,et al.  Structure and hydration of the M-state of the bacteriorhodopsin mutant D96N studied by neutron diffraction. , 1998, Journal of molecular biology.

[28]  J. Lanyi,et al.  Effects of the crystalline structure of purple membrane on the kinetics and energetics of the bacteriorhodopsin photocycle. , 1991, Biochemistry.

[29]  R. Glaeser,et al.  Structural characterization of the L-to-M transition of the bacteriorhodopsin photocycle. , 1998, Biophysical journal.

[30]  J. Lanyi,et al.  Interaction of proton and chloride transfer pathways in recombinant bacteriorhodopsin with chloride transport activity: implications for the chloride translocation mechanism. , 1996, Biochemistry.

[31]  J. Vonck.  A three-dimensional difference map of the N intermediate in the bacteriorhodopsin photocycle: part of the F helix tilts in the M to N transition. , 1996, Biochemistry.

[32]  J. Lanyi,et al.  The last phase of the reprotonation switch in bacteriorhodopsin: the transition between the M-type and the N-type protein conformation depends on hydration. , 1997, Biochemistry.

[33]  G. Varo,et al.  The role of water in the extracellular half channel of bacteriorhodopsin. , 1997, Biophysical journal.

[34]  M. P. Heyn,et al.  Between the ground‐ and M‐state of bacteriorhodopsin the retinal transition dipole moment tilts out of the plane of the membrane by only 3° , 1991, FEBS letters.

[35]  H Luecke,et al.  Structure of bacteriorhodopsin at 1.55 A resolution. , 1999, Journal of molecular biology.

[36]  R. Henderson,et al.  Protein conformational changes in the bacteriorhodopsin photocycle. , 1999, Journal of molecular biology.

[37]  R. Griffin,et al.  Early and late M intermediates in the bacteriorhodopsin photocycle: a solid-state NMR study. , 1998, Biochemistry.

[38]  R. Korenstein,et al.  Bacteriorhodopsin: Biphasic kinetics of phototransients and of light‐induced proton transfer by sub‐bacterial Halobacterium halobium particles and by reconstituted liposomes , 1976, FEBS letters.

[39]  M. Kataoka,et al.  Arginine remarkably prolongs the lifetime of the M‐intermediate in the bacteriorhodopsin photocycle at room temperature , 1989 .

[40]  J. Lanyi,et al.  Protein changes associated with reprotonation of the Schiff base in the photocycle of Asp96-->Asn bacteriorhodopsin. The MN intermediate with unprotonated Schiff base but N-like protein structure. , 1992, The Journal of biological chemistry.

[41]  Masasuke Yoshida,et al.  ON THE TWO FORMS OF INTERMEDIATE M OF BACTERIORHODOPSIN , 1981 .

[42]  W. Stoeckenius,et al.  Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. , 1974, The Journal of biological chemistry.

[43]  K. Gerwert,et al.  A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. , 1993, Biophysical journal.

[44]  J. Lanyi,et al.  THE TWO CONSECUTIVE M SUBSTATES IN THE PHOTOCYCLE OF BACTERIORHODOPSIN ARE AFFECTED SPECIFICALLY BY THE D85N AND D96N RESIDUE REPLACEMENTS , 1992, Photochemistry and photobiology.

[45]  B Hess,et al.  Light-driven protonation changes of internal aspartic acids of bacteriorhodopsin: an investigation by static and time-resolved infrared difference spectroscopy using [4-13C]aspartic acid labeled purple membrane. , 1985, Biochemistry.

[46]  S. P. Fodor,et al.  Chromophore structure in bacteriorhodopsin's N intermediate: implications for the proton-pumping mechanism. , 1988, Biochemistry.

[47]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[48]  J. Lanyi,et al.  Conversion of bacteriorhodopsin into a chloride ion pump. , 1995, Science.

[49]  E. Bamberg,et al.  Voltage dependence of proton pumping by bacteriorhodopsin is regulated by the voltage-sensitive ratio of M1 to M2. , 1998, Biophysical journal.

[50]  M. P. Heyn,et al.  Evidence for the first phase of the reprotonation switch of bacteriorhodopsin from time-resolved photovoltage and flash photolysis experiments on the photoreversal of the M-intermediate. , 1997, Biophysical journal.

[51]  Hans Frauenfelder,et al.  Complexity in proteins , 1995, Nature Structural Biology.

[52]  S. Misra.  Contribution of proton release to the B2 photocurrent of bacteriorhodopsin. , 1998, Biophysical journal.

[53]  Evidence for charge-controlled conformational changes in the photocycle of bacteriorhodopsin. , 1998, Biophysical journal.

[54]  J. Nagle,et al.  Molecular models of proton pumps , 1981 .

[55]  J. Lanyi,et al.  Deriving the intermediate spectra and photocycle kinetics from time-resolved difference spectra of bacteriorhodopsin. The simpler case of the recombinant D96N protein. , 1993, Biophysical journal.

[56]  T. Thorgeirsson,et al.  Transient channel-opening in bacteriorhodopsin: an EPR study. , 1997, Journal of molecular biology.

[57]  D. Oesterhelt,et al.  Closing in on bacteriorhodopsin: progress in understanding the molecule. , 1999, Annual review of biophysics and biomolecular structure.

[58]  W. Eisfeld,et al.  Resonance Raman and optical transient studies on the light-induced proton pump of bacteriorhodopsin reveal parallel photocycles. , 1993, Biochemistry.

[59]  S. Caplan,et al.  Modulation excitation spectrophotometry of purple membrane of Halobacterium halobium , 1975, Nature.

[60]  J. Lanyi,et al.  Thermodynamics and energy coupling in the bacteriorhodopsin photocycle. , 1991, Biochemistry.

[61]  Y. Amemiya,et al.  Crystallographic characterization by X‐ray diffraction of the M‐intermediate from the photo‐cycle of bacteriorhodopsin at room temperature , 1991, FEBS letters.

[62]  S. P. Balashov,et al.  [New intermediates in the photochemical transformation of rhodopsin]. , 1977, Biofizika.

[63]  R. Lozier,et al.  Procedure for testing kinetic models of the photocycle of bacteriorhodopsin. , 1982, Biophysical journal.

[64]  E. Lam,et al.  Nonionic detergent effects on spectroscopic characteristics and the photocycle of bacteriorhodopsin in purple membranes. , 1983, Archives of biochemistry and biophysics.

[65]  W. Stoeckenius,et al.  Kinetics and stoichiometry of light-induced proton release and uptake from purple membrane fragments, Halobacterium halobium cell envelopes, and phospholipid vesicles containing oriented purple membrane. , 1976, Biochimica et biophysica acta.

[66]  B. Hess,et al.  Hydration effects on the photocycle of bacteriorhodopsin in thin layers of purple membrane , 1977, Nature.

[67]  H Luecke,et al.  Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. , 1998, Science.

[68]  P. Ormos,et al.  Mechanism of generation and regulation of photopotential by bacteriorhodopsin in bimolecular lipid membrane. , 1978, Biochimica et biophysica acta.

[69]  B. Hess,et al.  Spectrally silent transitions in the bacteriorhodopsin photocycle. , 1996, Biophysical journal.

[70]  D. Oesterhelt,et al.  Time‐resolved X‐ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin. , 1991, The EMBO journal.

[71]  R. Glaeser,et al.  Two progressive substrates of the M-intermediate can be identified in glucose-embedded, wild-type bacteriorhodopsin. , 1994, Biophysical journal.

[72]  P. Tavan,et al.  A mechanism for the light-driven proton pump of Halobacterium halobium , 1978, Nature.

[73]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[74]  K. Gerwert,et al.  Fourier transform infrared double-flash experiments resolve bacteriorhodopsin's M1 to M2 transition. , 1997, Biophysical journal.

[75]  J. Lanyi,et al.  Pathways of the rise and decay of the M photointermediate(s) of bacteriorhodopsin. , 1990, Biochemistry.

[76]  W. Stoeckenius,et al.  Bacteriorhodopsin: a light-driven proton pump in Halobacterium Halobium. , 1975, Biophysical journal.

[77]  A. J. Clifford,et al.  BIOCHIMICA ET BIOPHYSICA ACTA , 2022 .

[78]  J. Lanyi,et al.  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. , 1994, Biochemistry.

[79]  J. Lanyi,et al.  Kinetic and spectroscopic evidence for an irreversible step between deprotonation and reprotonation of the Schiff base in the bacteriorhodopsin photocycle. , 1991, Biochemistry.

[80]  T. Yoshizawa,et al.  Water structural changes in the bacteriorhodopsin photocycle: analysis by Fourier transform infrared spectroscopy. , 1992, Biochemistry.

[81]  A. Kaulen,et al.  Interrelations of M‐intermediates in bacteriorhodopsin photocycle , 1992, FEBS letters.

[82]  M. Gerstein,et al.  Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. , 1993, The EMBO journal.