Structural determinants of purple membrane assembly.

The purple membrane is a two-dimensional crystalline lattice formed by bacteriorhodopsin and lipid molecules in the cytoplasmic membrane of Halobacterium salinarum. High-resolution structural studies, in conjunction with detailed knowledge of the lipid composition, make the purple membrane one of the best models for elucidating the forces that are responsible for the assembly and stability of integral membrane protein complexes. In this review, recent mutational efforts to identify the structural features of bacteriorhodopsin that determine its assembly in the purple membrane are discussed in the context of structural, calorimetric and reconstitution studies. Quantitative evidence is presented that interactions between transmembrane helices of neighboring bacteriorhodopsin molecules contribute to purple membrane assembly. However, other specific interactions, particularly between bacteriorhodopsin and lipid molecules, may provide the major driving force for assembly. Elucidating the molecular basis of protein-protein and protein-lipid interactions in the purple membrane may provide insights into the formation of integral membrane protein complexes in other systems.

[1]  D. Oesterhelt,et al.  Homologous bacterio-opsin-encoding gene expression via site-specific vector integration. , 1993, Gene.

[2]  Y. Mukohata,et al.  THE WHITE MEMBRANE OF CRYSTALLINE BACTERIOOPSIN IN HALOBACTERIUM HALOBIUM STRAIN R1mW AND ITS CONVERSION INTO PURPLE MEMBRANE BY EXOGENOUS RETINAL , 1981 .

[3]  M. Krebs,et al.  Intramembrane substitutions in helix D of bacteriorhodopsin disrupt the purple membrane. , 1997, Journal of molecular biology.

[4]  R. Henderson,et al.  Three-dimensional model of purple membrane obtained by electron microscopy , 1975, Nature.

[5]  E. Beckmann,et al.  Lipid location in deoxycholate-treated purple membrane at 2.6 A. , 1995, Journal of molecular biology.

[6]  C Menzel,et al.  Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 A resolution. , 1999, Structure.

[7]  F. Hartl,et al.  Principles of protein folding in the cellular environment. , 1999, Current opinion in structural biology.

[8]  M. Krebs,et al.  Role of helix-helix interactions in assembly of the bacteriorhodopsin lattice. , 1999, Biochemistry.

[9]  A. Agostiano,et al.  Light‐dependent and Biochemical Properties of Two Different Bands of Bacteriorhodopsin Isolated on Phenyl‐Sepharose CL‐4B , 1999 .

[10]  S M Prince,et al.  Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: modular assembly and protein pigment interactions. , 1997, Journal of molecular biology.

[11]  D. Oesterhelt,et al.  [21] Biogenesis of purple membrane in halobacteria , 1983 .

[12]  J. Lanyi,et al.  An efficient system for the synthesis of bacteriorhodopsin in Halobacterium halobium. , 1990, Gene.

[13]  J. Torres,et al.  Analysis of conformational changes in bacteriorhodopsin upon retinal removal. , 1996, Biophysical journal.

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

[15]  E. Pebay-Peyroula,et al.  X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. , 1997, Science.

[16]  U. Wölfer,et al.  Bacteriorhodopsin precursor is processed in two steps. , 1988, European journal of biochemistry.

[17]  A. Bogan,et al.  Anatomy of hot spots in protein interfaces. , 1998, Journal of molecular biology.

[18]  D. Oesterhelt,et al.  Localization of glycolipids in membranes by in vivo labeling and neutron diffraction. , 1998, Molecular cell.

[19]  H. G. Khorana.  Anderegg, R. J.,Nihei, K.,and Biemann Amino acid sequence of bacteriorhodopsin , 1979 .

[20]  A. Kidera,et al.  The structure of bacteriorhodopsin at 3.0 A resolution based on electron crystallography: implication of the charge distribution. , 1999, Journal of molecular biology.

[21]  R Henderson,et al.  Specific labelling of the protein and lipid on the extracellular surface of purple membrane. , 1978, Journal of molecular biology.

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

[23]  Akinori Kidera,et al.  Surface of bacteriorhodopsin revealed by high-resolution electron crystallography , 1997, Nature.

[24]  Bacteriorhodopsin: the mechanism of 2D-array formation and the structure of retinal in the protein. , 1995, Biophysical chemistry.

[25]  J. Rigaud,et al.  Monomer-oligomer equilibrium of bacteriorhodopsin in reconstituted proteoliposomes. A freeze-fracture electron microscope study. , 1987, The Journal of biological chemistry.

[26]  PHASE BEHAVIOR AND INTERACTIONS OF THE MEMBRANE-PROTEIN BACTERIORHODOPSIN , 1999 .

[27]  W. Stoeckenius,et al.  A MORPHOLOGICAL STUDY OF HALOBACTERIUM HALOBIUM AND ITS LYSIS IN MEDIA OF LOW SALT CONCENTRATION , 1967, The Journal of cell biology.

[28]  C. Brouillette,et al.  pH dependence of bacteriorhodopsin thermal unfolding. , 1987, Biochemistry.

[29]  A. Watts,et al.  The essential role of specific Halobacterium halobium polar lipids in 2D-array formation of bacteriorhodopsin. , 1992, Biochimica et biophysica acta.

[30]  R. Hendler,et al.  Membrane-mediated control of the bacteriorhodopsin photocycle. , 1994, Biochemistry.

[31]  J. Sturtevant,et al.  Phase transitions of the purple membranes of Halobacterium halobium. , 1978, Biochemistry.

[32]  T. Thorgeirsson,et al.  Bacteriorhodopsin D85N: three spectroscopic species in equilibrium. , 1993, Biochemistry.

[33]  James H. Prestegard,et al.  A Transmembrane Helix Dimer: Structure and Implications , 1997, Science.

[34]  D. Engelman,et al.  Membrane protein folding and oligomerization: the two-stage model. , 1990, Biochemistry.

[35]  W. G. Martin,et al.  Characterization and composition of the purple and red membrane from Halobacterium cutirubrum;. , 1975, Canadian journal of biochemistry.

[36]  Dieter Oesterhelt,et al.  [3] Reconstitution of the retinal proteins bacteriorhodopsin and halorhodopsin , 1982 .

[37]  [53] Isolation of the white membrane of crystalline bacterio-opsin from Halobacterium halobium R1mW lacking carotenoid , 1982 .

[38]  L. Miercke,et al.  Purification of bacteriorhodopsin and characterization of mature and partially processed forms. , 1989, The Journal of biological chemistry.

[39]  A. Watts,et al.  The effect of temperature and protein content on the dispersive properties of bacteriorhodopsin from H. halobium in reconstituted DMPC complexes free of endogenous purple membrane lipids: A freeze-fracture electron microscopy study , 1989 .

[40]  M. Sumper,et al.  Studies on the biosynthesis of bacterio-opsin. Demonstration of the existence of protein species structurally related to bacterio-opsin. , 1978, European journal of biochemistry.

[41]  T. Mitsui,et al.  Phase transitions of the purple membrane and the brown holo-membrane X-ray diffraction, circular dichroism spectrum and absorption spectrum studies , 1981 .

[42]  K. Schulten,et al.  The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. , 1996, Structure.

[43]  F. Payan,et al.  Carbohydrate binding sites in a pancreatic α‐amylase‐substrate complex, derived from X‐ray structure analysis at 2.1 Å resolution , 1995, Protein science : a publication of the Protein Society.

[44]  D. Engelman,et al.  Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices. , 1992, The Journal of biological chemistry.

[45]  S. DasSarma,et al.  Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker , 2000, Molecular microbiology.

[46]  M. Sumper,et al.  Biogenesis of purple membrane: Regulation of bacterio‐opsin synthesis , 1976, FEBS letters.

[47]  W. Stoeckenius,et al.  SPONTANEOUS AGGREGATION OF BACTERIORHODOPSIN IN BROWN MEMBRANE , 1981 .

[48]  W. Kühlbrandt,et al.  Trimerization and crystallization of reconstituted light‐harvesting chlorophyll a/b complex. , 1994, The EMBO journal.

[49]  D. Oesterhelt,et al.  Towards structural investigations on isotope labelled native bacteriorhodopsin in detergent micelles by solution-state NMR spectroscopy , 1997 .

[50]  Y. Mukohata,et al.  SOME OBSERVATIONS ON THE MORPHOGENESIS OF LATTICE STRUCTURE IN THE PURPLE MEMBRANE , 1981 .

[51]  D. Engelman,et al.  Sequence specificity in the dimerization of transmembrane alpha-helices. , 1992, Biochemistry.

[52]  R. Hendler,et al.  Chemical and functional studies on the importance of purple membrane lipids in bacteriorhodopsin photocycle behavior , 1996, FEBS letters.

[53]  J M Sturtevant,et al.  Thermodynamic measurements of the contributions of helix-connecting loops and of retinal to the stability of bacteriorhodopsin. , 1992, Biochemistry.

[54]  D. Engelman,et al.  The effect of point mutations on the free energy of transmembrane alpha-helix dimerization. , 1997, Journal of molecular biology.

[55]  H. Khorana,et al.  Structure and thermal stability of monomeric bacteriorhodopsin in mixed pospholipid/detergent micelles , 1989, Proteins.

[56]  M. Krebs,et al.  Membrane Insertion Kinetics of a Protein Domain In Vivo , 1999, The Journal of Biological Chemistry.

[57]  S. White,et al.  Membrane protein folding and stability: physical principles. , 1999, Annual review of biophysics and biomolecular structure.

[58]  P. Kraulis.  A program to produce both detailed and schematic plots of protein structures , 1991 .

[59]  R. Henderson,et al.  Temperature-dependent aggregation of bacteriorhodopsin in dipalmitoyl- and dimyristoylphosphatidylcholine vesicles. , 1978, Journal of molecular biology.

[60]  R. Hendler,et al.  Importance of specific native lipids in controlling the photocycle of bacteriorhodopsin. , 1998, Biochemistry.

[61]  Thermal transitions in the purple membrane from Halobacterium halobium , 1993, FEBS letters.

[62]  J. Riesle,et al.  D38 is an essential part of the proton translocation pathway in bacteriorhodopsin. , 1996, Biochemistry.

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

[64]  R. Hendler,et al.  Control of the integral membrane proton pump, bacteriorhodopsin, by purple membrane lipids of Halobacterium halobium. , 1996, Biochemistry.

[65]  D. Oesterhelt,et al.  Biosynthesis of the purple membrane of halobacteria. , 1976, Angewandte Chemie.

[66]  M. Kates,et al.  [13] Lipids of purple membrane from extreme halophiles and of methanogenic bacteria , 1982 .

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

[68]  R Henderson,et al.  Electron-crystallographic refinement of the structure of bacteriorhodopsin. , 1996, Journal of molecular biology.

[69]  T. Mitsui,et al.  Formation of the two-dimensional hexagonal lattice of bacteriorhodopsin in reconstituted brown membrane. , 1978, Biochimica et biophysica acta.

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