Architecture of helix bundle membrane proteins: An analysis of cytochrome c oxidase from bovine mitochondria
Erik Wallin
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Search for more papers by this authorTomitake Tsukihara
Institute for Protein Research, Osaka University, 3-2 Yamada-oka, Suita 565, Japan
Search for more papers by this authorShinya Yoshikawa
Department of Life Science, Himeji Institute of Technology, Kamigohri Akoh, Hyogo 678-12, Japan
Search for more papers by this authorGunnar Von Heijne
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Search for more papers by this authorCorresponding Author
Arne Elofsson
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, SwedenSearch for more papers by this authorErik Wallin
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Search for more papers by this authorTomitake Tsukihara
Institute for Protein Research, Osaka University, 3-2 Yamada-oka, Suita 565, Japan
Search for more papers by this authorShinya Yoshikawa
Department of Life Science, Himeji Institute of Technology, Kamigohri Akoh, Hyogo 678-12, Japan
Search for more papers by this authorGunnar Von Heijne
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Search for more papers by this authorCorresponding Author
Arne Elofsson
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, Sweden
Department of Biochemistry, Stockholm University, S-106 91 Stockholm, SwedenSearch for more papers by this authorAbstract
We have analyzed the structure of mitochondrial cytochrome c oxidase in terms of general characteristics thought to be important for describing the architecture of helix bundle membrane proteins. Many aspects of the structure are similar to what has previously been found for the photosynthetic reaction center and bacteriorhodopsin. Our results lead to a considerably more precise general picture of membrane protein architecture than has hitherto been possible to obtain.
References
- Allen J, Feher G, Yeates T, Komiya H, Rees D. 1987. Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc Natl Acad Sci USA 84: 6162–6166.
- Aurora R, Srinivasan R, Rose GD. 1994. Rules for α-helix termination by glycine. Science 264: 1126–1130.
- Bairoch A, Boeckmann B. 1991. The SwissProt protein sequence data bank. Nucleic Acids Res 19: 2247–2249.
- Bowie JU, Luthy R, Eisenberg D. 1991. A method to identify protein sequences that fold into a known 3-dimensional structure. Science 253: 164–170.
- Claverie J-M, Daulmiere C. 1991. Smoothing profiles with sliding windows: Better to wear a hat! CABIOS 7: 113–115.
-
Conolly MJ.
1983.
Analytical molecular surface calculation.
J Appl Crystallogr
17:
548–558.
10.1107/S0021889883010985 Google Scholar
- Cowan SW, Rosenbusch JP. 1994. Folding pattern diversity of integral membrane proteins. Science 264: 914–916.
- Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP. 1992. Crystal structures explain functional properties of two E. coli porins. Nature 358: 727–733.
- Deisenhofer J, Epp O, Miki K, Huber R, Michel H. 1985. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution. Nature 318: 618–624.
- Doig AJ, Baldwin RL. 1995. N- and C-capping preferences for all 20 amino acids in α-helical peptides. Protein Sci 4: 1325–1336.
- Eisenberg D, McLachlan AD. 1986. Solvation energy in protein folding. Nature 319: 199–203.
- Engelman DM, Steitz TA, Goldman A. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem 15: 321–353.
- Gavel Y, von Heijne G. 1992. The distribution of charged amino acids in mitochondrial inner membrane proteins suggests different modes of membrane integration for nuclearly and mitochondrially encoded proteins. Eur J Biochem 205: 1207–1215.
- Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R. 1996. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 259: 393–421.
- Iwata S, Ostermeier C, Ludwig B, Michel H. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660–669.
- Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577–2637.
- Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946–950.
- Kuhlbrandt W, Wang DN, Fujiyoshi Y. 1994. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621.
- Kyte J, Doolittle RF. 1982. A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132.
-
Le Grand S,
Merz KJ.
1993.
Rapid approximation to molecular surface area via the use of booleans look-up tables.
J Global Optimiz
3:
49–66.
10.1007/BF01100239 Google Scholar
- MacArthur MW, Thornton JM. 1991. Influence of proline residues on protein conformation. J Mol Biol 218: 397–412.
- McDermott G, Price SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ, Isaacs NW. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521.
- Pawagi AB, Wang J, Silverman M, Reithmeier RAF, Deber CM. 1994. Transmembrane aromatic amino acid distribution in P-glycoprotein. A functional role in broad substrate specificity. J Mol Biol 235: 554–564.
- Pearson WR, Lipman DJ. 1988. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444–2448.
- Persson B, Argos P. 1994. Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J Mol Biol 237: 182–192.
- Rao JK, Argos A. 1986. A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869: 197–214.
- Rees DC, DeAntonio L, Eisenberg D. 1989a. Hydrophobic organization of membrane proteins. Science 245: 510–513.
- Rees DC, Komiya H, Yeates TO, Allen JP, Feher G. 1989b. The bacterial photosynthetic reaction center as a model for membrane proteins. Annu Rev Biochem 58: 607–633.
- Richardson JS, Richardson DC. 1988. Amino acid preferences for specific locations at the ends of α-helices. Science 240: 1648–1652.
- Samatey FA, Xu C, Popot J-C. 1995. On the distribution of amino acid residues in transmembrane α-helix bundles. Proc Natl Acad Sci USA 92: 4577–4581.
- Schneider TD, Stormo GD, Gold L, Ehrenfeucht A. 1986. Information content of binding sites on nucleotide sequences. J Mol Biol 788: 415–431.
- Taylor WR, Jones DT, Green NM. 1994. A method for α-helical integral membrane protein fold prediction. Proteins Struct Fund Genet 18: 281–294.
- Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
- Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. 1995. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269: 1069–1064.
- Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. 1996. The whole stucture of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272: 1136–1144.
- von Heijne G. 1986. The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5: 3021–3027.
- von Heijne G. 1991. Proline kinks in transmembrane α-helices. J Mol Biol 218: 499–503.
- von Heijne G. 1992. Membrane protein structure prediction—Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487–494.
- von Heijne G. 1994. Membrane proteins: From sequence to structure. Annu Rev Biophys Biomol Struct 23: 167–192.
- Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E, Schulz GE. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science 254: 1627–1630.
- Woolfson DN, Williams DH. 1990. The influence of proline residues on α-helical structure. FEBS Lett 277: 185–188.
- Yeates TO, Komiya H, Rees DC, Allen JP, Feher G. 1987. Structure of the reaction center from Rhodobacter sphaeroides: Membrane-protein interactions. Proc Natl Acad Sci USA 84: 6438–6442.