Advertisement

Journal of Molecular Evolution

, Volume 77, Issue 4, pp 134–158 | Cite as

Evolution of the Genetic Code by Incorporation of Amino Acids that Improved or Changed Protein Function

  • Brian R. FrancisEmail author
Original Paper

Abstract

Fifty years have passed since the genetic code was deciphered, but how the genetic code came into being has not been satisfactorily addressed. It is now widely accepted that the earliest genetic code did not encode all 20 amino acids found in the universal genetic code as some amino acids have complex biosynthetic pathways and likely were not available from the environment. Therefore, the genetic code evolved as pathways for synthesis of new amino acids became available. One hypothesis proposes that early in the evolution of the genetic code four amino acids—valine, alanine, aspartic acid, and glycine—were coded by GNC codons (N = any base) with the remaining codons being nonsense codons. The other sixteen amino acids were subsequently added to the genetic code by changing nonsense codons into sense codons for these amino acids. Improvement in protein function is presumed to be the driving force behind the evolution of the code, but how improved function was achieved by adding amino acids has not been examined. Based on an analysis of amino acid function in proteins, an evolutionary mechanism for expansion of the genetic code is described in which individual coded amino acids were replaced by new amino acids that used nonsense codons differing by one base change from the sense codons previously used. The improved or altered protein function afforded by the changes in amino acid function provided the selective advantage underlying the expansion of the genetic code. Analysis of amino acid properties and functions explains why amino acids are found in their respective positions in the genetic code.

Keywords

Genetic code Evolution Protein function 

Notes

Acknowledgments

I wish to thank Professor Kensal van Holde for helpful comments on this paper.

Conflict of interest

The author declares that he has no conflict of interest.

Supplementary material

239_2013_9567_MOESM1_ESM.pdf (214 kb)
Supplementary material 1 (PDF 214 kb)

References

  1. Abillon E, Bremier L, Cardinaud R (1990) Conformational calculations on the Ala14-Pro27 LC1 segment of rabbit skeletal myosin. Biochim Biophys Acta 1037:394–400PubMedGoogle Scholar
  2. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628PubMedGoogle Scholar
  3. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615PubMedGoogle Scholar
  4. Agris PF, Vendeix FAP, Graham WD (2007) tRNA’s wobble decoding of the genome: 40 years of modification. J Mol Biol 366:1–13PubMedGoogle Scholar
  5. Ahvazi B, Coulombe R, Delarge M, Vedadi M, Zhang L, Meighen E, Vrielink A (2000) Crystal structure of the NADP+-dependent aldehyde dehydrogenase from Vibrio harveyi: structural implications for cofactor specificity and affinity. Biochem J 349:853–861PubMedPubMedCentralGoogle Scholar
  6. An Bondar, Dau H (2012) Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim Biophys Acta 1817:1177–1190Google Scholar
  7. Anjana R, Vaishnavi MK, Sherlin D, Kumer SP, Naveen K, Kanth PS, Sekar K (2012) Aromatic–aromatic interactions in structures of proteins and protein–DNA complexes: a study based on orientation and distance. Bioinformation 8:1220–1224PubMedPubMedCentralGoogle Scholar
  8. Aravind L, Ponting CP (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signaling proteins. FEMS Microbiol Lett 176:111–116PubMedGoogle Scholar
  9. Arnesano F, Banci L, Bertini I, Mangani S, Thompsett AR (2003) A redox switch in CopC: an intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites. Proc Natl Acad Sci USA 100:3814–3819PubMedGoogle Scholar
  10. Arraiano CM, Matos RG, Barbas A (2010) RNase II: the finer details of the Modus operandi of a molecular killer. RNA Biol 7:276–281PubMedGoogle Scholar
  11. Ascenzi P, Santucci R, Coletta M, Polticelli F (2010) Cytochromes: reactivity of the “dark side” of the heme. Biophys Chem 152:21–27PubMedGoogle Scholar
  12. Ash MR, Guilfoyle A, Clarke RJ, Guss JM, Maher MJ, Jormakka M (2010) Potassium-activated GTPase reaction in the G protein-coupled ferrous iron transporter B. J Biol Chem 285:14594–14602PubMedPubMedCentralGoogle Scholar
  13. Ash MR, Maher MJ, Guss JM, Jormakka M (2011) The initiation of GTP hydrolysis by the G-domain of FeoB: insights from a transition state complex structure. PLoS ONE 6:e23355PubMedPubMedCentralGoogle Scholar
  14. Aurora R, Rose GD (1998) Helix capping. Protein Sci 7:21–38PubMedPubMedCentralGoogle Scholar
  15. Babu YS, Bugg CE, Cook WJ (1988) Structure of calmodulin refined at 2.2 Å resolution. J Biol Chem 204:191–204Google Scholar
  16. Baldwin RL (2007) Energetics of protein folding. J Mol Biol 371:283–301PubMedGoogle Scholar
  17. Banbula A, Potempa J, Travis J, Fernandez-Catalán C, Mann K, Huber R, Bode W, Medrano F (1998) Amino-acid sequence and three-dimensional structure of the Staphylococcus aureus metalloproteinase at 1.72 Å resolution. Structure 6:1185–1193PubMedGoogle Scholar
  18. Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P (2010) Affinity gradients drive copper to cellular destinations. Nature 465:645–648PubMedGoogle Scholar
  19. Barford D, Johnson LN (1989) The allosteric transition of glycogen phosphorylase. Nature 340:609–616PubMedGoogle Scholar
  20. Bastug T, Heinzelmann G, Kuyucak S, Salim M, Vandenberg RJ, Ryan RM (2012) Position of the third Na+ site in the aspartate transporter GltPh and the human glutamate transporter, EAAT1. PLoS ONE 7:e33058PubMedPubMedCentralGoogle Scholar
  21. Benner SA, Cohen MA, Gonnet GH (1993) Empirical and structural models for insertions and deletions in the divergent evolution of proteins. J Mol Biol 229:1065–1082PubMedGoogle Scholar
  22. Blow DM, Birktoft JJ, Hartley BS (1969) Role of a buried acid group in the mechanism of action of chymotrypsin. Nature 221:337–340PubMedGoogle Scholar
  23. Boal AK, Rosenzweig AC (2009) Structural biology of copper trafficking. Chem Rev 109:4760–4779PubMedPubMedCentralGoogle Scholar
  24. Bobofchak KM, Pineda AO, Mathews FS, Di Cera E (2005) Energetic and structural consequences of perturbing Gly-193 in the oxyanion hole of serine proteases. J Biol Chem 280:25644–25650PubMedGoogle Scholar
  25. Bocharov EV, Mayzel ML, Volynsky PE, Mineev KS, Tkach EN, Ermolyuk YS, Schulga AA, Efremov RG, Arseniev AS (2010) Left-handed dimer of EphA2 transmembrane domain: helix packing diversity among receptor tyrosine kinases. Biophys J 98:881–889PubMedPubMedCentralGoogle Scholar
  26. Bocharov EV, Mineev KS, Goncharuk MV, Arseniev AS (2012) Structural and thermodynamic insight into the process of “weak” dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim Biophys Acta 1818:2158–2170PubMedGoogle Scholar
  27. Braun P, von Heijne G (1999) The aromatic residues Trp and Phe have different effects on the positioning of a transmembrane helix in the microsomal membrane. Biochemistry 38:9778–9782PubMedGoogle Scholar
  28. Brieba LG, Sousa R (2000) Roles of histidine 784 and tyrosine 639 in ribose discrimination by T7 RNA polymerase. Biochemistry 39:919–923PubMedGoogle Scholar
  29. Brooks DJ, Fresco JR (2002) Increased frequency of cysteine, tyrosine, and phenylalanine residues since the last universal ancestor. Mol Cell Proteomics 1:125–131PubMedGoogle Scholar
  30. Brosig B, Langosch D (1998) The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci 7:1052–1056PubMedPubMedCentralGoogle Scholar
  31. Buhrman G, Holzapfel G, Fetics S, Mattos C (2010) Allosteric modulation of Ras positions Q61 for a direct role in catalysis. Proc Natl Acad Sci USA 107:4931–4936PubMedGoogle Scholar
  32. Buis JM, Broderick JB (2005) Pyruvate formate-lyase activating enzyme: elucidation of a novel mechanism for glycyl radical formation. Arch Biochem Biophys 433:288–296PubMedGoogle Scholar
  33. Bujacz G, Jaskolski M, Alexandratos J, Wlodawer A, Merkel G, Katz RA, Shalka AM (1996) The catalytic domain of avian sarcoma virus integrase: conformation of the active-site residues in the presence of different cations. Structure 4:89–96PubMedGoogle Scholar
  34. Bulaj G, Kortemme T, Goldenberg DP (1998) Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry 37:8965–8972PubMedGoogle Scholar
  35. Burley SK, Petsko GA (1985) Aromatic–aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28PubMedGoogle Scholar
  36. Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–210PubMedGoogle Scholar
  37. Bywater RP, Thomas D, Vriend G (2001) A sequence and structural study of transmembrane helices. J Comput Aided Mol Des 15:533–552PubMedGoogle Scholar
  38. Caesar CE, Esbjörner EK, Lincoln P, Nordén B (2006) Membrane interactions of cell-penetrating peptides probed by tryptophan fluorescence and dichroism techniques: correlations of structure to cellular uptake. Biochemistry 45:7682–7692PubMedGoogle Scholar
  39. Calvin K, Xue S, Ellis C, Mitchell MH, Li H (2008) Probing the catalytic triad of an archaeal RNA splicing endonuclease. Biochemistry 47:13659–13665PubMedPubMedCentralGoogle Scholar
  40. Carmel AB, Matthews BW (2004) Crystal structure of the BstDEAD N-terminal domain: a novel DEAD protein from Bacillus stearothermophilus. RNA 10:66–74PubMedPubMedCentralGoogle Scholar
  41. Carter CW, Duax WL (2002) Did tRNA synthetase classes arise on opposite strands of the same gene? Mol Cell 10:705–708PubMedGoogle Scholar
  42. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo—transport of ferrous iron into bacteria. Biometals 19:145–157Google Scholar
  43. Cashin AL, Torrice MM, McMenimen KA, Lester HA, Dougherty DA (2007) Chemical-scale studies on the role of a conserved aspartate in preorganizing the agonist binding site of the nicotinic acetylcholine receptor. Biochemistry 46:630–639PubMedPubMedCentralGoogle Scholar
  44. Cavalier-Smith T (2001) Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis. J Mol Evol 53:555–595PubMedGoogle Scholar
  45. Chakrabarti P (1993) Anion binding sites in protein structures. J Mol Biol 234:463–482PubMedGoogle Scholar
  46. Chakraborty R, Pydi SP, Gleim S, Dakshinamurti S, Hwa J, Chelikani P (2012) Site-directed mutations and the polymorphic variant Ala160Thr in the human thromboxane receptor uncover a structural role for transmembrane helix 4. PLoS ONE 7:e29996PubMedPubMedCentralGoogle Scholar
  47. Chandra BR, Yogavel M, Sharma A (2007) Structural analysis of ABC-family periplasmic zinc binding protein provides new insights into mechanism of ligand uptake and release. J Mol Biol 367:970–982PubMedPubMedCentralGoogle Scholar
  48. Chapman HA, Riese RJ, Shi GP (1997) Emerging roles for cysteine proteases in human biology. Annu Rev Physiol 59:63–88PubMedGoogle Scholar
  49. Charlier HA, Runquist JA, Miziorko HM (1994) Evidence supporting catalytic roles for aspartate residues in phosphoribulokinase. Biochemistry 33:9343–9350PubMedGoogle Scholar
  50. Cheetham GMT, Steitz TA (1999) Structure of a transcribing T7 RNA polymerase initiation complex. Science 286:2305–2309PubMedGoogle Scholar
  51. Chen J, Stites WE (2001) Packing is a key selection factor in the evolution of protein hydrophobic cores. Biochemistry 40:15280–15289PubMedGoogle Scholar
  52. Chen J, Lu Z, Sakon J, Stites WE (2004) Proteins with simplified hydrophobic cores compared to other packing mutants. Biophys Chem 110:239–248PubMedGoogle Scholar
  53. Chen C, Saxena AK, Simcoke WN, Garboczi DN, Pedersen PL, Ko YH (2006) Mitochondrial ATP synthase. Crystal structure of the catalytic F1 unit in a vanadate-induced transition-like state and implications for mechanism. J Biol Chem 281:13777–13783PubMedGoogle Scholar
  54. Chevalier BS, Monnat RJ Jr, Stoddard BL (2001) The homing endonuclease I-Cre-I uses three metals, one of which is shared between two active sites. Nat Struct Biol 8:312–316PubMedGoogle Scholar
  55. Chivers PT, Prehoda KE, Raines RT (1997) The CXXC motif: a rheostat in the active site. Biochemistry 36:4061–4066PubMedGoogle Scholar
  56. Cho HS, Pelton JG, Yan D, Kustu S, Wemmer DE (2001) Phosphoaspartates in bacterial signal transduction. Curr Opin Struct Biol 11:679–684PubMedGoogle Scholar
  57. Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain. Science 309:581–585PubMedGoogle Scholar
  58. Chothia C, Gough J, Vogel C, Teichmann SA (2003) Evolution of the protein repertoire. Science 300:1701–1703PubMedGoogle Scholar
  59. Chou PY, Fasman GD (1978) Empirical predictions of protein conformation. Annu Rev Biochem 47:251–276PubMedGoogle Scholar
  60. Cobessi D, Tête-Favier F, Marchal S, Branlant G, Aubry A (2000) Structural and biochemical investigations of the catalytic mechanism of an NADP-dependent aldehyde dehydrogenase from Streptococcus mutans. J Mol Biol 300:141–152PubMedGoogle Scholar
  61. Coleman PM, Freeman HC, Guss JM, Murata M, Norris VA, Ramshaw JAM, Venkatappa MP (1978) X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature 272:319–324Google Scholar
  62. Coleman DE, Berghuis AM, Lee E, Linder ME, Gilman AG, Sprang SR (1994) Structures of active conformations of Giα1 and the mechanism of GTP hydrolysis. Science 265:1405–1412PubMedGoogle Scholar
  63. Copley RR, Barton GJ (1994) A structural analysis of phosphate and sulfate binding sites in proteins. Estimation of the propensities for binding and conservation of phosphate binding sites. J Mol Biol 242:321–329PubMedGoogle Scholar
  64. Cordes FS, Bright JN, Sansom MS (2002) Proline-induced distortions in transmembrane helices. J Mol Biol 323:951–960PubMedGoogle Scholar
  65. Crick FHC (1968) The origin of the genetic code. J Mol Biol 38:367–379PubMedGoogle Scholar
  66. Crick FHC, Brenner S, Klug A, Pieczenik G (1976) A speculation on the origin of protein synthesis. Orig Life 7:389–397Google Scholar
  67. Cunningham F, Poulsen BE, Ip W, Deber CM (2011) Beta-branched residues adjacent to GG4 motifs promote the efficient association of glycophorin A transmembrane helices. Biopolymers 96:340–347PubMedGoogle Scholar
  68. Dale T, Fahlman RP, Olejniczak M, Uhlenbeck OC (2009) Specificity of the ribosomal A site for aminoacyl-tRNAs. Nucleic Acids Res 37:1202–1210PubMedPubMedCentralGoogle Scholar
  69. Dang S, Sun L, Huang Y, Lu F, Liu Y, Gong H, Wang J, Yan N (2010) Structure of a fucose transporter in an outward-open conformation. Nature 467:734–738PubMedGoogle Scholar
  70. Davis BK (1999) Evolution of the genetic code. Prog Biophys Mol Biol 72:157–243PubMedGoogle Scholar
  71. Demmers JA, Haverkamp J, Heck AJ, Koeppe RE 2nd, Killian JA (2000) Electrospray ionization mass spectrometry as a tool to analyze hydrogen/deuterium exchange kinetics of transmembrane peptides in lipid bilayers. Proc Natl Acad Sci USA 97:3189–3194PubMedGoogle Scholar
  72. Di Cera E (2006) A structural perspective on enzymes activated by monovalent cations. J Biol Chem 281:1305–1308PubMedGoogle Scholar
  73. Di Giulio M (2001) A blind empiricism against the coevolution theory of the origin of the genetic code. J Mol Evol 53:724–732PubMedGoogle Scholar
  74. Dieci G, Hermann-Le Denmat S, Lukhtanov E, Thuriaux P, Werner M, Sentenac A (1995) A universally conserved region of the largest subunit participates in the active site of RNA polymerase III. EMBO J 14:3766–3776PubMedPubMedCentralGoogle Scholar
  75. Dill KA (1990) Dominant forces in protein folding. Biochemistry 29:7133–7155PubMedGoogle Scholar
  76. Dilworth D, Gudavicius G, Leung A, Nelson CJ (2012) The roles of peptidyl-proline isomerases in gene regulation. Biochem Cell Biol 90:55–69PubMedGoogle Scholar
  77. Ding S, Ingleby L, Ahern CA, Horn R (2005) Investigating the putative hinge in Shaker potassium channel. J Gen Physiol 126:213–226PubMedPubMedCentralGoogle Scholar
  78. Doig AJ (2002) Recent advances in helix–coil theory. Biophys Chem 101–102:281–293PubMedGoogle Scholar
  79. Donald JE, Kulp DW, DeGrado WF (2011) Salt bridges: geometrically specific, designable interactions. Proteins 79:898–915PubMedPubMedCentralGoogle Scholar
  80. Doublié S, Tabor S, Long AM, Richardson CC, Ellenberger T (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391:251–258PubMedGoogle Scholar
  81. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Nature 280:69–77Google Scholar
  82. Drawz SM, Bethel CR, Hujer KM, Hurless KN, Distler AM, Caselli E, Prati F, Bonomo RA (2009) The role of a second-shell residue in modifying substrate and inhibitor interactions in the SHV β-lactamase: a study of ambler position Asn276. Biochemistry 48:4557–4566PubMedPubMedCentralGoogle Scholar
  83. Dreusicke D, Schulz GE (1986) The glycine-rich loop of adenylate kinase forms a giant anion hole. FEBS Lett 208:301–304PubMedGoogle Scholar
  84. Dutzler R (2004) The structural basis of ClC chloride channel function. Trends Neurosci 27:315–320PubMedGoogle Scholar
  85. Dutzler R, Campbell EB, MacKinnon R (2003) Gating the selectivity filter in ClC chloride channels. Science 300:108–112PubMedGoogle Scholar
  86. Eigen M, Schuster P (1978) The hypercycle. A principle of natural self-organization. Part C: the realistic hypercycle. Naturwissenschaften 65:341–369Google Scholar
  87. Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:217–228PubMedGoogle Scholar
  88. Eitinger T, Mandrand-Berthelot M-A (2000) Nickel transport systems in microorganisms. Arch Microbiol 173:1–9PubMedGoogle Scholar
  89. Epand RM, Epand RF, Martin I, Ruysschaert J-M (2001) Membrane interactions of mutated forms of the influenza fusion peptide. Biochemistry 40:8800–8807PubMedGoogle Scholar
  90. Eshaghi S, Niegowski D, Kohl A, Martinez Molina D, Lesley SA, Nordlund P (2006) Crystal structure of a divalent metal ion transporter CorA at 2.9 angstrom resolution. Science 313:354–357PubMedGoogle Scholar
  91. Estabrook RA, Lipson R, Hopkins B, Reich N (2004) The coupling of tight DNA binding and base flipping: identification of a conserved structural motif in base flipping enzymes. J Biol Chem 279:31419–31428PubMedGoogle Scholar
  92. Feng L, Campbell EB, Hsiung Y, MacKinnon R (2010) Structure of a eukaryotic CLC transporter defines an intermediate state in the transport cycle. Science 330:635–641PubMedPubMedCentralGoogle Scholar
  93. Fersht AR, Shi J-P, Knill-Jones J, Lowe DM, Wilkinson AJ, Blow DM, Brick P, Carter P, Waye MMY, Winter G (1985) Hydrogen bonding and biological specificity analyzed by protein engineering. Nature 314:235–238PubMedGoogle Scholar
  94. Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21:R877–R883PubMedPubMedCentralGoogle Scholar
  95. Fillingame RH, Angevine CM, Dimitriev OY (2002) Coupling proton movements to c-ring rotation in F1F0 ATP synthase: aqueous access channels and helix rotations at the a–c interface. Biochim Biophys Acta 1555:29–36PubMedGoogle Scholar
  96. Finer-Moore JS, Liu L, Schafmeister CE, Birdsall DL, Mau T, Santi DV, Stroud RM (1996) Partitioning roles of side chains in affinity, orientation, and catalysis with structures for mutant complexes: asparagine-229 in thymidylate synthase. Biochemistry 35:5125–5136PubMedGoogle Scholar
  97. Fleming KG, Engelman DM (2001) Specificity in transmembrane helix–helix interactions can define a hierarchy of stability for sequence variants. Proc Natl Acad Sci USA 98:14380–14384Google Scholar
  98. Flemming D, Hellwig P, Friedrich T (2003) Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase. J Biol Chem 278:3055–3062PubMedGoogle Scholar
  99. Francis BR (2011) An alternative to the RNA world hypothesis. Trends Evol Biol 3:e2Google Scholar
  100. Frazão C, McVey CE, Amblar M, Barbas A, Vonrhein C, Arraiano CM (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443:110–114PubMedGoogle Scholar
  101. Freeland SJ, Hurst LD (1998) The genetic code is one in a million. J Mol Evol 47:238–248PubMedPubMedCentralGoogle Scholar
  102. Fukunaga R, Fukai S, Ishitani R, Nureki O, Yokoyama S (2004) Crystal structures of the CPI domain from Thermus thermophilus isoleucyl-tRNA synthetase and its complex with l-valine. J Biol Chem 279:8396–8402PubMedGoogle Scholar
  103. Galili L, Rothman A, Kozachkov L, Rimon A, Padan E (2002) Trans membrane domain IV is involved in ion transport activity and pH regulation of the NhaA-Na+/H+ antiporter of Escherichia coli. Biochemistry 41:609–617PubMedGoogle Scholar
  104. Gao X, Lu F, Zhou L, Dang S, Sun L, Li X, Wang J, Shi Y (2009) Structure and mechanism of an amino acid antiporter. Science 324:1565–1568PubMedGoogle Scholar
  105. Gastinel LN, Cambillau C, Bourne Y (1999) Crystal structures of the bovine β4galactosyltransferase catalytic domain and its complex with uridine diphosphogalactose. EMBO J 18:3546–3557PubMedPubMedCentralGoogle Scholar
  106. Gifford JL, Walsh MP, Vogel HJ (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405:199–221PubMedGoogle Scholar
  107. Giles NM, Watts AB, Giles GI, Fry FH, Littlechild JA, Jacob C (2003) Metal and redox modulation of cysteine protein function. Chem Biol 10:677–693PubMedGoogle Scholar
  108. Glusker JP (1991) Structural aspects of metal liganding to functional groups in proteins. Adv Protein Chem 42:1–76PubMedGoogle Scholar
  109. Gourdon P, Liu X-Y, Skjorringe T, Morth JP, Møller LB, Pedersen BP (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–65PubMedGoogle Scholar
  110. Greenwald J, Butler SL, Bushman FD, Choe S (1999) The mobility of an HIV-1 integrase active site loop is correlated with catalytic activity. Biochemistry 38:8892–8898PubMedGoogle Scholar
  111. Grosjean H, de Crécy-Lagard V, Marck C (2010) Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett 584:252–264PubMedGoogle Scholar
  112. Guo M, Chong YE, Beebe K, Shapiro R, Yang XL, Schimmel P (2009) The C-Ala domain brings together editing and aminoacylation functions on one tRNA. Science 325:744–747PubMedPubMedCentralGoogle Scholar
  113. Harding MM (2004) The architecture of metal coordination groups in proteins. Acta Crystallogr D 60:849–859PubMedGoogle Scholar
  114. Hardman RM, Stansfeld PJ, Dalibalta S, Sutcliffe MJ, Mitcheson JS (2007) Activation gating of hERG potassium channels: S6 glycines are not required as gating hinges. J Biol Chem 282:31972–31981PubMedGoogle Scholar
  115. Harris TK, Turner GJ (2002) Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life 53:85–98PubMedGoogle Scholar
  116. Hattori M, Iwase N, Furuya N, Tanaka Y, Tsukazaki T, Ishitani R, Maguire ME, Ito K, Maturana A, Nureki O (2009) Mg2+-dependent gating of bacterial MgtE channel underlies Mg2+ homoestasis. EMBO J 28:3602–3612PubMedPubMedCentralGoogle Scholar
  117. Heathcote P, Jones MR, Fyfe PK (2003) Type I photosynthetic reaction centres: structure and function. Philos Trans R Soc Lond B 358:231–243Google Scholar
  118. Hellinga HW, Evans PR (1987) Mutations in the active site of Escherichia coli phosphofructokinase. Nature 327:437–439PubMedGoogle Scholar
  119. Herzberg O, James M (1985) Structure of the calcium regulatory muscle protein troponin-C at 2.8 Å resolution. Nature 313:653–659PubMedGoogle Scholar
  120. Higgs PG (2009) A four column theory for the origin of the genetic code: tracing the evolutionary pathways that gave rise to an optimized code. Biol Direct 4:16PubMedPubMedCentralGoogle Scholar
  121. Hirata A, Fujishima K, Yamagami R, Kawamura T, Banfield JF, Kanai A, Hori H (2012) X-ray structure of the fourth type of archaeal tRNA splicing endonuclease: insights into the evolution of a novel three-unit composition and a unique loop involved in broad substrate specificity. Nucleic Acids Res 40:10554–10566PubMedPubMedCentralGoogle Scholar
  122. Hirst J (2010) Towards the molecular mechanism of respiratory complex I. Biochem J 425:327–339Google Scholar
  123. Holden HM, Benning MM, Haller T, Gerlt JA (2001) The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme A thioesters. Acc Chem Res 34:145–157PubMedGoogle Scholar
  124. Holder JB, Bennett AF, Chen J, Spencer DS, Byrne MP, Stites WE (2001) Energetics of side chain packing in staphylococcal nuclease assessed by exchange of valines, isoleucines, and leucines. Biochemistry 40:13998–14003PubMedGoogle Scholar
  125. Holliday GL, Mitchell JB, Thornton JM (2009) Understanding the functional roles of amino acid residues in enzyme catalysis. J Mol Biol 390:560–577PubMedGoogle Scholar
  126. Houk KN, Lee JK, Tantillo DJ, Bahmanyar S, Hietbrink BN (2001) Crystal structures of orotidine monophosphate decarboxylase: does the structure reveal the mechanism of nature’s most proficient enzyme? ChemBioChem 2:113–118PubMedGoogle Scholar
  127. Howard BR, Endrizzi JA, Remington SJ (2000) Crystal structure of Escherichia coli malate synthase G complexed with magnesium and glyoxylate at 2.0Å resolution: mechanistic implications. Biochemistry 39:3156–3168PubMedGoogle Scholar
  128. Huang H, Chopra R, Verdine Gl, Harrison SC (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282:1669–1675PubMedGoogle Scholar
  129. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929–940PubMedGoogle Scholar
  130. Hunte C, Screpanti E, Venturi M, Padan E, Michel H (2005) Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435:1197–1202PubMedGoogle Scholar
  131. Iiams V, Desai BJ, Fedorov AA, Federov EV, Almo SC, Gerlt JA (2011) Mechanism of the orotidine-5′-monophosphate decarboxylase-catalyzed reaction: importance of residues in the orotate binding site. Biochemistry 50:8497–8507PubMedPubMedCentralGoogle Scholar
  132. Ikehara K (2002) Origins of gene, genetic code, protein and life: comprehensive view of life systems from a GNC–SNS primitive genetic code hypothesis. J Biosci 27:165–186Google Scholar
  133. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S, Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281:64–71PubMedGoogle Scholar
  134. Jayaram H, Accardi A, Wu F, Williams C, Miller C (2008) Ion permeation through a Cl-selective channel designed from a CLC Cl−/H+ exchanger. Proc Natl Acad Sci USA 105:11194–11199PubMedGoogle Scholar
  135. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) The open pore conformation of potassium channels. Nature 417:523–526PubMedGoogle Scholar
  136. Jiang J, Nadas IA, Kim MA, Franz KJ (2005) A Mets motif peptide found in copper transport proteins selectively binds Cu(I) with methionine-only coordination. Inorg Chem 44:9787–9794PubMedGoogle Scholar
  137. Jimenez-Sanchez A (1995) On the origin and evolution of the genetic code. J Mol Evol 41:712–716PubMedGoogle Scholar
  138. Jin T, Peng L, Mirshahi T, Rohacs T, Chan KW, Sanchez R, Logothetis E (2002) The βγ subunits of G proteins gate a K+ channel by pivoted bending of a transmembrane segment. Mol Cell 10:469–481PubMedGoogle Scholar
  139. Jordan SR, Pabo CO (1988) Structure of the lambda complex at 2.5Å resolution: details of the repressor–operator interactions. Science 242:893–899PubMedGoogle Scholar
  140. Joseph-McCarthy D, Rost LE, Komives EA, Petsko GA (1994) Crystal structure of the mutant yeast triosephosphate isomerase in which the catalytic base glutamic acid 165 is changed to aspartic acid. Biochemistry 33:2824–2829PubMedGoogle Scholar
  141. Karsten E, Chooback L, Liu D, Hwang CC, Lynch C, Cook PF (1999) Mapping the active site topography of the NAD-malic enzyme via alanine-scanning site-directed mutagenesis. Biochemistry 38:10527–10532PubMedGoogle Scholar
  142. Kaushik N, Singh K, Alluru I, Modak MJ (1999) Tyrosine 222, a member of the YXDD motif of MuLV RT, is catalytically essential and is a major component of the fidelity center. Biochemistry 38:2617–2627PubMedGoogle Scholar
  143. Kieseritzky G, Knapp E-W (2011) Charge transport in the ClC-type chloride-proton anti-porter from Escherichia coli. J Biol Chem 286:2976–2986PubMedGoogle Scholar
  144. Killian JA, von Heijne G (2000) How proteins adapt to a membrane–water interface. Trends Biochem Sci 25:429–434PubMedGoogle Scholar
  145. Kim EE, Wyckoff HW (1991) Reaction mechanism of alkaline phosphatase based on crystal structures. Two metal ion catalysis. J Mol Biol 218:449–464PubMedGoogle Scholar
  146. Kim Y, Geiger JH, Hahn S, Sigler PB (1993a) Crystal structure of a yeast TBP/TATA-box complex. Nature 365:512–520PubMedGoogle Scholar
  147. Kim JL, Nikolov DB, Burley SK (1993b) Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 365:520–527PubMedGoogle Scholar
  148. Klieger G, Grothe R, Mallick P, Eisenberg D (2002) GXXXG and AXXXA: common α-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41:5990–5997Google Scholar
  149. Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 308:267–269PubMedGoogle Scholar
  150. Knight RD, Freeland SJ, Landweber LF (1999) Selection, history and chemistry: the three faces of the genetic code. Trends Biochem Sci 24:241–247PubMedGoogle Scholar
  151. Knoop V, Groth-Malonek M, Gebert M, Eifler K, Weyand K (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Gen Genomics 274:205–216Google Scholar
  152. Knowles JR (1991) Enzyme catalysis: not different, just better. Nature 350:121–124PubMedGoogle Scholar
  153. Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421PubMedGoogle Scholar
  154. Kolberg M, Strand KR, Graff P, Andersson KK (2004) Structure, function, and mechanism of ribonucleotide reductases. Biochim Biophys Acta 1699:1–34PubMedGoogle Scholar
  155. Koshland DE Jr (1976) The evolution of function in enzymes. Fed Proc 35:2104–2111PubMedGoogle Scholar
  156. Krapp S, Münster-Kühnel AK, Kaiser JT, Tiralongo J, Gerardy-Schahn R, Jacob H (2003) The crystal structure of murine CMP-5-N-acetylneuraminic acid synthetase. J Mol Biol 334:625–637PubMedGoogle Scholar
  157. Krishnamurthy H, Gouaux E (2012) X-ray structure of LeuT in substrate-free outward-open and apo inward-open states. Nature 481:469–474PubMedPubMedCentralGoogle Scholar
  158. Kuiper MJ, Davies PL, Walker VK (2001) A theoretical model of a plant antifreeze protein from Lolium perenne. Biophys J 81:3560–3565PubMedPubMedCentralGoogle Scholar
  159. Kuo A, Gulbis JM, Antcliff JF, Rahman T, Lowe ED, Zimmer J, Cuthbertson J, Ashcroft FM, Ezaki T, Doyle DA (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300:1922–1926PubMedGoogle Scholar
  160. Kursula I, Partanen S, Lambier AM, Wierenga RK (2002) The importance of the conserved Arg191-Asp227 salt bridge of triosephosphate isomerase for folding, stability, and catalysis. FEBS Lett 518:39–42PubMedGoogle Scholar
  161. Kurz LC, Nakra T, Stein R, Plungkhen W, Riley M, Hsu F, Drysdale GR (1998) Effects of changes in three catalytic residues on the relative stabilities of some of the intermediates and transition states in the citrate synthase reaction. Biochemistry 37:9724–9737PubMedGoogle Scholar
  162. Landolt-Marticorina C, Williams KA, Deber CM, Reithmeier RA (1993) Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J Mol Biol 229:602–608Google Scholar
  163. Lawrence MC, Pilling PA, Epa VC, Berry AM, Ogunniyi AD, Paton JC (1999) The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6:1553–1561Google Scholar
  164. Ledvina PS, Tsai AL, Wang Z, Koehl E, Quiocho FA (1998) Dominant role of local dipolar interactions in phosphate binding to a receptor cleft with an electronegative charge surface: equilibrium, kinetic, and crystallographic studies. Protein Sci 7:2550–2559PubMedPubMedCentralGoogle Scholar
  165. Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612:1–40PubMedGoogle Scholar
  166. Lee YH, Deka RK, Norgard MV, Radolf JD, Hasemann CA (2002) Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat Struct Biol 6:628–633Google Scholar
  167. Lee HJ, Svahn E, Swanson JMJ, Lepp H, Voth GA, Brzezinski P, Gennis RB (2010) The intricate role of water in proton transport through cytochrome c oxidase. J Am Chem Soc 132:16225–16239PubMedPubMedCentralGoogle Scholar
  168. Lehman N, Jukes TH (1988) Genetic code development by stop codon takeover. J Theor Biol 135:203–214PubMedGoogle Scholar
  169. Lehoux IE, Mitra B (1999) (S)-Mandelate dehydrogenase from Pseudomonas putida: mutations of the catalytic base histidine-274 and chemical rescue of activity. Biochemistry 38:9948–9955PubMedGoogle Scholar
  170. Lei M, Podell ER, Baumann P, Cech TR (2003) DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426:198–203PubMedGoogle Scholar
  171. Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci USA 106:4677–4682PubMedGoogle Scholar
  172. Lewis EB (1951) Pseudoallelism and gene evolution. Cold Spring Harbor Symp Quant Biol 16:159–174PubMedGoogle Scholar
  173. Lewis HA, Musunuru K, Jensen KB, Edo C, Chen H, Darnell RB, Burley SK (2000) Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 100:323–332PubMedGoogle Scholar
  174. Lewis RN, Liu F, Krivanek R, Rybar P, Hianik T, Flach CR, Mendelsohn R, Chen Y, Mant CT, Hodges RS, McElhaney RN (2007) Studies of the minimum hydrophobicity of α-helical peptides required to maintain a stable transmembrane association with phospholipid bilayer membranes. Biochemistry 46:1042–1054PubMedPubMedCentralGoogle Scholar
  175. Li L, Cook PF (2006) The 2′-phosphate of NADP is responsible for proper orientation of the nicotinamide ring in the oxidative decarboxylation reaction catalyzed by sheep liver 6-phosphogluconate dehydrogenase. J Biol Chem 281:36803–36810PubMedGoogle Scholar
  176. Li de la Sierra-Gallay I, Pellegrini O, Condon C (2005) Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z. Nature 433:657–661PubMedGoogle Scholar
  177. Lin J, Abeygunawardana C, Frick DN, Bessman MJ, Mildvan AS (1997) Solution structure of the quaternary MutT-M2+-AMPCPP-M2+ complex and mechanism of its pyrophosphohydrolase action. Biochemistry 36:1199–1211PubMedGoogle Scholar
  178. Linder P, Jankowsky E (2011) From unwinding to clamping—the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12:505–516PubMedGoogle Scholar
  179. Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20PubMedGoogle Scholar
  180. Liu L-P, Deber CM (1998) Uncoupling hydrophobicity and helicity in transmembrane segments. α-helical propensities of the amino acids in non-polar environments. J Biol Chem 273:23645–23648PubMedGoogle Scholar
  181. Long M (2000) A new function evolved from gene fusion. Genome Res 10:1743–1756Google Scholar
  182. Long F, Su CC, Zimmermann MT, Boyken SE, Rajashankar KR, Jernigan RL, Yu EW (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467:484–488PubMedPubMedCentralGoogle Scholar
  183. Lu H, Marti T, Booth PJ (2001) Proline residues in transmembrane α helices affect the folding of bacteriorhodopsin. J Mol Biol 308:437–446PubMedGoogle Scholar
  184. Lu KP, Finn G, Lee TH, Nicholson LK (2007) Prolyl cistrans isomerization as a molecular timer. Nat Chem Biol 3:619–629PubMedGoogle Scholar
  185. Luecke H, Quiocho FA (1990) High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347:402–406PubMedGoogle Scholar
  186. Lunin VV, Dobrovetsky E, Khutoreskaya G, Zhang R, Joachimiak A, Doyle DA, Bochkarev A, Maguire ME, Edwards AM, Koth CM (2006) Crystal structure of the CorA Mg2+ transporter. Nature 440:833–837PubMedGoogle Scholar
  187. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155PubMedGoogle Scholar
  188. MacArthur MW, Thornton JM (1991) Influence of proline residues on protein conformation. J Mol Biol 218:397–412PubMedGoogle Scholar
  189. MacKenzie KR, Prestegard JH, Engelman DM (1997) A transmembrane helix dimer: structure and implications. Science 276:131–133PubMedGoogle Scholar
  190. MacKinnon R (2003) Potassium channels. FEBS Lett 555:62–65PubMedGoogle Scholar
  191. Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98PubMedGoogle Scholar
  192. Marshall NM, Garner DK, Wilson TD, Gao YG, Robinson H, Nilges MJ, Li Y (2009) Rationally tuning the reduction potential of a single cupredoxin beyond the natural range. Nature 462:113–116PubMedPubMedCentralGoogle Scholar
  193. Martin JL (1995) Thioredoxin—a fold for all reasons. Structure 3:245–250PubMedGoogle Scholar
  194. Massey SE (2006) A sequential “2-1-3” model of genetic code evolution that explains codon restraints. J Mol Evol 62:809–810PubMedGoogle Scholar
  195. Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662PubMedGoogle Scholar
  196. Meinhart A, Cramer P (2004) Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA processing factors. Nature 430:223–226PubMedGoogle Scholar
  197. Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164PubMedGoogle Scholar
  198. Meyer E, Cole G, Radhakrishnan R (1988) Structure of native pancreatic elastase at 1.65 Å resolution. Acta Cryst B44:26–38Google Scholar
  199. Milburn MV, Tong L, deVos AM, Brünger A, Yamaizumi Z, Nishimura S, Kim SH (1990) Molecular switch for signal transduction: structural differences between active and inactive forms of protooncogenic ras proteins. Science 247:939–945PubMedGoogle Scholar
  200. Miller C, Nguitragool W (2009) A provisional transport mechanism for a chloride channel-type Cl/H+ exchanger. Philos Trans R Soc Lond B 364:175–180Google Scholar
  201. Mineev KS, Bocharov EV, Pustovalova YE, Bocharova OV, Chupin VV, Arseniev AS (2010) Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases. J Mol Biol 400:231–243PubMedGoogle Scholar
  202. Mitome N, Ono S, Sato H, Susuki T, Sone N, Yoshida M (2010) Essential arginine residue of the Fo-a subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the Fo proton channel. Biochem J 430:171–177PubMedGoogle Scholar
  203. Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949–955PubMedGoogle Scholar
  204. Modis Y, Filppula SA, Novikov DK, Norledge B, Hiltunen JK, Wierenga RK (1998) The crystal structure of dienoyl-CoA isomerase at 1.5Å resolution reveals the importance of aspartate and glutamate sidechains for catalysis. Structure 6:957–970PubMedGoogle Scholar
  205. Mok YK, Elisseeva EL, Davidson AR, Forman-Kay JD (2001) Dramatic stabilization of an SH3 domain by a single substitution: roles of the folded and unfolded states. J Mol Biol 307:913–928PubMedGoogle Scholar
  206. Monod J (1971) Chance and Necessity. A. A. Knopf, Inc., New York p143Google Scholar
  207. Morth JP, Pedersen BP, Buch-Pedersen MJ, Andersen JP, Vilsen B, Palmgren MG, Nissen P (2011) A structural overview of the plasma membrane Na+, K+-ATPase and H+-ATPase ion pumps. Nat Rev Mol Cell Biol 12:60–70PubMedGoogle Scholar
  208. Mueller-Cajar O, Stotz M, Wendler P, Hartl FU, Bracher A, Hayer-Hartl M (2011) Structure and function of the AAA+ protein CbbX, a red-type rubisco activase. Nature 479:194–199PubMedGoogle Scholar
  209. Muller CW, Schulz GE (1992) Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor Ap5A refined at 1.9 Å resolution. A model for a catalytic transition state. J Mol Biol 224:159–177PubMedGoogle Scholar
  210. Murata T, Yamato I, Kakinuma Y, Leslie AGW, Walker JE (2005) Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae. Science 308:654–659PubMedGoogle Scholar
  211. Neagoe I, Stauber T, Fidzinski P, Bergsdorf EY, Jentsch TJ (2010) The late endosomal ClC-6 mediates proton/chloride countertransport in heterologous plasma membrane expression. J Biol Chem 285:21689–21697PubMedPubMedCentralGoogle Scholar
  212. Nevskaya N, Tishchenko S, Volchkov S, Kljashtorny V, Nikonova E, Nikonov O, Nikulin A, Köhrer C, Piendl W, Zimmermann R, Stockley P, Garber M, Nikonov S (2006) New insights into the interaction of ribosomal protein L1 with RNA. J Mol Biol 355:747–759PubMedGoogle Scholar
  213. Nguyen HD, Marchut AJ, Hall CK (2004) Solvent effects on the conformational transition of a model polyalanine peptide. Protein Sci 13:2909–2924PubMedPubMedCentralGoogle Scholar
  214. Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Restetnikova L, Clark BF, Nyborg J (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EFTu, and a GTP analog. Science 270:1464–1472PubMedGoogle Scholar
  215. Nordin N, Guskov A, Phua T, Sahaf N, Xia Y, Lu S, Eshaghi H, Eshaghi S (2013) Exploring the structure and function of Thermotoga maritima CorA reveals the mechanism of gating and ion selectivity in Co2+/Mg2+ transport. Biochem J. doi: 10.1042/BJ20121745 PubMedPubMedCentralGoogle Scholar
  216. O’Neal CJ, Jobling MG, Holmes RK, Hol WGJ (2005) Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309:1093–1096PubMedGoogle Scholar
  217. Obungu VH, Wang Y, Amyot SM, Gocke CB, Beattie DS (2000) Mutations in the tether region of the iron–sulfur protein affect the activity and assembly of the cytochrome bc1 complex of yeast mitochondria. Biochim Biophys Acta 1457:36–44PubMedGoogle Scholar
  218. Ohno S (1970) Evolution by gene duplication. Springer, HeidelbergGoogle Scholar
  219. Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC (2005) Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat Struct Mol Biol 12:788–793PubMedGoogle Scholar
  220. Ordentlich A, Barak D, Kronman C, Ariel N, Segall Y, Velan B, Shafferman A (1998) Functional characteristics of the oxyanion hole in human acetylcholinesterase. J Biol Chem 273:19509–19517PubMedGoogle Scholar
  221. Orgel LE (1987) Evolution of the genetic apparatus. Cold Spring Harb Symp Quant Biol 52:9–16PubMedGoogle Scholar
  222. Ose T, Kuoki K, Matsushima M, Maenaka K, Kumagai I (2009) Importance of the hydrogen bonding network including Asp52 for catalysis, as revealed by Asn59 mutant hen egg-white lysozymes. J Biochem 146:651–657PubMedGoogle Scholar
  223. Otto SP, Yong P (2002) The evolution of gene duplicates. Adv Genetics 46:451–483Google Scholar
  224. Pace CN, Scholtz JM (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys J 75:422–427PubMedPubMedCentralGoogle Scholar
  225. Paddock ML, Feher G, Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555:45–50PubMedGoogle Scholar
  226. Page M, Di Cera E (2006) Role of Na+ and K+ in enzyme function. Physiol Rev 86:1049–1092PubMedGoogle Scholar
  227. Pal D, Chakrabarti P (1998) Different types of interactions involving cysteine sulfhydryl group in proteins. J Biomol Struct Dyn 15:1059–1072PubMedGoogle Scholar
  228. Pannifer AD, Flint AJ, Tonks NK, Barford D (1998) Visualization of the cysteinyl-phosphate intermediate of a protein-tyrosine phosphatase by X-ray crystallography. J Biol Chem 273:10454–10462PubMedGoogle Scholar
  229. Park IS, Michel LO, Pearson MA, Jabri E, Karplus PA, Wang S, Dong J, Scott RA, Koehler BP, Johnson MK, Hausinger RP (1996) Characterization of the mononickel metallocenter in H134A mutant urease. J Biol Chem 271:18632–18637PubMedGoogle Scholar
  230. Pascarella S, Argos P (1992) Analysis of insertions and deletions in protein structures. J Mol Biol 224:461–471PubMedGoogle Scholar
  231. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353–358PubMedPubMedCentralGoogle Scholar
  232. Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane pump. Nature 450:1111–1114PubMedGoogle Scholar
  233. Pei XY, Titman CM, Frank RA, Leeper FJ, Luisi BF (2008) Snapshots of catalysis in the E1 subunit of the pyruvate dehydrogenase multienzyme complex. Structure 16:1860–1872PubMedPubMedCentralGoogle Scholar
  234. Pejchal R, Ludwig ML (2004) Cobalamin-independent methionine synthase (MetE): a face-to-face double barrel that evolved by gene duplication. PLoS Biol 3:e31PubMedPubMedCentralGoogle Scholar
  235. Perham RN (1991) Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein. Biochemistry 30:8501–8512PubMedGoogle Scholar
  236. Pomowski A, Zumft WG, Kroneck PM, Einsle O (2011) N2O binding at a [4Cu:2S] copper–sulfur cluster in nitrous oxide reductase. Nature 477:234–237PubMedGoogle Scholar
  237. Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3:827–837PubMedGoogle Scholar
  238. Puig S, Lee J, Lau M, Thiele DJ (2002) Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem 277:26021–26030PubMedGoogle Scholar
  239. Purohit P, Auerbach A (2011) Glycine hinges with opposing actions at the acetylcholine receptor-channel transmitter binding site. Mol Pharmacol 79:351–359PubMedPubMedCentralGoogle Scholar
  240. Radford SE, Laue ED, Perham RN, Martin SR, Appella E (1989) Conformational flexibility and folding of synthetic peptides representing an interdomain segment of polypeptide chain in the pyruvate dehydrogenase multienzyme complex of Escherichia coli. J Biol Chem 264:767–775PubMedGoogle Scholar
  241. Richardson JS, Richardson DC (1989) Principles and patterns of protein conformation. In: Fasman GD (ed) Prediction of protein structure and the principles of protein conformation. Plenum Press, New York, pp 1–98Google Scholar
  242. Rigoutsos I, Riek P, Graham RM, Novotny J (2003) Structural details (kinks and non-α conformations) in transmembrane helices are intrahelically determined and can be predicted by sequence pattern descriptors. Nucleic Acids Res 31:4625–4631PubMedPubMedCentralGoogle Scholar
  243. Riordan JF (1979) Arginyl residues and anion binding sites in proteins. Mol Cell Biochem 26:71–90PubMedGoogle Scholar
  244. Rodin S, Ohno S (1995) Two types of aminoacyl tRNA synthetases could be originally encoded by complementary strands of nucleic acids. Orig Life Evol Biosphere 25:565–589Google Scholar
  245. Rossman MG, Moras D, Olson KW (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature 250:194–199Google Scholar
  246. Runquist JA, Rios SE, Vinarov DA, Miziorko HM (2001) Functional evaluation of serine/threonine residues in the P-loop of Rhodobacter sphaeroides phosphoribulokinase. Biochemistry 40:14530–14537PubMedGoogle Scholar
  247. Russ WP, Engelman DM (2000) The GxxxG motif: a framework for transmembrane helix–helix association. J Mol Biol 296:911–919PubMedGoogle Scholar
  248. Sankararamakrishnan R, Weinstein H (2000) Molecular dynamics simulations predict a tilted orientation for the helical region of dynorphin A(1–17) in dimyristoylphosphatidylcholine bilayers. Biophys J 79:2331–2344PubMedPubMedCentralGoogle Scholar
  249. Sansom MSP, Weinstein H (2000) Hinges, swivels and switches: the role of prolines in signalling via transmembrane α-helices. Trends Pharmacol Sci 21:445–451PubMedGoogle Scholar
  250. Sansom MS, Shrivastava IH, Bright JN, Tate J, Capener CE, Biggin PC (2002) Potassium channels: structures, models, simulations. Biochim Biophys Acta 1565:294–307PubMedGoogle Scholar
  251. Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop—a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15:430–434PubMedGoogle Scholar
  252. Sauter NK, Mau T, Rader SD, Agard DA (1998) Structure of α-lytic protease complexed with its pro region. Nat Struct Biol 5:945–950PubMedGoogle Scholar
  253. Schmidt BH, Burgin AB, Deweese JE, Osheroff N, Berger JM (2010) A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465:641–644PubMedPubMedCentralGoogle Scholar
  254. Schmitt E, Moulinier L, Fujiwara S, Imanaka T, Thierry J-C, Moras D (1998) Crystal structure of aspartyl-tRNA synthetase from Pyrococcus kodakaraensis KOD: archaeon specificity and catalytic mechanism of adenylate formation. EMBO J 17:5227–5237PubMedPubMedCentralGoogle Scholar
  255. Schörken U, Thorell S, Schürmann M, Jia J, Sprenger GA, Schneider G (2001) Identification of catalytically important residues in the active site of Escherichia coli transaldolase. Eur J Biochem 268:2408–2415PubMedGoogle Scholar
  256. Schumacher MA, Goodman RH, Brennan RG (2000a) The structure of a CREB bZIP.somatostatin CRE complex reveals the basis for selective dimerization and divalent cation-enhanced DNA binding. J Biol Chem 275:35242–35247PubMedGoogle Scholar
  257. Schumacher MA, Scott DM, Mathews II, Ealick SE, Roos DS, Ullman B, Brennan RG (2000b) Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding. J Mol Biol 298:875–893PubMedGoogle Scholar
  258. Screpanti E, Hunte C (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J Struct Biol 159:261–267PubMedGoogle Scholar
  259. Sekar K, Yu BZ, Rogers J, Lutton J, Liu X, Chen X, Tsai MD, Jain MK, Sundaralingam M (1997) Phospholipase A2 engineering. Structural and functional roles of the highly conserved active site residue aspartate-99. Biochemistry 36:3104–3114PubMedGoogle Scholar
  260. Selmer T, Pierik AJ, Heider J (2005) New glycyl radical enzymes catalyzing key metabolic steps in anaerobic bacteria. Biol Chem 386:981–988PubMedGoogle Scholar
  261. Serrano L, Bycroft M, Fersht AR (1991) Aromatic–aromatic interactions and protein stability. Investigation by double-mutant cycles. J Mol Biol 218:465–475PubMedGoogle Scholar
  262. Shi Z, Olson CA, Rose GD, Baldwin RL, Kallenbach NR (2002) Polyproline II structure in a sequence of seven alanine residues. Proc Natl Acad Sci USA 99:9190–9195PubMedGoogle Scholar
  263. Shiels JC, Tuite JB, Nolan SJ, Baranger AM (2002) Investigation of a conserved stacking interaction in target site recognition by the U1A protein. Nucleic Acids Res 30:550–558PubMedPubMedCentralGoogle Scholar
  264. Shinoda T, Ogawa H, Cornelius F, Toyoshima C (2009) Crystal structure of the sodium–potassium pump at 2.4 Å resolution. Nature 459:446–450PubMedGoogle Scholar
  265. Sirover MA (1997) Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J Cell Biochem 66:133–140PubMedGoogle Scholar
  266. Smith JA, Pease LG (1980) Reverse turns in peptides and proteins. CRC Crit Rev Biochem 8:315–399PubMedGoogle Scholar
  267. Smith CM, Radzio-Andzelm E, Madhusudan, Akamine P, Taylor SS (1999) The catalytic subunit of cAMP-dependent protein kinase: prototype for an extended network of communication. Prog Biophys Mol Biol 71:313–341PubMedGoogle Scholar
  268. Snel B, Bork P, Huynen M (2000) Genome evolution. Gene fusion versus gene fission. Trends Genetics 16:9–11Google Scholar
  269. Sonneborn T (1965) Degeneracy of the genetic code: extent, nature, and genetic implications. In: Bryson V, Vogel H (eds) Evolving genes and proteins. Academic Press, New York, pp 377–397Google Scholar
  270. Spek EJ, Olson CA, Shi Z, Kallenbach NR (1999) Alanine is an intrinsic α-helix stabilizing amino acid. J Am Chem Soc 121:5571–5572Google Scholar
  271. Stanley AM, Fleming KG (2007) The role of a hydrogen bonding network in the transmembrane β-barrel OMPIA. J Mol Biol 370:912–924PubMedGoogle Scholar
  272. Stary A, Wacker SJ, Boukharta L, Zachariae U, Karimi-Nejad Y, Aqvist J, Vriend G, de Groot BL (2010) Toward a consensus model of the hERG potassium channel. ChemMedChem 5:455–467PubMedGoogle Scholar
  273. Stehle T, Schulz GE (1992) Refined structure of the complex between guanylate kinase and its substrate GMP at 2.0Å resolution. J Mol Biol 224:1127–1141PubMedGoogle Scholar
  274. Steitz TA, Steitz JA (1993) A general two-metal ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498–6502PubMedGoogle Scholar
  275. Stepanovic SZ, Potet F, Petersen CI, Smith JA, Meller J, Baiser JR, Kupershmidt S (2009) The evolutionarily conserved residue A653 plays a key role in HERG channel closing. J Physiol 587:2555–2566PubMedPubMedCentralGoogle Scholar
  276. Su CC, Long F, Lei HT, Bolla JR, Do SV, Rajashankar KR, Yu EW (2012) Charged amino acids (R83, E567, D617, E625, R669, and K678) of CusA are required for transport in the Cus efflux system. J Mol Biol 422:429–441PubMedPubMedCentralGoogle Scholar
  277. Svetlov V, Vassylyev DG, Artsimovitch I (2004) Discrimination against deoxyribonucleotide substrates by bacterial RNA polymerase. J Biol Chem 279:38087–38090PubMedPubMedCentralGoogle Scholar
  278. Tajkhorshid E, Nollert P, Jensen MØ, Miercke LJW, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296:525–530PubMedGoogle Scholar
  279. Takano K, Tsuchimori K, Yamagata Y, Yutani K (2000) Contribution of salt bridges near the surface of a protein to the conformational stability. Biochemistry 39:12375–12381PubMedGoogle Scholar
  280. Takeyama M, Ihara K, Moriyama Y, Noumi T, Ida K, Tomioka N, Itai A, Maeda M, Futai M (1990) The glycine-rich sequence of the β-subunit of Escherichia coli H+-ATPase is important for activity. J Biol Chem 265:21279–21284PubMedGoogle Scholar
  281. Tanaka J, Yanagawa H, Doi N (2011) Comparison of the frequency of functional SH3 domains with different limited sets of amino acids using mRNA display. PLoS ONE 6:e18034PubMedPubMedCentralGoogle Scholar
  282. Taylor FJ, Coates D (1989) The code within the codons. Biosystems 22:177–187PubMedGoogle Scholar
  283. Temiakov D, Patlan V, Anikin M, McAllister WT, Yokoyama S, Vassylyev DG (2004) Structural basis for substrate selection by T7 RNA polymerase. Cell 116:381–391PubMedGoogle Scholar
  284. Tholema N, Vor der Brüggen M, Mäser P, Nakamura T, Schroeder JI, Kobayashi H, Uozumi N, Bakker EP (2005) All four putative selectivity filter glycine residues in KtrB are essential for high affinity and selective K+ uptake by the KtrAB system from Vibrio alginolyticus. J Biol Chem 280:41146–41154PubMedGoogle Scholar
  285. Tieleman DP, Shrivastava IH, Ulmschneider MR, Sansom MS (2001) Proline-induced hinges in transmembrane helices: possible roles in ion channel gating. Proteins 44:63–72PubMedGoogle Scholar
  286. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405:647–655PubMedGoogle Scholar
  287. Trifonov EN (2004) The triplet code from first principles. J Biomol Struct Dyn 22:1–11Google Scholar
  288. Trotta CR, Paushkin SV, Patel M, Li H, Peltz SW (2006) Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site. Nature 441:375–377PubMedGoogle Scholar
  289. Tsigelny IF, Sharikov Y, Greenberg JP, Miller MA, Kouznetsova VL, Larson CA, Howell SB (2012) An all-atom model of the structure of human copper transporter 1. Cell Biochem Biophys 63:223–234PubMedPubMedCentralGoogle Scholar
  290. Usher KC, Remington SJ, Martin DP, Drueckhammer DG (1994) A very short hydrogen bond provides only moderate stabilization of an enzyme-inhibitor complex of citrate synthase. Biochemistry 33:7753–7759PubMedGoogle Scholar
  291. van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a protein-conducting channel. Nature 427:36–44PubMedGoogle Scholar
  292. van der Gulik PTS, Hoff WD (2011) Unassigned codons, nonsense suppression and anticodon modifications in the evolution of the genetic code. J Mol Evol 73:59–69PubMedGoogle Scholar
  293. Vassylyev DG, Sekine S, Laptenko O, Lee J, Vassylyev MN, Borukhov S, Yokoyama S (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6Å resolution. Nature 417:712–719PubMedGoogle Scholar
  294. Veis A, Nawrot CF (1970) Basicity differences among peptide bonds. J Am Chem Soc 92:3910–3914PubMedGoogle Scholar
  295. Veltman OR, Eijsink VG, Vriend G, de Kreij A, Venema G, Van den Burg B (1998) Probing catalytic hinge bending motions in thermolysis-like proteases by glycine → alanine mutations. Biochemistry 37:5305–5311PubMedGoogle Scholar
  296. Venkatesan R, Alahuhta M, Pihko PM, Wierenga RK (2011) High resolution crystal structures of triosephosphate isomerase complexed with its suicide inhibitors: the conformational flexibility of the catalytic glutamate in its closed, liganded active site. Protein Sci 20:1387–1397PubMedPubMedCentralGoogle Scholar
  297. Vertommen D, Bertrand L, Sontag B, Di Pietro A, Louckx MP, Vidal H, Hue L, Rider MH (1996) The ATP-binding site in the 2-kinase domain of liver 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Study of the role of Lys-54 and Thr-55 by site-directed mutagenesis. J Biol Chem 271:17875–17880PubMedGoogle Scholar
  298. Vetsigian K, Woese C, Goldenfeld N (2006) Collective evolution and the genetic code. Proc Natl Acad Sci USA 103:10696–10701PubMedGoogle Scholar
  299. Villafane A, Voskoboynik Y, Ruhl I, Sannino D, Maezato Y, Blim P, Bini E (2011) CopR of Sulfolobus solfataricus represents a novel class of archaeal-specific copper-responsive activators of transcription. Microbiology 157:2808–2817PubMedGoogle Scholar
  300. Vogel G (1998) Tracking the history of the genetic code. Science 281:329–331PubMedGoogle Scholar
  301. Vogel HJ, Schibli DJ, Jing W, Lohmeier-Vogel EM, Epand RF, Epand RM (2002) Towards a structure–function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem Cell Biol 80:49–63PubMedGoogle Scholar
  302. von Heijne G, Gavel Y (1988) Topogenic signals in integral membrane proteins. Eur J Biochem 174:671–678Google Scholar
  303. Vyas Nk, Vyas MN, Quiocho FA (2003) Crystal structure of M. tuberculosis ABC phosphate transport receptor; specificity and charge compensation dominated by ion-dipole interactions. Structure 11:765–777PubMedGoogle Scholar
  304. Wahl MC, Bourenkov GP, Bartunik HD, Huber R (2000) Flexibility, conformational diversity and two dimerization modes in complexes of ribosomal protein L12. EMBO J 19:174–186PubMedPubMedCentralGoogle Scholar
  305. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951PubMedPubMedCentralGoogle Scholar
  306. Walsh CT (1979) Enzymatic reaction mechanisms. WH Freeman, San FranciscoGoogle Scholar
  307. Wan Q, Ahmed MF, Fairman J, Gorzelle B, de la Fuente M, Dealwis C, Maguire ME (2011) X-ray crystallography and isothermal titration calorimetry studies of the Salmonella zinc transporter. Structure 19:700–710PubMedPubMedCentralGoogle Scholar
  308. Wang X, Deng Z, Kemp RG (1998) An essential methionine residue involved in substrate binding by phosphofructokinases. Biochem Biophys Res Commun 250:466–468PubMedGoogle Scholar
  309. Watson JD, Milner-White EJ (2002) A novel main-chain anion-binding site in proteins: the nest. A particular combination of ϕ, ψ values in successive residues gives rise to anion-binding sites that occur commonly and are found often at functionally important regions. J Mol Biol 315:171–182PubMedGoogle Scholar
  310. Wedekind JE, Poyner RR, Reed Gh, Rayment I (1994) Chelation of serine 39 to Mg2+ latches a gate at the active site of enolase: structure of the bis(Mg2+) complex of yeast enolase and the intermediate analog phosphonoacetohydroxamate at 2.1Å resolution. Biochemistry 33:9333–9342PubMedGoogle Scholar
  311. Wierenga RK, Kapetaniou EG, Venkatesan R (2010) Triosephosphate isomerase: a highly evolved biocatalyst. Cell Mol Life Sci 67:3961–3982PubMedGoogle Scholar
  312. Williams KA, Deber CM (1991) Proline residues in transmembrane helices: structural or dynamic role? Biochemistry 30:8919–8923PubMedGoogle Scholar
  313. Wise E, Yew WS, Babbitt PC, Gerlt JA, Rayment I (2002) Homologous (β/α)8-barrel enzymes that catalyze unrelated reactions: orotidine-5′-monophosphate decarboxylase and 3-keto-l-gulonate-6-phosphate decarboxylase. Biochemistry 41:3861–3869PubMedGoogle Scholar
  314. Woese CR (1965) On the evolution of the genetic code. Proc Natl Acad Sci USA 54:1546–1552PubMedGoogle Scholar
  315. Woese CR, Dugre DH, Saxinger WC, Dugre SA (1966) The molecular basis for the genetic code. Proc Natl Acad Sci USA 55:966–974PubMedGoogle Scholar
  316. Wong JT (1975) A co-evolution theory of the genetic code. Proc Natl Acad Sci USA 72:1909–1912Google Scholar
  317. Wong JT (1988) Evolution of the genetic code. Microbiol Sci 5:174–181Google Scholar
  318. Wotring VE, Miller TS, Weiss DS (2003) Mutations at the GABA receptor selectivity filter: a possible role for effective charges. J Physiol 548(Pt2):527–540PubMedPubMedCentralGoogle Scholar
  319. Wu WJ, Raleigh DP (1998) Local control of peptide conformation: stabilization of cis proline peptide bonds by aromatic proline interactions. Biopolymers 45:381–394PubMedGoogle Scholar
  320. Wu LF, Tomich JM, Saier MH (1990) Structure and evolution of a multidomain multiphosphoryl transfer protein. Nucleotide sequence of the fruB(HI) gene in Rhodobacter capsulatus and comparisons with homologous genes from other organisms. J Mol Biol 213:687–703PubMedGoogle Scholar
  321. Xue S, Calvin K, Li H (2006) RNA recognition and cleavage by a splicing endonuclease. Science 312:906–910PubMedGoogle Scholar
  322. Yang W, Lee JY, Nowotny M (2006) Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol Cell 22:5–13PubMedGoogle Scholar
  323. Yang YC, Lin S, Chang PC, Lin HC, Kuo CC (2011) Functional extension of amino acid triads from the fourth transmembrane segment (S4) into its external linker in Shaker K+ channels. J Biol Chem 286:37503–37514PubMedPubMedCentralGoogle Scholar
  324. Yao J, Dyson HJ, Wright PE (1994) Three-dimensional structure of a type VI turn in a linear peptide in water solution. Evidence for stacking of aromatic rings as a major stabilizing factor. J Mol Biol 243:754–766PubMedGoogle Scholar
  325. Yarus M, Widmann JJ, Knight R (2009) RNA-amino acid binding: a stereochemical era for the genetic code. J Mol Evol 69:406–429Google Scholar
  326. Yau WM, Wimley WC, Gawrisch K, White SH (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37:14713–14718PubMedGoogle Scholar
  327. Yin YW, Steitz TA (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase. Science 298:1387–1395PubMedGoogle Scholar
  328. Yohannan S, Faham S, Yang D, Whitelegge JP, Bowie JU (2004) The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. PNAS 101:957–963Google Scholar
  329. Yuan J, O’Donoghue P, Ambrogelly A, Gundllapalli S, Sherrer RL, Palioura S, Simonović M, Söll D (2010a) Distinct genetic code expansion strategies for selenocysteine and pyrrolysine are reflected in different aminoacyl-tRNA formation systems. FEBS Lett 584:342–349PubMedPubMedCentralGoogle Scholar
  330. Yuan P, Leonetti MD, Pico AR, Hsiung Y, MacKinnon R (2010b) Structure of the human BK channel Ca2+-activation apparatus at 3.0Å resolution. Science 329:182–186PubMedPubMedCentralGoogle Scholar
  331. Zhang YP, Lewis RN, Hodges RS, McElhaney RN (2001) Peptide models of the helical hydrophobic transmembrane segments of membrane proteins: interactions of acetyl-K2-(LA)12–K2-amide with phosphatidylethanolamine bilayer membranes. Biochemistry 40:474–482PubMedGoogle Scholar
  332. Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, He J, Wang J, Clapham DE, Yan N (2012) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:130–134PubMedPubMedCentralGoogle Scholar
  333. Zhou GC, Parikh SL, Tyler PC, Evans GB, Furneaux RH, Zubkova OV, Benjes PA, Schramm VL (2004) Inhibitors of ADP-ribosylating bacterial toxins based on oxacarbenium ion character at their transition states. J Am Chem Soc 126:5690–5698PubMedGoogle Scholar
  334. Zimmerman SA, Ferry JG (2006) Proposal for a hydrogen bond network in the active site of the prototypic γ-class carbonic anhydrase. Biochemistry 45:5149–5157PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Molecular BiologyUniversity of WyomingLaramieUSA

Personalised recommendations