Skip to main content
Log in

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

  • Original Paper
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abillon E, Bremier L, Cardinaud R (1990) Conformational calculations on the Ala14-Pro27 LC1 segment of rabbit skeletal myosin. Biochim Biophys Acta 1037:394–400

    Article  CAS  PubMed  Google Scholar 

  • Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628

    Article  CAS  PubMed  Google Scholar 

  • Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615

    Article  CAS  PubMed  Google Scholar 

  • Agris PF, Vendeix FAP, Graham WD (2007) tRNA’s wobble decoding of the genome: 40 years of modification. J Mol Biol 366:1–13

    Article  CAS  PubMed  Google Scholar 

  • 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 349:853–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An Bondar, Dau H (2012) Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim Biophys Acta 1817:1177–1190

    Article  CAS  Google Scholar 

  • 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 8:1220–1224

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 176:111–116

    Article  CAS  PubMed  Google Scholar 

  • 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 100:3814–3819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arraiano CM, Matos RG, Barbas A (2010) RNase II: the finer details of the Modus operandi of a molecular killer. RNA Biol 7:276–281

    Article  CAS  PubMed  Google Scholar 

  • Ascenzi P, Santucci R, Coletta M, Polticelli F (2010) Cytochromes: reactivity of the “dark side” of the heme. Biophys Chem 152:21–27

    Article  CAS  PubMed  Google Scholar 

  • 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 285:14594–14602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e23355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aurora R, Rose GD (1998) Helix capping. Protein Sci 7:21–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babu YS, Bugg CE, Cook WJ (1988) Structure of calmodulin refined at 2.2 Å resolution. J Biol Chem 204:191–204

    CAS  Google Scholar 

  • Baldwin RL (2007) Energetics of protein folding. J Mol Biol 371:283–301

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P (2010) Affinity gradients drive copper to cellular destinations. Nature 465:645–648

    Article  CAS  PubMed  Google Scholar 

  • Barford D, Johnson LN (1989) The allosteric transition of glycogen phosphorylase. Nature 340:609–616

    Article  CAS  PubMed  Google Scholar 

  • 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:e33058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benner SA, Cohen MA, Gonnet GH (1993) Empirical and structural models for insertions and deletions in the divergent evolution of proteins. J Mol Biol 229:1065–1082

    Article  CAS  PubMed  Google Scholar 

  • Blow DM, Birktoft JJ, Hartley BS (1969) Role of a buried acid group in the mechanism of action of chymotrypsin. Nature 221:337–340

    Article  CAS  PubMed  Google Scholar 

  • Boal AK, Rosenzweig AC (2009) Structural biology of copper trafficking. Chem Rev 109:4760–4779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 280:25644–25650

    Article  CAS  PubMed  Google Scholar 

  • 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 98:881–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1818:2158–2170

    Article  CAS  PubMed  Google Scholar 

  • 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 38:9778–9782

    Article  CAS  PubMed  Google Scholar 

  • Brieba LG, Sousa R (2000) Roles of histidine 784 and tyrosine 639 in ribose discrimination by T7 RNA polymerase. Biochemistry 39:919–923

    Article  CAS  PubMed  Google Scholar 

  • Brooks DJ, Fresco JR (2002) Increased frequency of cysteine, tyrosine, and phenylalanine residues since the last universal ancestor. Mol Cell Proteomics 1:125–131

    Article  CAS  PubMed  Google Scholar 

  • Brosig B, Langosch D (1998) The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci 7:1052–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107:4931–4936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buis JM, Broderick JB (2005) Pyruvate formate-lyase activating enzyme: elucidation of a novel mechanism for glycyl radical formation. Arch Biochem Biophys 433:288–296

    Article  CAS  PubMed  Google Scholar 

  • 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 4:89–96

    Article  CAS  PubMed  Google Scholar 

  • Bulaj G, Kortemme T, Goldenberg DP (1998) Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry 37:8965–8972

    Article  CAS  PubMed  Google Scholar 

  • Burley SK, Petsko GA (1985) Aromatic–aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28

    Article  CAS  PubMed  Google Scholar 

  • Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–210

    Article  CAS  PubMed  Google Scholar 

  • Bywater RP, Thomas D, Vriend G (2001) A sequence and structural study of transmembrane helices. J Comput Aided Mol Des 15:533–552

    Article  CAS  PubMed  Google Scholar 

  • 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 45:7682–7692

    Article  CAS  PubMed  Google Scholar 

  • Calvin K, Xue S, Ellis C, Mitchell MH, Li H (2008) Probing the catalytic triad of an archaeal RNA splicing endonuclease. Biochemistry 47:13659–13665

    Article  CAS  PubMed  Google Scholar 

  • Carmel AB, Matthews BW (2004) Crystal structure of the BstDEAD N-terminal domain: a novel DEAD protein from Bacillus stearothermophilus. RNA 10:66–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carter CW, Duax WL (2002) Did tRNA synthetase classes arise on opposite strands of the same gene? Mol Cell 10:705–708

    Article  CAS  PubMed  Google Scholar 

  • Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo—transport of ferrous iron into bacteria. Biometals 19:145–157

    Article  CAS  Google Scholar 

  • 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 46:630–639

    Article  CAS  PubMed  Google Scholar 

  • 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 53:555–595

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarti P (1993) Anion binding sites in protein structures. J Mol Biol 234:463–482

    Article  CAS  PubMed  Google Scholar 

  • 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:e29996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 367:970–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman HA, Riese RJ, Shi GP (1997) Emerging roles for cysteine proteases in human biology. Annu Rev Physiol 59:63–88

    Article  CAS  PubMed  Google Scholar 

  • Charlier HA, Runquist JA, Miziorko HM (1994) Evidence supporting catalytic roles for aspartate residues in phosphoribulokinase. Biochemistry 33:9343–9350

    Article  CAS  PubMed  Google Scholar 

  • Cheetham GMT, Steitz TA (1999) Structure of a transcribing T7 RNA polymerase initiation complex. Science 286:2305–2309

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Stites WE (2001) Packing is a key selection factor in the evolution of protein hydrophobic cores. Biochemistry 40:15280–15289

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Lu Z, Sakon J, Stites WE (2004) Proteins with simplified hydrophobic cores compared to other packing mutants. Biophys Chem 110:239–248

    Article  CAS  PubMed  Google Scholar 

  • 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 281:13777–13783

    Article  CAS  PubMed  Google Scholar 

  • 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 8:312–316

    Article  CAS  PubMed  Google Scholar 

  • Chivers PT, Prehoda KE, Raines RT (1997) The CXXC motif: a rheostat in the active site. Biochemistry 36:4061–4066

    Article  CAS  PubMed  Google Scholar 

  • Cho HS, Pelton JG, Yan D, Kustu S, Wemmer DE (2001) Phosphoaspartates in bacterial signal transduction. Curr Opin Struct Biol 11:679–684

    Article  CAS  PubMed  Google Scholar 

  • Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain. Science 309:581–585

    Article  CAS  PubMed  Google Scholar 

  • Chothia C, Gough J, Vogel C, Teichmann SA (2003) Evolution of the protein repertoire. Science 300:1701–1703

    Article  CAS  PubMed  Google Scholar 

  • Chou PY, Fasman GD (1978) Empirical predictions of protein conformation. Annu Rev Biochem 47:251–276

    Article  CAS  PubMed  Google Scholar 

  • 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 300:141–152

    Article  CAS  PubMed  Google Scholar 

  • 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 272:319–324

    Article  Google Scholar 

  • 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 265:1405–1412

    Article  CAS  PubMed  Google Scholar 

  • 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 242:321–329

    CAS  PubMed  Google Scholar 

  • Cordes FS, Bright JN, Sansom MS (2002) Proline-induced distortions in transmembrane helices. J Mol Biol 323:951–960

    Article  CAS  PubMed  Google Scholar 

  • Crick FHC (1968) The origin of the genetic code. J Mol Biol 38:367–379

    Article  CAS  PubMed  Google Scholar 

  • Crick FHC, Brenner S, Klug A, Pieczenik G (1976) A speculation on the origin of protein synthesis. Orig Life 7:389–397

    Article  CAS  PubMed  Google Scholar 

  • 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 96:340–347

    Article  CAS  PubMed  Google Scholar 

  • Dale T, Fahlman RP, Olejniczak M, Uhlenbeck OC (2009) Specificity of the ribosomal A site for aminoacyl-tRNAs. Nucleic Acids Res 37:1202–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 467:734–738

    Article  CAS  PubMed  Google Scholar 

  • Davis BK (1999) Evolution of the genetic code. Prog Biophys Mol Biol 72:157–243

    Article  CAS  PubMed  Google Scholar 

  • 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 97:3189–3194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Cera E (2006) A structural perspective on enzymes activated by monovalent cations. J Biol Chem 281:1305–1308

    Article  PubMed  CAS  Google Scholar 

  • Di Giulio M (2001) A blind empiricism against the coevolution theory of the origin of the genetic code. J Mol Evol 53:724–732

    Article  PubMed  CAS  Google Scholar 

  • 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 14:3766–3776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dill KA (1990) Dominant forces in protein folding. Biochemistry 29:7133–7155

    Article  CAS  PubMed  Google Scholar 

  • Dilworth D, Gudavicius G, Leung A, Nelson CJ (2012) The roles of peptidyl-proline isomerases in gene regulation. Biochem Cell Biol 90:55–69

    Article  CAS  PubMed  Google Scholar 

  • Ding S, Ingleby L, Ahern CA, Horn R (2005) Investigating the putative hinge in Shaker potassium channel. J Gen Physiol 126:213–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doig AJ (2002) Recent advances in helix–coil theory. Biophys Chem 101–102:281–293

    Article  PubMed  Google Scholar 

  • Donald JE, Kulp DW, DeGrado WF (2011) Salt bridges: geometrically specific, designable interactions. Proteins 79:898–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 391:251–258

    Article  PubMed  Google Scholar 

  • 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 280:69–77

    CAS  Google Scholar 

  • 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 48:4557–4566

    Article  CAS  PubMed  Google Scholar 

  • Dreusicke D, Schulz GE (1986) The glycine-rich loop of adenylate kinase forms a giant anion hole. FEBS Lett 208:301–304

    Article  CAS  PubMed  Google Scholar 

  • Dutzler R (2004) The structural basis of ClC chloride channel function. Trends Neurosci 27:315–320

    Article  CAS  PubMed  Google Scholar 

  • Dutzler R, Campbell EB, MacKinnon R (2003) Gating the selectivity filter in ClC chloride channels. Science 300:108–112

    Article  CAS  PubMed  Google Scholar 

  • Eigen M, Schuster P (1978) The hypercycle. A principle of natural self-organization. Part C: the realistic hypercycle. Naturwissenschaften 65:341–369

    Article  CAS  Google Scholar 

  • Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:217–228

    Article  CAS  PubMed  Google Scholar 

  • Eitinger T, Mandrand-Berthelot M-A (2000) Nickel transport systems in microorganisms. Arch Microbiol 173:1–9

    Article  CAS  PubMed  Google Scholar 

  • Epand RM, Epand RF, Martin I, Ruysschaert J-M (2001) Membrane interactions of mutated forms of the influenza fusion peptide. Biochemistry 40:8800–8807

    Article  CAS  PubMed  Google Scholar 

  • 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 313:354–357

    Article  CAS  PubMed  Google Scholar 

  • 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 279:31419–31428

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Campbell EB, Hsiung Y, MacKinnon R (2010) Structure of a eukaryotic CLC transporter defines an intermediate state in the transport cycle. Science 330:635–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 314:235–238

    Article  CAS  PubMed  Google Scholar 

  • Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21:R877–R883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1555:29–36

    Article  CAS  PubMed  Google Scholar 

  • 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 35:5125–5136

    Article  CAS  PubMed  Google Scholar 

  • 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 98:14380–14384

    Article  Google Scholar 

  • 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 278:3055–3062

    Article  CAS  PubMed  Google Scholar 

  • Francis BR (2011) An alternative to the RNA world hypothesis. Trends Evol Biol 3:e2

    Article  CAS  Google Scholar 

  • 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 443:110–114

    Article  PubMed  CAS  Google Scholar 

  • Freeland SJ, Hurst LD (1998) The genetic code is one in a million. J Mol Evol 47:238–248

    Article  CAS  PubMed  Google Scholar 

  • 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 279:8396–8402

    Article  CAS  PubMed  Google Scholar 

  • 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 41:609–617

    Article  CAS  PubMed  Google Scholar 

  • 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 324:1565–1568

    Article  CAS  PubMed  Google Scholar 

  • Gastinel LN, Cambillau C, Bourne Y (1999) Crystal structures of the bovine β4galactosyltransferase catalytic domain and its complex with uridine diphosphogalactose. EMBO J 18:3546–3557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 405:199–221

    Article  CAS  PubMed  Google Scholar 

  • Giles NM, Watts AB, Giles GI, Fry FH, Littlechild JA, Jacob C (2003) Metal and redox modulation of cysteine protein function. Chem Biol 10:677–693

    Article  CAS  PubMed  Google Scholar 

  • Glusker JP (1991) Structural aspects of metal liganding to functional groups in proteins. Adv Protein Chem 42:1–76

    Article  CAS  PubMed  Google Scholar 

  • Gourdon P, Liu X-Y, Skjorringe T, Morth JP, Møller LB, Pedersen BP (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–65

    Article  CAS  PubMed  Google Scholar 

  • 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 38:8892–8898

    Article  CAS  PubMed  Google Scholar 

  • 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 584:252–264

    Article  CAS  PubMed  Google Scholar 

  • 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 325:744–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harding MM (2004) The architecture of metal coordination groups in proteins. Acta Crystallogr D 60:849–859

    Article  PubMed  CAS  Google Scholar 

  • 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 282:31972–31981

    Article  CAS  PubMed  Google Scholar 

  • Harris TK, Turner GJ (2002) Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life 53:85–98

    Article  CAS  PubMed  Google Scholar 

  • 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 28:3602–3612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heathcote P, Jones MR, Fyfe PK (2003) Type I photosynthetic reaction centres: structure and function. Philos Trans R Soc Lond B 358:231–243

    Article  CAS  Google Scholar 

  • Hellinga HW, Evans PR (1987) Mutations in the active site of Escherichia coli phosphofructokinase. Nature 327:437–439

    Article  CAS  PubMed  Google Scholar 

  • Herzberg O, James M (1985) Structure of the calcium regulatory muscle protein troponin-C at 2.8 Å resolution. Nature 313:653–659

    Article  CAS  PubMed  Google Scholar 

  • 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 4:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 40:10554–10566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirst J (2010) Towards the molecular mechanism of respiratory complex I. Biochem J 425:327–339

    Article  CAS  Google Scholar 

  • 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 34:145–157

    Article  CAS  PubMed  Google Scholar 

  • 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 40:13998–14003

    Article  CAS  PubMed  Google Scholar 

  • Holliday GL, Mitchell JB, Thornton JM (2009) Understanding the functional roles of amino acid residues in enzyme catalysis. J Mol Biol 390:560–577

    Article  CAS  PubMed  Google Scholar 

  • 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 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • 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 39:3156–3168

    Article  CAS  PubMed  Google Scholar 

  • 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 282:1669–1675

    Article  CAS  PubMed  Google Scholar 

  • 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 126:929–940

    Article  CAS  PubMed  Google Scholar 

  • 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 435:1197–1202

    Article  CAS  PubMed  Google Scholar 

  • 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 50:8497–8507

    Article  CAS  PubMed  Google Scholar 

  • 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 27:165–186

    Article  CAS  PubMed  Google Scholar 

  • 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 281:64–71

    Article  CAS  PubMed  Google Scholar 

  • 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 105:11194–11199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) The open pore conformation of potassium channels. Nature 417:523–526

    Article  CAS  PubMed  Google Scholar 

  • 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 44:9787–9794

    Article  CAS  PubMed  Google Scholar 

  • Jimenez-Sanchez A (1995) On the origin and evolution of the genetic code. J Mol Evol 41:712–716

    Article  CAS  PubMed  Google Scholar 

  • 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 10:469–481

    Article  CAS  PubMed  Google Scholar 

  • Jordan SR, Pabo CO (1988) Structure of the lambda complex at 2.5Å resolution: details of the repressor–operator interactions. Science 242:893–899

    Article  CAS  PubMed  Google Scholar 

  • 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 33:2824–2829

    Article  CAS  PubMed  Google Scholar 

  • 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 38:10527–10532

    Article  CAS  PubMed  Google Scholar 

  • 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 38:2617–2627

    Article  CAS  PubMed  Google Scholar 

  • Kieseritzky G, Knapp E-W (2011) Charge transport in the ClC-type chloride-proton anti-porter from Escherichia coli. J Biol Chem 286:2976–2986

    Article  CAS  PubMed  Google Scholar 

  • Killian JA, von Heijne G (2000) How proteins adapt to a membrane–water interface. Trends Biochem Sci 25:429–434

    Article  CAS  PubMed  Google Scholar 

  • Kim EE, Wyckoff HW (1991) Reaction mechanism of alkaline phosphatase based on crystal structures. Two metal ion catalysis. J Mol Biol 218:449–464

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Geiger JH, Hahn S, Sigler PB (1993a) Crystal structure of a yeast TBP/TATA-box complex. Nature 365:512–520

    Article  CAS  PubMed  Google Scholar 

  • Kim JL, Nikolov DB, Burley SK (1993b) Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 365:520–527

    Article  CAS  PubMed  Google Scholar 

  • Klieger G, Grothe R, Mallick P, Eisenberg D (2002) GXXXG and AXXXA: common α-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41:5990–5997

    Article  CAS  Google Scholar 

  • Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 308:267–269

    Article  CAS  PubMed  Google Scholar 

  • Knight RD, Freeland SJ, Landweber LF (1999) Selection, history and chemistry: the three faces of the genetic code. Trends Biochem Sci 24:241–247

    Article  CAS  PubMed  Google Scholar 

  • 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 274:205–216

    Article  CAS  Google Scholar 

  • Knowles JR (1991) Enzyme catalysis: not different, just better. Nature 350:121–124

    Article  CAS  PubMed  Google Scholar 

  • Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421

    Article  CAS  PubMed  Google Scholar 

  • Kolberg M, Strand KR, Graff P, Andersson KK (2004) Structure, function, and mechanism of ribonucleotide reductases. Biochim Biophys Acta 1699:1–34

    Article  CAS  PubMed  Google Scholar 

  • Koshland DE Jr (1976) The evolution of function in enzymes. Fed Proc 35:2104–2111

    CAS  PubMed  Google Scholar 

  • 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 334:625–637

    Article  CAS  PubMed  Google Scholar 

  • Krishnamurthy H, Gouaux E (2012) X-ray structure of LeuT in substrate-free outward-open and apo inward-open states. Nature 481:469–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuiper MJ, Davies PL, Walker VK (2001) A theoretical model of a plant antifreeze protein from Lolium perenne. Biophys J 81:3560–3565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 300:1922–1926

    Article  CAS  PubMed  Google Scholar 

  • 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 518:39–42

    Article  CAS  PubMed  Google Scholar 

  • 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 37:9724–9737

    Article  CAS  PubMed  Google Scholar 

  • 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 229:602–608

    Article  Google Scholar 

  • 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 6:1553–1561

    Article  Google Scholar 

  • 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 7:2550–2559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612:1–40

    Article  CAS  PubMed  Google Scholar 

  • 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 6:628–633

    Google Scholar 

  • 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 132:16225–16239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehman N, Jukes TH (1988) Genetic code development by stop codon takeover. J Theor Biol 135:203–214

    Article  CAS  PubMed  Google Scholar 

  • Lehoux IE, Mitra B (1999) (S)-Mandelate dehydrogenase from Pseudomonas putida: mutations of the catalytic base histidine-274 and chemical rescue of activity. Biochemistry 38:9948–9955

    Article  CAS  PubMed  Google Scholar 

  • Lei M, Podell ER, Baumann P, Cech TR (2003) DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426:198–203

    Article  CAS  PubMed  Google Scholar 

  • 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 106:4677–4682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis EB (1951) Pseudoallelism and gene evolution. Cold Spring Harbor Symp Quant Biol 16:159–174

    Article  CAS  PubMed  Google Scholar 

  • 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 100:323–332

    Article  CAS  PubMed  Google Scholar 

  • 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 46:1042–1054

    Article  CAS  PubMed  Google Scholar 

  • 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 281:36803–36810

    Article  CAS  PubMed  Google Scholar 

  • 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 433:657–661

    Article  PubMed  CAS  Google Scholar 

  • 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 36:1199–1211

    Article  CAS  PubMed  Google Scholar 

  • Linder P, Jankowsky E (2011) From unwinding to clamping—the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12:505–516

    Article  CAS  PubMed  Google Scholar 

  • Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20

    Article  CAS  PubMed  Google Scholar 

  • 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 273:23645–23648

    Article  CAS  PubMed  Google Scholar 

  • Long M (2000) A new function evolved from gene fusion. Genome Res 10:1743–1756

    Article  Google Scholar 

  • 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 467:484–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu H, Marti T, Booth PJ (2001) Proline residues in transmembrane α helices affect the folding of bacteriorhodopsin. J Mol Biol 308:437–446

    Article  CAS  PubMed  Google Scholar 

  • Lu KP, Finn G, Lee TH, Nicholson LK (2007) Prolyl cistrans isomerization as a molecular timer. Nat Chem Biol 3:619–629

    Article  CAS  PubMed  Google Scholar 

  • Luecke H, Quiocho FA (1990) High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347:402–406

    Article  CAS  PubMed  Google Scholar 

  • 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 440:833–837

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • MacArthur MW, Thornton JM (1991) Influence of proline residues on protein conformation. J Mol Biol 218:397–412

    Article  CAS  PubMed  Google Scholar 

  • MacKenzie KR, Prestegard JH, Engelman DM (1997) A transmembrane helix dimer: structure and implications. Science 276:131–133

    Article  CAS  PubMed  Google Scholar 

  • MacKinnon R (2003) Potassium channels. FEBS Lett 555:62–65

    Article  CAS  PubMed  Google Scholar 

  • Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98

    Article  CAS  PubMed  Google Scholar 

  • 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 462:113–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin JL (1995) Thioredoxin—a fold for all reasons. Structure 3:245–250

    Article  CAS  PubMed  Google Scholar 

  • Massey SE (2006) A sequential “2-1-3” model of genetic code evolution that explains codon restraints. J Mol Evol 62:809–810

    Article  CAS  PubMed  Google Scholar 

  • 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 308:659–662

    Article  CAS  PubMed  Google Scholar 

  • Meinhart A, Cramer P (2004) Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA processing factors. Nature 430:223–226

    Article  CAS  PubMed  Google Scholar 

  • Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164

    Article  CAS  PubMed  Google Scholar 

  • Meyer E, Cole G, Radhakrishnan R (1988) Structure of native pancreatic elastase at 1.65 Å resolution. Acta Cryst B44:26–38

    Article  CAS  Google Scholar 

  • 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 247:939–945

    Article  CAS  PubMed  Google Scholar 

  • Miller C, Nguitragool W (2009) A provisional transport mechanism for a chloride channel-type Cl/H+ exchanger. Philos Trans R Soc Lond B 364:175–180

    Article  CAS  Google Scholar 

  • 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 400:231–243

    Article  CAS  PubMed  Google Scholar 

  • 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 430:171–177

    Article  CAS  PubMed  Google Scholar 

  • Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949–955

    Article  CAS  PubMed  Google Scholar 

  • 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 6:957–970

    Article  CAS  PubMed  Google Scholar 

  • 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 307:913–928

    Article  CAS  PubMed  Google Scholar 

  • Monod J (1971) Chance and Necessity. A. A. Knopf, Inc., New York p143

    Google Scholar 

  • 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 12:60–70

    Article  CAS  PubMed  Google Scholar 

  • 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 479:194–199

    Article  CAS  PubMed  Google Scholar 

  • 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 224:159–177

    Article  CAS  PubMed  Google Scholar 

  • 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 308:654–659

    Article  CAS  PubMed  Google Scholar 

  • 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 285:21689–21697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 355:747–759

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HD, Marchut AJ, Hall CK (2004) Solvent effects on the conformational transition of a model polyalanine peptide. Protein Sci 13:2909–2924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 270:1464–1472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  Google Scholar 

  • O’Neal CJ, Jobling MG, Holmes RK, Hol WGJ (2005) Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309:1093–1096

    Article  PubMed  CAS  Google Scholar 

  • 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 1457:36–44

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, Heidelberg

    Book  Google Scholar 

  • Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC (2005) Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat Struct Mol Biol 12:788–793

    Article  CAS  PubMed  Google Scholar 

  • 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 273:19509–19517

    Article  CAS  PubMed  Google Scholar 

  • Orgel LE (1987) Evolution of the genetic apparatus. Cold Spring Harb Symp Quant Biol 52:9–16

    Article  CAS  PubMed  Google Scholar 

  • 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 146:651–657

    Article  CAS  PubMed  Google Scholar 

  • Otto SP, Yong P (2002) The evolution of gene duplicates. Adv Genetics 46:451–483

    Article  CAS  Google Scholar 

  • Pace CN, Scholtz JM (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys J 75:422–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paddock ML, Feher G, Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555:45–50

    Article  CAS  PubMed  Google Scholar 

  • Page M, Di Cera E (2006) Role of Na+ and K+ in enzyme function. Physiol Rev 86:1049–1092

    Article  CAS  PubMed  Google Scholar 

  • Pal D, Chakrabarti P (1998) Different types of interactions involving cysteine sulfhydryl group in proteins. J Biomol Struct Dyn 15:1059–1072

    Article  CAS  PubMed  Google Scholar 

  • 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 273:10454–10462

    Article  CAS  PubMed  Google Scholar 

  • 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 271:18632–18637

    Article  CAS  PubMed  Google Scholar 

  • Pascarella S, Argos P (1992) Analysis of insertions and deletions in protein structures. J Mol Biol 224:461–471

    Article  CAS  PubMed  Google Scholar 

  • Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane pump. Nature 450:1111–1114

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1860–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pejchal R, Ludwig ML (2004) Cobalamin-independent methionine synthase (MetE): a face-to-face double barrel that evolved by gene duplication. PLoS Biol 3:e31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perham RN (1991) Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein. Biochemistry 30:8501–8512

    Article  CAS  PubMed  Google Scholar 

  • Pomowski A, Zumft WG, Kroneck PM, Einsle O (2011) N2O binding at a [4Cu:2S] copper–sulfur cluster in nitrous oxide reductase. Nature 477:234–237

    Article  CAS  PubMed  Google Scholar 

  • Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3:827–837

    Article  CAS  PubMed  Google Scholar 

  • 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 277:26021–26030

    Article  CAS  PubMed  Google Scholar 

  • Purohit P, Auerbach A (2011) Glycine hinges with opposing actions at the acetylcholine receptor-channel transmitter binding site. Mol Pharmacol 79:351–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 264:767–775

    Article  CAS  PubMed  Google Scholar 

  • 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 1–98

    Google Scholar 

  • 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 31:4625–4631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riordan JF (1979) Arginyl residues and anion binding sites in proteins. Mol Cell Biochem 26:71–90

    Article  CAS  PubMed  Google Scholar 

  • 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 25:565–589

    Article  CAS  Google Scholar 

  • Rossman MG, Moras D, Olson KW (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature 250:194–199

    Article  Google Scholar 

  • Runquist JA, Rios SE, Vinarov DA, Miziorko HM (2001) Functional evaluation of serine/threonine residues in the P-loop of Rhodobacter sphaeroides phosphoribulokinase. Biochemistry 40:14530–14537

    Article  CAS  PubMed  Google Scholar 

  • Russ WP, Engelman DM (2000) The GxxxG motif: a framework for transmembrane helix–helix association. J Mol Biol 296:911–919

    Article  CAS  PubMed  Google Scholar 

  • 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 79:2331–2344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sansom MSP, Weinstein H (2000) Hinges, swivels and switches: the role of prolines in signalling via transmembrane α-helices. Trends Pharmacol Sci 21:445–451

    Article  CAS  PubMed  Google Scholar 

  • Sansom MS, Shrivastava IH, Bright JN, Tate J, Capener CE, Biggin PC (2002) Potassium channels: structures, models, simulations. Biochim Biophys Acta 1565:294–307

    Article  CAS  PubMed  Google Scholar 

  • Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop—a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15:430–434

    Article  PubMed  Google Scholar 

  • Sauter NK, Mau T, Rader SD, Agard DA (1998) Structure of α-lytic protease complexed with its pro region. Nat Struct Biol 5:945–950

    Article  CAS  PubMed  Google Scholar 

  • 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 465:641–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:5227–5237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 268:2408–2415

    Article  PubMed  Google Scholar 

  • 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 275:35242–35247

    Article  CAS  PubMed  Google Scholar 

  • 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 298:875–893

    Article  CAS  PubMed  Google Scholar 

  • Screpanti E, Hunte C (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J Struct Biol 159:261–267

    Article  CAS  PubMed  Google Scholar 

  • 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 36:3104–3114

    Article  CAS  PubMed  Google Scholar 

  • Selmer T, Pierik AJ, Heider J (2005) New glycyl radical enzymes catalyzing key metabolic steps in anaerobic bacteria. Biol Chem 386:981–988

    Article  CAS  PubMed  Google Scholar 

  • Serrano L, Bycroft M, Fersht AR (1991) Aromatic–aromatic interactions and protein stability. Investigation by double-mutant cycles. J Mol Biol 218:465–475

    Article  CAS  PubMed  Google Scholar 

  • 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 99:9190–9195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:550–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinoda T, Ogawa H, Cornelius F, Toyoshima C (2009) Crystal structure of the sodium–potassium pump at 2.4 Å resolution. Nature 459:446–450

    Article  CAS  PubMed  Google Scholar 

  • Sirover MA (1997) Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J Cell Biochem 66:133–140

    Article  CAS  PubMed  Google Scholar 

  • Smith JA, Pease LG (1980) Reverse turns in peptides and proteins. CRC Crit Rev Biochem 8:315–399

    Article  CAS  PubMed  Google Scholar 

  • 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 71:313–341

    Article  CAS  PubMed  Google Scholar 

  • Snel B, Bork P, Huynen M (2000) Genome evolution. Gene fusion versus gene fission. Trends Genetics 16:9–11

    Article  CAS  Google Scholar 

  • 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 377–397

    Chapter  Google Scholar 

  • Spek EJ, Olson CA, Shi Z, Kallenbach NR (1999) Alanine is an intrinsic α-helix stabilizing amino acid. J Am Chem Soc 121:5571–5572

    Article  CAS  Google Scholar 

  • Stanley AM, Fleming KG (2007) The role of a hydrogen bonding network in the transmembrane β-barrel OMPIA. J Mol Biol 370:912–924

    Article  CAS  PubMed  Google Scholar 

  • 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 5:455–467

    Article  CAS  PubMed  Google Scholar 

  • Stehle T, Schulz GE (1992) Refined structure of the complex between guanylate kinase and its substrate GMP at 2.0Å resolution. J Mol Biol 224:1127–1141

    Article  CAS  PubMed  Google Scholar 

  • Steitz TA, Steitz JA (1993) A general two-metal ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498–6502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 587:2555–2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 422:429–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svetlov V, Vassylyev DG, Artsimovitch I (2004) Discrimination against deoxyribonucleotide substrates by bacterial RNA polymerase. J Biol Chem 279:38087–38090

    Article  CAS  PubMed  Google Scholar 

  • 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 296:525–530

    Article  CAS  PubMed  Google Scholar 

  • Takano K, Tsuchimori K, Yamagata Y, Yutani K (2000) Contribution of salt bridges near the surface of a protein to the conformational stability. Biochemistry 39:12375–12381

    Article  CAS  PubMed  Google Scholar 

  • 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 265:21279–21284

    Article  CAS  PubMed  Google Scholar 

  • 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:e18034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor FJ, Coates D (1989) The code within the codons. Biosystems 22:177–187

    Article  CAS  PubMed  Google Scholar 

  • Temiakov D, Patlan V, Anikin M, McAllister WT, Yokoyama S, Vassylyev DG (2004) Structural basis for substrate selection by T7 RNA polymerase. Cell 116:381–391

    Article  CAS  PubMed  Google Scholar 

  • 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 280:41146–41154

    Article  CAS  PubMed  Google Scholar 

  • Tieleman DP, Shrivastava IH, Ulmschneider MR, Sansom MS (2001) Proline-induced hinges in transmembrane helices: possible roles in ion channel gating. Proteins 44:63–72

    Article  CAS  PubMed  Google Scholar 

  • Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405:647–655

    Article  CAS  PubMed  Google Scholar 

  • Trifonov EN (2004) The triplet code from first principles. J Biomol Struct Dyn 22:1–11

    Article  CAS  PubMed  Google Scholar 

  • 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 441:375–377

    Article  CAS  PubMed  Google Scholar 

  • 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 63:223–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:7753–7759

    Article  CAS  PubMed  Google Scholar 

  • 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 427:36–44

    Article  PubMed  CAS  Google Scholar 

  • van der Gulik PTS, Hoff WD (2011) Unassigned codons, nonsense suppression and anticodon modifications in the evolution of the genetic code. J Mol Evol 73:59–69

    Article  CAS  PubMed  Google Scholar 

  • 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 417:712–719

    Article  CAS  PubMed  Google Scholar 

  • Veis A, Nawrot CF (1970) Basicity differences among peptide bonds. J Am Chem Soc 92:3910–3914

    Article  CAS  PubMed  Google Scholar 

  • 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 37:5305–5311

    Article  CAS  PubMed  Google Scholar 

  • 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 20:1387–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 271:17875–17880

    Article  CAS  PubMed  Google Scholar 

  • Vetsigian K, Woese C, Goldenfeld N (2006) Collective evolution and the genetic code. Proc Natl Acad Sci USA 103:10696–10701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 157:2808–2817

    Article  CAS  PubMed  Google Scholar 

  • Vogel G (1998) Tracking the history of the genetic code. Science 281:329–331

    Article  CAS  PubMed  Google Scholar 

  • 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 80:49–63

    Article  CAS  PubMed  Google Scholar 

  • von Heijne G, Gavel Y (1988) Topogenic signals in integral membrane proteins. Eur J Biochem 174:671–678

    Article  Google Scholar 

  • 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 11:765–777

    Article  CAS  PubMed  Google Scholar 

  • Wahl MC, Bourenkov GP, Bartunik HD, Huber R (2000) Flexibility, conformational diversity and two dimerization modes in complexes of ribosomal protein L12. EMBO J 19:174–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:945–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh CT (1979) Enzymatic reaction mechanisms. WH Freeman, San Francisco

    Google Scholar 

  • 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 19:700–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Deng Z, Kemp RG (1998) An essential methionine residue involved in substrate binding by phosphofructokinases. Biochem Biophys Res Commun 250:466–468

    Article  CAS  PubMed  Google Scholar 

  • 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 315:171–182

    Article  CAS  PubMed  Google Scholar 

  • 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 33:9333–9342

    Article  CAS  PubMed  Google Scholar 

  • Wierenga RK, Kapetaniou EG, Venkatesan R (2010) Triosephosphate isomerase: a highly evolved biocatalyst. Cell Mol Life Sci 67:3961–3982

    Article  CAS  PubMed  Google Scholar 

  • Williams KA, Deber CM (1991) Proline residues in transmembrane helices: structural or dynamic role? Biochemistry 30:8919–8923

    Article  CAS  PubMed  Google Scholar 

  • 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 41:3861–3869

    Article  CAS  PubMed  Google Scholar 

  • Woese CR (1965) On the evolution of the genetic code. Proc Natl Acad Sci USA 54:1546–1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR, Dugre DH, Saxinger WC, Dugre SA (1966) The molecular basis for the genetic code. Proc Natl Acad Sci USA 55:966–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong JT (1975) A co-evolution theory of the genetic code. Proc Natl Acad Sci USA 72:1909–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong JT (1988) Evolution of the genetic code. Microbiol Sci 5:174–181

    CAS  PubMed  Google Scholar 

  • Wotring VE, Miller TS, Weiss DS (2003) Mutations at the GABA receptor selectivity filter: a possible role for effective charges. J Physiol 548(Pt2):527–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu WJ, Raleigh DP (1998) Local control of peptide conformation: stabilization of cis proline peptide bonds by aromatic proline interactions. Biopolymers 45:381–394

    Article  CAS  PubMed  Google Scholar 

  • 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 213:687–703

    Article  CAS  PubMed  Google Scholar 

  • Xue S, Calvin K, Li H (2006) RNA recognition and cleavage by a splicing endonuclease. Science 312:906–910

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Lee JY, Nowotny M (2006) Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol Cell 22:5–13

    Article  CAS  PubMed  Google Scholar 

  • 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 286:37503–37514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 243:754–766

    Article  CAS  PubMed  Google Scholar 

  • Yarus M, Widmann JJ, Knight R (2009) RNA-amino acid binding: a stereochemical era for the genetic code. J Mol Evol 69:406–429

    Article  CAS  PubMed  Google Scholar 

  • Yau WM, Wimley WC, Gawrisch K, White SH (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37:14713–14718

    Article  CAS  PubMed  Google Scholar 

  • Yin YW, Steitz TA (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase. Science 298:1387–1395

    Article  CAS  PubMed  Google Scholar 

  • 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 101:957–963

    Article  CAS  Google Scholar 

  • 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 584:342–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 329:182–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 40:474–482

    Article  CAS  PubMed  Google Scholar 

  • 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 486:130–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 126:5690–5698

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman SA, Ferry JG (2006) Proposal for a hydrogen bond network in the active site of the prototypic γ-class carbonic anhydrase. Biochemistry 45:5149–5157

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brian R. Francis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 214 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Francis, B.R. Evolution of the Genetic Code by Incorporation of Amino Acids that Improved or Changed Protein Function. J Mol Evol 77, 134–158 (2013). https://doi.org/10.1007/s00239-013-9567-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-013-9567-y

Keywords

Navigation