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Molecular anatomy: Phyletic relationships derived from three-dimensional structures of proteins

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Summary

A distance measure that reflects the dissimilarity among structures has been developed on the basis of the three-dimensional structures of similar proteins, this being totally independent of sequence in the sense that only the relative spatial positions of mainchain alpha-carbon atoms need be known. This procedure leads to phyletic relationships that are in general correlated with the sequence phylogenies based on residue type. Such relationships among known protein three-dimensional structures are also a useful aid to their classification and selection in knowledge-based modeling using homologous structures. We have applied this approach to six homologous sets of proteins: immunoglobulin fragments, globins, cytochromesc, serine proteinases, eye-lens gamma crystallins, and dinucleotide-binding domains.

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References

  • Ambler RP, Meyer TE, Kamen MD, Schichman SA, Sawyer L (1981) A reassessment of the structure ofParacoccus cytochromec-550. J Mol Biol 147:351–356

    Article  PubMed  Google Scholar 

  • Argos P, Hanei M, Wilson JM, Kelley WN (1983) A possible nucleotide-binding domain in the tertiary fold of phosphoribosyltransferases. J Biol Chem 25:6450–6457

    Google Scholar 

  • Arutyunyan ÉG, Kuranova IP, Vainshtein BK, Steigemann W (1980) X-ray structural investigation of leghemoglobin VI. Structure of acetate-ferrileghemoglobin at a resolution of 2.0 A. Krystallografiya 25:80–103

    Google Scholar 

  • Bajaj M, Blundell T (1984) Evolution and the tertiary structure of proteins. Annu Rev Biophys Bioeng 13:453–492

    Article  PubMed  Google Scholar 

  • Baldwin JM (1980) The structure of human carbonmonoxy haemoglobin at 2.7 Å resolution. J Mol Biol 136:103–128

    Article  PubMed  Google Scholar 

  • Barker WC, Ketcham LK, Dayhoff MO (1978) Immunoglobulins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation. Washington DC, pp 197–227

    Google Scholar 

  • Bernstein FC, Koetzle TF, Williams GJB, Meyer eF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The Protein Data Bank: a computer based archival file for macromolecular structures. J Mol Biol 112:535–542

    PubMed  Google Scholar 

  • Birktoft JJ, Banaszak LJ (1983) The presence of a histidineaspartic acid pair in the active site 2-hydroxyacid dehydrogenases. X-ray refinement of cytoplasmic malate dehydrogenase. J Bio. Chem 258:472–482

    Google Scholar 

  • Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow G (1981) The molecular structure and stability of the eye lens: x-ray analysis of gamma-crystallin II. Nature 289:771–777

    PubMed  Google Scholar 

  • Blundell T, Carney D, Gardner S, Hayes F, Howlin B, Hubbard T, Overington J, Singh DA, Sibanda BL, Sutcliffe M (1988a) Knowledge-based protein modelling and design. Eur J Biochem 172:513–520

    Article  PubMed  Google Scholar 

  • Blundell TL, Elliot G, Gardner SP, Hubbard T, Islam I, Johnson M, Mantafounis D, Murray-Rust P, Overington J, Pitts JE, Šali A, Sibanda BL, Singh J, Sternberg MJE, Sutcliffe MJ, Thornton JM, Travers P (1988b) Protein engineering and design. Phil Trans R Soc Lond, series B (in press)

  • Bode W, Chen Z, Bartels K, Kutzbach C, Schmidt-Kastner G, Bartunik H (1983) Refined 2 Å x-ray crystal structure of porcine pancreatic kallikrein A, a specific trypsin-like serine proteinase. Crystallization, structure determination, crystallographic refinement, structure and its comparison with bovine trypsin. J Mol Biol 164:237–282

    Article  PubMed  Google Scholar 

  • Bolton W, Perutz MF (1970) Three dimensional Fourier synthesis of horse deoxyhaemoglobin at 2.8 Å resolution. Nature 228:551–552

    PubMed  Google Scholar 

  • Brändén C-I, Schneider G, Lindqvist Y, Andersson I, Knight S, Lorimer G (1987) Structural and evolutionary aspects of the key enzymes in photorespiration; RuBisCO and glycolate oxidase. Cold Spring Harbor Symp Quant Biol LII:491–498

    Google Scholar 

  • Buehner M, Ford GC, Moras D, Olsen KW, Rossmann MG (1973) D-glyceraldehyde-3-phosphate dehydrogenase: three dimensional structure and evolutionary significance. Proc Natl Acad Sci USA 70:3052–3054

    PubMed  Google Scholar 

  • Carter DC, Melis KA, O'Donnell SE, Burgess BK, Furey WF, Wang B-C, Stout CD (1985) Crystal structure ofAzotobacter cytochromec 5 at 2.5 Å resolution. J Mol Biol 184:279–295

    Article  PubMed  Google Scholar 

  • Cederlund E, Lindqvist Y, Söderlund G, Brändén C-I, Jörnvall H (1988) Primary structure of glycolate oxidase from spinach. Eur J Biochem 173:523–530

    PubMed  Google Scholar 

  • Chothia, C, Lesk AM (1982) Evolution of proteins formed by β-sheets: I. Plastocyanin and azurin. J Mol Biol 160:309–323

    Article  PubMed  Google Scholar 

  • Chothia C, Lesk AM (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5:823–826

    PubMed  Google Scholar 

  • Crippen GM (1977) A novel approach to calculation of conformation: distance geometry. J Comp Physiol 24:96–107

    Google Scholar 

  • Deisenhofer J (1981). Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A fromStaphylococcus aureus at 2.9- and 2.8-Å resolution. Biochemistry 20:2361–2370

    PubMed  Google Scholar 

  • Dickerson RE (1971) The structure of cytochromec and the rates of molecular evolution. J Mol Evol 1:26–45

    Article  PubMed  Google Scholar 

  • Dickerson RE, Timkovitch R, almassy RJ (1976) The cytochrome fold and the evolution of bacterial energy metabolism. J Mol Biol 100:473–491

    PubMed  Google Scholar 

  • Doolittle RF (1979) Protein evolution. In: Neurath H, Hill RL (eds) The proteins, vol IV, ed 3. Academic Press, New York, pp 1–118

    Google Scholar 

  • Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry?. Science 214:149–159

    PubMed  Google Scholar 

  • Eklund H, Nordström B, Zeppezauer E, Söderlund G, Ohlsson I, Boiwe T, Söderberg B-O, Tapia O, Brändén C-I, Ekeson E (1976) Three-dimensional structure of horse liver alcohol dehydrogenase at 2.4 Å resolution. J Mol Biol 102:27–59

    PubMed  Google Scholar 

  • Epp O, Lattman EE, Schiffer M, Huber R, Palm W (1975) The molecular structure of a dimer composed of the Bence-Jones protein Rei refined at 2.0 Å resolution. Biochemistry 14:4943–4952

    Article  PubMed  Google Scholar 

  • Eventoff W, Rossmann MG (1975) The evolution of dehydrogenases and kinases. CRC Crit Rev Biochem 3:111–140

    PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Feng D-F, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25: 351–360

    PubMed  Google Scholar 

  • Feng D-F, Johnson MS, Doolittle RF (1985) Aligning amino acid sequences: comparison of commonly used methods. J Mol Evol 21:112–125

    Article  Google Scholar 

  • Fermi G, Perutz M, Shaanan B, Fourme R (1984) The crystal structure of human deoxyhaemoglobin at 1.74 Å resolution. J Mol Biol 175:159–174

    Article  PubMed  Google Scholar 

  • Ferro DR, Hermans J (1977) A different best rigid-body molecular fit routine. Acta Crystallogr A33:345–347

    Article  Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 15:279–284

    Google Scholar 

  • Fredman ML (1984) Computing evolutionary similarity measures with length independent gap penalties. Bull Math Biol 46:553–566

    Article  Google Scholar 

  • Frier JA, Perutz MF (1977) Structure of human foetal deoxyhaemoglobin. J Mol Biol 112:97–112

    PubMed  Google Scholar 

  • Fujinaga M, James MNG (1987) Rat submaxillary gland protease, tonin. Structure solution and refinement at 1.8 Å resolution. J Mol Biol 195:373–396

    Article  PubMed  Google Scholar 

  • Fujinaga M, Delbaere LTJ, Brayer GD, James MNG (1985) Refined structure ofα-lytic proteinase at 1.7 Å resolution. Analysis of hydrogen bonding and solvent structure. J Mol Biol 184:479–502

    Article  PubMed  Google Scholar 

  • Furey W, Wang BC, Yoo CS, Sax M (1983) Structure of a novel Bence-Jones protein (Rhe) fragment at 1.6 Å resolution. J Mol Biol 167:661–692

    PubMed  Google Scholar 

  • Girling RL, Houston TE, Schmidt WC, Amma EL (1980) Macromolecular structure refinement by restrained least-squares and interactive graphics as applied to sickling deer type III hemoglobin. Acta Crystallogr A36:43–50

    Article  Google Scholar 

  • Goodman M, Moore GW, Masuda G (1975) Darwinian evolution in the genealogy of haemoglobin. Nature 253:603–608

    Article  PubMed  Google Scholar 

  • Haser R, Pierrot M, Frey M, Payan F, Astier JP, Bruschi M, Le Gall J (1979) Structure and sequence of the multihaem cytochromec 3. Nature 282:806–810

    Article  PubMed  Google Scholar 

  • Higuchi Y, Kusunoki M, Matsuura Y, Yasuoka N, Kakudo M (1984) Refined structure of cytochromec 3 at 1.8 Å resolution. J Mol Biol 172:109–139

    Article  PubMed  Google Scholar 

  • Honzatko RB, Hendrickson WA, Love WE (1985) Refinement of a molecular model for lamprey hemoglobin fromPetromyzon marinus J Mol Biol 184:147–164

    Article  PubMed  Google Scholar 

  • Hotelling H (1933) Analysis of a complex of statistical variables into principal components. J Educ Psychol 24:417–441

    Google Scholar 

  • Hubbard TJP, Blundell TL (1987) Comparison of solvent-inaccessible cores of homologous proteins: definitions useful for protein modelling. Protein Eng 1:159–171

    PubMed  Google Scholar 

  • Hunt LT, Hurst-Calderone S, Dayhoff MO (1978) Globins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation. Washington DC, pp 229–249

    Google Scholar 

  • James MNG, Sielecki AR, Brayer GD, Delbaere LTJ, Bauer C-A (1980) Structures of product and inihibitor complexes ofStreptomyces griseus protease A at 1.8 Å resolution. A model for serine proteinase catalysis. J Mol Biol 144:43–88

    Article  PubMed  Google Scholar 

  • Jennings A (1978) Matrix computations for engineers and scientists. John Wiley and Sons, Chichester

    Google Scholar 

  • Kabsch W (1978) A discussion of the solution for the best rotation to relate two sets of vectors. Acta Crystallogr A34: 827–828

    Article  Google Scholar 

  • Kenknight CE (1984) Comparison of methods of matching protein structures. Acta Crystallogr A40:708–712

    Article  Google Scholar 

  • Kernighan BW, Ritchie DM (1978) The C programming language. Prentice-Hall, Englewoods Cliffs NJ

    Google Scholar 

  • Kortt AA, Burns JE, Trinick MJ, Appleby CA (1985) The amino acid sequence of hemoglobin I fromParasponia andersonii, a nonleguminous plant. FEBS Lett 180:55–60

    Article  Google Scholar 

  • Lazure C, Leduc C, Seidah NG, Thilbault G, Genest J, Chritien M (1984) Amino acid similarity of rat submaxillary tonin reveals similarities to serine proteases. Nature 307:555–558

    Article  PubMed  Google Scholar 

  • Lesk AM, Chothia C (1980) How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins. J Mol Biol 136: 225–270

    Article  PubMed  Google Scholar 

  • Lesk AM, Chothia C (1982) Evolution of proteins formed by β-sheets. II. The core of the immunoglobulin domains. J Mol Biol 160:325–342

    Article  PubMed  Google Scholar 

  • Leunissen JAM, de Jong WW (1986) Phylogenetic trees constructured from the hydrophobic values of protein sequences. J Theor Biol 119:189–196

    PubMed  Google Scholar 

  • Marquart M, Deisenhofer J, Huber R, Palm W (1980) Crystallographic refinement and atomic models of the intact immunoglobulin molecule Kol and its antigen-binding fragment at 3.0 Å and 1.9 Å resolution. J Mol Biol 141:369–391

    Article  PubMed  Google Scholar 

  • Matsuura Y, Takano T, Kickerson RE (1982) Structure of cytochromec 551 fromP. aeruginosa refined at 1.6 Å resolution and comparison of the two redox forms. J Mol Biol 156:389–409

    Article  PubMed  Google Scholar 

  • Matthews BW, Rossmann MG (1985) Comparison of protein structures. Methods Enzymol 115:397–420

    PubMed  Google Scholar 

  • McLachlan AD (1979) Gene duplications in the structural evolution of chymotrypsin. J Mol Biol 128:49–79

    Article  PubMed  Google Scholar 

  • McLachlan AD (1982) Rapid comparison of protein structures, Acta Crystallogr A34:871–873

    Article  Google Scholar 

  • Meyer E, Cole G, Radahakrishnan R, Epp O (1988) Structure of native porcine pancreatic elastase at 1.65 Å resolution. Acta Crystallogr B44:26–38

    Article  PubMed  Google Scholar 

  • Moras D, Olsen KW, Sabesan MN, Buehner M, Ford GC, Rossmann MG (1975) Studies of the asymmetry in the three dimensional structure of lobster D-glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 250:9137–9162

    PubMed  Google Scholar 

  • Needleman SA, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    Article  PubMed  Google Scholar 

  • Ochi H, Hata Y, Tanaka N, Kanudo M, Sakurai T, Aihara S, Morita Y (1983) Structure of rice ferricytochromec at 2.0 Å resolution. J Mol Biol 166:407–418

    PubMed  Google Scholar 

  • Ohlsson I, Nordström B, Brändén C-I (1974) Structural and functional similarities within the coenzyme binding domains of dehydrogenases. J Mol Biol 89:339–354

    Article  PubMed  Google Scholar 

  • Padlan EA, Love WE (1985) Refined crystal structure of deoxyhemoglobin S. I. Restrained least-squares refinement at 3.0-Å resolution. J Biol Chem 260:8272–8279

    PubMed  Google Scholar 

  • Pai EF, Karplus PA, Schulz GE (1988) Crystallographic analysis of the binding of NADPH, NADPH fragments, and NADPH analogues to glutathione reductase. Biochemistry 27:4465–4474

    Article  PubMed  Google Scholar 

  • Pierrot M, Haser R, Frey M, Payan F, Astier J-P (1982) Crystal structures and electron transfer properties of cytochromec 3. J Biol Chem 257:14341–14348

    PubMed  Google Scholar 

  • Rao ST, Rossmann MG (1973) Comparison of super-secondary structures in proteins. J Mol Biol 76:241–256

    Article  PubMed  Google Scholar 

  • Read RJ, James MNG (1988) Refined crystal structure ofStreptomyces griseus trypsin at 1.7 Å resolution. J Mol Biol 200: 523–551

    Article  PubMed  Google Scholar 

  • Reynolds RA, Remington SJ, Weaver LH, Fisher RG, Anderson WF, Ammon HL, Matthews BW (1985) Structure of a serine protease from rat mast cells determined from twinned crystals by isomorphous and molecular replacement. Acta Crystallogr B41:139–147

    Article  Google Scholar 

  • Richardson JS (1977) β-sheet topology and the relatedness of proteins. Nature 268:495–500

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Salemme FR, Freer ST, Xuong NH, Alden RA, Kraut J (1973) The structure of oxidized cytochromec 2 ofRhodospirillum rubrum. J Biol Chem 248:3910–3921

    PubMed  Google Scholar 

  • Šali A, Turk V (1987) Prediction of the secondary structures of stefins and cystatins, the low-molecular mass protein inhibitors of cysteine proteinases. Biol Chem Hoppe-Seyler 368: 493–499

    PubMed  Google Scholar 

  • Saul FA, Amzel LM, Poljack RJ (1978) Preliminary refinement and structural analysis of the FAB fragment from human immunoglobulin NEW at 2.0 Å resolution. J Biol Chem 253: 585–597

    PubMed  Google Scholar 

  • Schreuder HA, van der Laan JM, Hol WGT, Drenth J (1988) Crystal structure ofp-hydroxybenzoate hydroxylase complexed with its reaction product. J Mol Biol 199:637–648

    Article  PubMed  Google Scholar 

  • Schulz GE, Schirmer RH, Sachsenheimer W, Pai EF (1978) The structure of the flavoenzyme glutathione reductase. Nature 273:120–124

    Article  PubMed  Google Scholar 

  • Schwartz RM, Dayhoff MO (1978) Cytochromes. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation. Washington DC, pp 29–44

    Google Scholar 

  • Shaanan B (1983) Structure of human oxyhaemoglobin at 2.1 Å resolution. J Mol Biol 171:31–59

    PubMed  Google Scholar 

  • Steigemann W, Weber E (1979) Structure of erythrocruorin in different ligand states refined at 1.4 Å resolution. J Mol Biol 127:309–338

    Article  PubMed  Google Scholar 

  • Sutcliffe MJ, Haneef I, Carney D, Blundell TL (1987a) Knowledge based modelling of homologous proteins, part I: threedimensional frameworks derived from simultaneous superposition of multiple structures. Protein Eng 1:377–384

    PubMed  Google Scholar 

  • Sutcliffe MJ, Hayes FRF, Blundell TL (1987b) Knowledgebased modelling of homologous proteins, part II: rules for the conformations of substituted sidechains. Protein Eng 1:385–392

    PubMed  Google Scholar 

  • Takano T (1977) Structure of myoglobin at 2.0 Å resolution, II. Structure of deoxymyoglobin from sperm whale. J Mol Biol 110:569–584

    PubMed  Google Scholar 

  • Takano T, Dickerson RE (1981a) Conformational changes of cytochromec. I. Ferrocytochromec structure refined at 1.5 Å resolution. J Mol Biol 153:79–94

    Article  PubMed  Google Scholar 

  • Takano T, Dickerson RE (1981b) Conformational changes of cytochromec. II. Ferricytochromec refinement at 1.8 Å resolution and comparison with the ferrocytochrome structure. J Mol Biol 153:95–115

    Article  PubMed  Google Scholar 

  • Thieme R, Pai EF, Schirmer RH, Schulz GE (1981) Threedimensional structure of glutathione reductase at 2 Å resolution. J Mol Biol 152:763–782

    Article  PubMed  Google Scholar 

  • Thorndike RM (1978) Correlation procedures for research. Gardner Press, New York, pp 1–340

    Google Scholar 

  • Timkovich R, Dickerson RE (1976) The structure ofParacoccus denitrificans cytochromec 550. J Biol Chem 251:4033–4046

    PubMed  Google Scholar 

  • Tsukada H, Blow DM (1985) Structure ofα-chymotrypsin refined at 1.68 Å resolution. J Mol Biol 184:703–711

    Article  PubMed  Google Scholar 

  • Wakabayashi S, Matsubara H, Webster DA (1986) Primary sequence of a dimeric bacterial hemoglobin fromVitreoscilla. Nature 322:481–483

    Article  PubMed  Google Scholar 

  • Walter J, Steigemann W, Singh JP, Bartunik H, Bode W, Huber R (1982) On the disordered activation domain in trypsinogen. Chemical labelling and low-temperature crystallography. Acta Crystallogr B38:1462–1472

    Article  Google Scholar 

  • White, JL, Hackert ML, Buehner M, Adams MJ, Ford GC, Lentz PJ, Smiley IE, Steindel SJ, Rossmann MG (1976) A comparison of the structures of apo dogfish M4 lactate dehydrogenase and its ternary complexes. J Mol Biol 102:759–779

    Article  PubMed  Google Scholar 

  • White HE, Driessen HPC, Slingsby C, Moss DS, Turnell WG, Lindley PF, (1988a) The use of pseudosymmetry in the rotation function of γIVa-crystallin. Acta Crystallogr B44:172–178

    Article  PubMed  Google Scholar 

  • White HE, Driessen HPC, Slingsby C, Moss DS, Lindley PF (1988b) Packing interactions in the eye-lens: structural analysis, internal symmetry and lattice interactions of bovine gamma-IVa crystallin. J Mol Biol 207:217–235

    Article  Google Scholar 

  • Wierenga RK, Drenth J, Schulz GE (1983) Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain ofp-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase. J Mol Biol 167:725–739

    PubMed  Google Scholar 

  • Wierenga RK, De Maeyer MCH, Hol WGJ (1985) Interactions of pyrophosphate moieties withα-helices in dinucleotide binding proteins. Biochemistry 24:1346–1357

    Article  Google Scholar 

  • Wierenga RK, Terpstra P, Hol WG (1986) Prediction of the occurrence of the ADP βαβ-fold in proteins, using amino acid fingerprints. J Mol Biol 187:101–107

    Article  PubMed  Google Scholar 

  • Wistow G, Turnell B, Summers L, Slingsby C, Moss D, Miller L, Lindley P, Blundell T (1983) X-ray analysis of the eye lens protein gamma-II crystallin at 1.9 Å resolution. J Mol Biol 170:175–202

    PubMed  Google Scholar 

  • Young CL, Barker WC, Tomaselli CM, Dayhoff MO (1978) Serine proteases. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington DC, pp 73–93

    Google Scholar 

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  1. Michael J. Sutcliffe

    Present address: Inorganic Chemistry Laboratory, University of Oxford, South Parks Road, OX1 3QR, Oxford, UK

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  1. Laboratory of Molecular Biology, Department of Crystallography, Birkbeck College, University of London, WC1E 7HX, London, UK

    Mark S. Johnson, Michael J. Sutcliffe & Tom L. Blundell

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Johnson, M.S., Sutcliffe, M.J. & Blundell, T.L. Molecular anatomy: Phyletic relationships derived from three-dimensional structures of proteins. J Mol Evol 30, 43–59 (1990). https://doi.org/10.1007/BF02102452

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