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Analyses of cobalt–ligand and potassium–ligand bond lengths in metalloproteins: trends and patterns

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Abstract

Cobalt and potassium are biologically important metal elements that are present in a large array of proteins. Cobalt is mostly found in vivo associated with a corrin ring, which represents the core of the vitamin B12 molecule. Potassium is the most abundant metal in the cytosol, and it plays a crucial role in maintaining membrane potential as well as correct protein function. Here, we report a thorough analysis of the geometric properties of cobalt and potassium coordination spheres that was performed with high resolution on a representative set of structures from the Protein Data Bank and complemented by quantum mechanical calculations realized at the DFT level of theory (B3LYP/ SDD) on mononuclear model systems. The results allowed us to draw interesting conclusions on the structural characteristics of both Co and K centers, and to evaluate the importance of effects such as their association energies and intrinsic thermodynamic stabilities. Overall, the results obtained provide useful data for enhancing the atomic models normally applied in theoretical and computational studies of Co or K proteins performed at the quantum mechanical level, and for developing molecular mechanical parameters for treating Co or K coordination spheres in molecular mechanics or molecular dynamics studies.

Cobalt and potassium are biologically crucial metals that are present in a wide array of proteins. Here, a thorough analysis was performed of the geometric properties of Co and K coordination spheres and quantum mechanical calculations on mononuclear model systems. These results can be employed to enhance atomic QM models applied to the theoretical study of Co or K proteins, and to develop molecular mechanical parameters for use in molecular mechanics studies

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References

  1. Harding MM, Nowicki MW, Walkinshaw MD (2010) Metals in protein structures: a review of their principal features. Crystallogr Rev 16:247–302. doi:10.1080/0889311X.2010.485616

    Article  CAS  Google Scholar 

  2. Maret W (2010) Metalloproteomics, metalloproteomes, and the annotation of metalloproteins. Metallomics 2:117–125. doi:10.1039/B915804A

    Article  CAS  Google Scholar 

  3. Yamashita MM, Wesson L, Eisenman G, Eisenberg D (1990) Where metal ions bind in proteins. Proc Natl Acad Sci USA 87:5648–5652. doi:10.1073/pnas.87.15.5648

  4. Harding MM (2006) Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr D 62:678–682. doi:10.1107/S0907444906014594

  5. Dokmanić I, Šikić M, Tomić S (2008) Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination. Acta Crystallogr D 64:257–263. doi:10.1107/S090744490706595X

  6. Zheng H, Chruszcz M, Lasota P, Lebioda L, Minor W (2008) Data mining of metal ion environments present in protein structures. J Inorg Biochem 102:1765–1776. doi:10.1016/j.jinorgbio.2008.05.006

    Article  CAS  Google Scholar 

  7. Tamames JAC, Ramos MJ (2011) Metals in proteins: cluster analysis studies. J Mol Model 17:429–442. doi:10.1007/s00894-010-0733-5

    Article  CAS  Google Scholar 

  8. Tamames B, Sousa SF, Tamames J, Fernandes PA, Ramos MJ (2007) Analysis of zinc–ligand bond lengths in metalloproteins: trends and patterns. Proteins 69:466–475. doi:10.1002/prot.21536

  9. Sousa SF, Lopes AB, Fernandes PA, Ramos MJ (2009) The zinc proteome: a tale of stability and functionality. Dalton Trans 7946–7956. doi:10.1039/B904404C

  10. Abriata LA (2013) Investigation of non-corrin cobalt(II)-containing sites in protein structures of the Protein Data Bank. Acta Crystallogr B 69:176–183. doi:10.1107/S2052519213002959

  11. Harding MM (2002) Metal–ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr D 58:872–874. doi:10.1107/S0907444902003712

  12. Berman H, Henrick K, Nakamura H, Markley JL (2007) The Worldwide Protein Data Bank (wwPDB): ensuring a single, uniform archive of PDB data. Nucleic Acids Res 35:D301–D303. doi:10.1093/nar/gkl971

  13. Allen FH (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr B 58:380–388. doi:10.1107/S0108768102003890

  14. Hsin K, Sheng Y, Harding MM, Taylor P, Walkinshaw MD (2008) MESPEUS: a database of the geometry of metal sites in proteins. J Appl Crystallogr 41:963–968. doi:10.1107/S002188980802476X

    Article  CAS  Google Scholar 

  15. Hemavathi K, Kalaivani M, Udayakumar A, Sowmiya G, Jeyakanthan J, Sekar K (2009) MIPS: metal interactions in protein structures. J Appl Crystallogr 43:196–199. doi:10.1107/S002188980903982X

    Article  Google Scholar 

  16. Tus A, Rakipovic A, Peretin G, Tomic S, Sikic M (2012) BioMe: biologically relevant metals. Nucleic Acids Res 40:W352–W357. doi:10.1093/nar/gks514

    Article  CAS  Google Scholar 

  17. Karlin S, Zhu Z-Y, Karlin KD (1997) The extended environment of mononuclear metal centers in protein structures. Proc Natl Acad Sci USA 94:14225–14230

  18. Irving H, Williams RJP (1953) The stability of transition-metal complexes. J Chem Soc 3192–3210. doi:10.1039/JR9530003192

  19. Brown KL (2005) Chemistry and enzymology of vitamin B12. Chem Rev 105:2075–2150. doi:10.1021/cr030720z

    Article  CAS  Google Scholar 

  20. Randaccio L, Geremia S, Demitri N, Wuerges J (2010) Vitamin B12: unique metalorganic compounds and the most complex vitamins. Molecules 15:3228–3259. doi:10.3390/molecules15053228

  21. Clardy SM, Allis DG, Fairchild TJ, Doyle RP (2011) Vitamin B12 in drug delivery: breaking through the barriers to a B12 bioconjugate pharmaceutical. Expert Opin Drug Deliv 8:127–140. doi:10.1517/17425247.2011.539200

    Article  CAS  Google Scholar 

  22. Kobayashi M, Shimizu S (1999) Cobalt proteins. Eur J Biochem 261:1–9. doi:10.1046/j.1432-1327.1999.00186.x

    Article  CAS  Google Scholar 

  23. Payne LR (1977) The hazards of cobalt. Occup Med 27:20–25. doi:10.1093/occmed/27.1.20

    Article  CAS  Google Scholar 

  24. Tower SS (2012) Arthroprosthetic cobaltism associated with metal on metal hip implants. BMJ 344:e430–e430. doi:10.1136/bmj.e430

    Article  Google Scholar 

  25. Abriata LA, González LJ, Llarrull LI, Tomatis PE, Myers WK, Costello AL, Tierney DL, Vila AJ (2008) Engineered mononuclear variants in Bacillus cereus metallo-β-lactamase BcII are inactive. Biochemistry (Mosc) 47:8590–8599. doi:10.1021/bi8006912

  26. Llarrull LI, Tioni MF, Vila AJ (2008) Metal content and localization during turnover in B. cereus metallo-β-lactamase. J Am Chem Soc 130:15842–15851. doi:10.1021/ja801168r

  27. Maret W, Vallee B (1993) Cobalt as probe and label of proteins. Methods Enzymol 226:52–71

    Article  CAS  Google Scholar 

  28. Bhosale SH, Rao MB, Deshpande VV (1996) Molecular and industrial aspects of glucose isomerase. Microbiol Rev 60:280–300

    CAS  Google Scholar 

  29. Page MJ, Cera ED (2006) Role of Na+ and K+ in enzyme function. Physiol Rev 86:1049–1092. doi:10.1152/physrev.00008.2006

  30. Cera ED (2006) A structural perspective on enzymes activated by monovalent cations. J Biol Chem 281:1305–1308. doi:10.1074/jbc.R500023200

    Article  Google Scholar 

  31. Harding MM (2001) Geometry of metal–ligand interactions in proteins. Acta Crystallogr D 57:401–411. doi:10.1107/S0907444900019168

  32. Shibata N, Masuda J, Tobimatsu T, Toraya T, Suto K, Morimoto Y (1993) Yasuoka N (1999) A new mode of B12 binding and the direct participation of a potassium ion in enzyme catalysis: X-ray structure of diol dehydratase. Struct Lond Engl 7:997–1008

  33. Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on the univalent cations. Annu Rev Plant Physiol 17:47–76. doi:10.1146/annurev.pp. 17.060166.000403

    Article  CAS  Google Scholar 

  34. Andersson CE, Mowbray SL (2002) Activation of ribokinase by monovalent cations. J Mol Biol 315:409–419. doi:10.1006/jmbi.2001.5248

    Article  CAS  Google Scholar 

  35. Ahmad A, Akhtar MS, Bhakuni V (2001) Monovalent cation-induced conformational change in glucose oxidase leading to stabilization of the enzyme. Biochemistry (Mosc) 40:1945–1955

    Article  CAS  Google Scholar 

  36. Babu CS, Dudev T, Casareno R, Cowan JA, Lim C (2003) A combined experimental and theoretical study of divalent metal ion selectivity and function in proteins: application to E. coli ribonuclease H1. J Am Chem Soc 125:9318–9328. doi:10.1021/ja034956w

  37. Ryde U (2007) Accurate metal-site structures in proteins obtained by combining experimental data and quantum chemistry. Dalton Trans 607–625. doi:10.1039/B614448A

  38. Brás NF, Fernandes PA, Ramos MJ (2010) QM/MM studies on the β-galactosidase catalytic mechanism: hydrolysis and transglycosylation reactions. J Chem Theory Comput 6:421–433. doi:10.1021/ct900530f

  39. Alberto ME, Marino T, Ramos MJ, Russo N (2010) Atomistic details of the catalytic mechanism of Fe(III)–Zn(II) purple acid phosphatase. J Chem Theory Comput 6:2424–2433. doi:10.1021/ct100187c

  40. Ribeiro AJM, Ramos MJ, Fernandes PA (2012) The catalytic mechanism of HIV-1 integrase for DNA 3′-end processing established by QM/MM calculations. J Am Chem Soc 134:13436–13447. doi:10.1021/ja304601k

  41. Ramos MJ, Fernandes PA (2008) Computational enzymatic catalysis. Acc Chem Res 41:689–698. doi:10.1021/ar7001045

    Article  CAS  Google Scholar 

  42. Sousa SF, Fernandes PA, Ramos MJ (2009) The search for the mechanism of the reaction catalyzed by farnesyltransferase. Chem Eur J 15:4243–4247. doi:10.1002/chem.200802745

  43. Blomberg MRA, Borowski T, Himo F, Liao R-Z, Siegbahn PEM (2014) Quantum chemical studies of mechanisms for metalloenzymes. Chem Rev (in press). doi:10.1021/cr400388t

  44. Román-Meléndez GD, von Glehn P, Harvey JN, Mulholland AJ, Marsh ENG (2014) Role of active site residues in promoting cobalt–carbon bond homolysis in adenosylcobalamin-dependent mutases revealed through experiment and computation. Biochemistry (Mosc) 53:169–177. doi:10.1021/bi4012644

    Article  Google Scholar 

  45. Zhu X, Teng M, Niu L, Xu C, Wang Y (1999) Structure of xylose isomerase from Streptomyces diastaticus no. 7 strain M1033 at 1.85 Å resolution. Acta Crystallogr D 56:129–136. doi:10.1107/S0907444999015097

  46. Masuda J, Shibata N, Morimoto Y, Toraya T, Yasuoka N (2000) How a protein generates a catalytic radical from coenzyme B (12): X-ray structure of a diol-dehydratase-adeninylpentylcobalamin complex. Struct Fold Des 8:775–788. doi:10.1016/S0969-2126(00)00164-7

    Article  CAS  Google Scholar 

  47. Iverson TM, Alber BE, Kisker C, Ferry JG, Rees DC (1999) A closer look at the active site of gamma-class carbonic anhydrases: high-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. Biochemistry (Mosc) 39:9222–9231. doi:10.1021/bi000204s

  48. Hall PR, Zheng R, Antony L, Pusztai-Carey M, Carey PR, Yee VC (2003) Transcarboxylase 5S structures: assembly and catalytic mechanism of a multienzyme complex subunit. Embo J 23:3621–3631. doi:10.1038/sj.emboj.7600373

    Article  Google Scholar 

  49. Casares S, Lopez-Mayorga O, Vega MC, Camara-Artigas A, Conejero-Lara F (2005) Cooperative propagation of local stability changes from low-stability and high-stability regions in a SH3 domain. Proteins 67:531–547. doi:10.1002/prot.21284

    Article  Google Scholar 

  50. Svetlitchnaia T, Svetlitchnyi V, Meyer O, Dobbek H (2006) Structural insights into methyltransfer reactions of a corrinoid iron–sulfur protein involved in acetyl-CoA synthesis. Proc Natl Acad Sci USA 103:14331–14336. doi:10.1073/pnas.0601420103

  51. Flynn GE, Black KD, Islas LD, Sankaran B, Zagotta WN (2007) Structure and rearrangements in the carboxy-terminal region of SpIH channels. Structure 15:671–682. doi:10.1016/j.str.2007.04.008

    Article  CAS  Google Scholar 

  52. Palm GJ, Lederer T, Orth P, Saenger W, Takahashi M, Hillen W, Hinrichs W (2007) Specific binding of divalent metal ions to tetracycline and to the Tet repressor/tetracycline complex. J Biol Inorg Chem 13:1097. doi:10.1007/S00775-008-0395-2

    Article  Google Scholar 

  53. Puorger C, Eidam O, Capitani G, Erilov D, Grutter MG, Glockshuber R (2007) Infinite kinetic stability against dissociation of supramolecular protein complexes through donor strand complementation. Structure 16:631–642. doi:10.1016/j.str.2008.01.013

    Article  Google Scholar 

  54. Schlichting I, Jung C, Schulze H (1997) Crystal structure of cytochrome P-450cam complexed with the (1S)-camphor enantiomer. FEBS Lett 415:253–257. doi:10.1016/S0014-5793(97)01135-6

  55. Vanhooke JL, Thoden JB, Brunhuber NM, Blanchard JS, Holden HM (1998) Phenylalanine dehydrogenase from Rhodococcus sp. M4: high-resolution X-ray analyses of inhibitory ternary complexes reveal key features in the oxidative deamination mechanism. Biochemistry (Mosc) 38:2326–2339. doi:10.1021/bi982244q

  56. Thoden JB, Huang X, Raushel FM, Holden HM (1999) The small subunit of carbamoyl phosphate synthetase: snapshots along the reaction pathway. Biochemistry (Mosc) 38:16158–16166. doi:10.1021/bi991741j

    Article  CAS  Google Scholar 

  57. Mamat B, Roth A, Grimm C, Ermler U, Tziatzios C, Schubert D, Thauer RK, Shima S (2002) Crystal structures and enzymatic properties of three formyltransferases from archaea: environmental adaptation and evolutionary relationship. Protein Sci 11:2168–2178. doi:10.1110/ps.0211002

    Article  CAS  Google Scholar 

  58. Wolan DW, Cheong CG, Greasley SE, Wilson IA (2003) Structural insights into the human and avian IMP cyclohydrolase mechanism via crystal structures with the bound XMP inhibitor. Biochemistry (Mosc) 43:1171–1183. doi:10.1021/bi030162i

    Article  Google Scholar 

  59. Gan L, Seyedsayamdost M, Shuto S, Matsuda A, Petsko GA, Hedstrom L (2003) The immunosuppressive agent mizoribine monophosphate forms a transition state analogue complex with Inosine monophosphate dehydrogenase. Biochemistry (Mosc) 42:857–863. doi:10.1021/bi0271401

  60. Chaudhry C, Horwich AL, Brunger AT, Adams PD (2004) Exploring the structural dynamics of the E. coli chaperonin GroEL using translation-libration-screw crystallographic refinement of intermediate states. J Mol Biol 342:229–245. doi:10.1016/j.jmb.2004.07.015

  61. Morgunova E, Meining W, Illarionov B, Haase I, Jin G, Bacher A, Cushman M, Fischer M, Ladenstein R (2004) Crystal structure of lumazine synthase from Mycobacterium tuberculosis as a target for rational drug design: binding mode of a new class of purinetrione inhibitors. Biochemistry (Mosc) 44:2746. doi:10.1021/BI047848A

  62. Pioszak AA, Murayama K, Nakagawa N, Ebihara A, Kuramitsu S, Shirouzu M, Yokoyama S (2005) Structures of a putative RNA 5-methyluridine methyltransferase, Thermus thermophilus TTHA1280, and its complex with S-adenosyl-L-homocysteine. Acta Crystallogr F 61:867–874. doi:10.1107/S1744309105029842

  63. Blagova E, Levdikov V, Milioti N, Fogg MJ, Kalliomaa AK, Brannigan JA, Wilson KS, Wilkinson AJ (2004) Crystal structure of dihydrodipicolinate synthase (BA3935) from Bacillus anthracis at 1.94 Å resolution. Proteins 62:297–301. doi:10.1002/prot.20684

  64. Tocilj A, Schrag JD, Li Y, Schneider BL, Reitzer L, Matte A, Cygler M (2005) Crystal structure of N-succinylarginine dihydrolase AstB, bound to substrate and product, an enzyme from the arginine catabolic pathway of Escherichia coli. J Biol Chem 280:15800–15808. doi:10.1074/jbc.M413833200

  65. Nielsen TK, Hildmann C, Dickmanns A, Schwienhorst A, Ficner R (2005) Crystal structure of a bacterial class 2 histone deacetylase homologue. J Mol Biol 354:107–120. doi:10.1016/j.jmb.2005.09.065

    Article  CAS  Google Scholar 

  66. Satoh T, Sato K, Kanoh A, Yamashita K, Yamada Y, Igarashi N, Kato R, Nakano A, Wakatsuki S (2005) Structures of the carbohydrate recognition domain of Ca2+-independent cargo receptors Emp46p and Emp47p. J Biol Chem 281:10410–10419. doi:10.1074/jbc.M512258200

  67. Addlagatta A, Hu X, Liu JO, Matthews BW (2005) Structural basis for the functional differences between type I and type II human methionine aminopeptidases. Biochemistry (Mosc) 44:14741–14749. doi:10.1021/bi051691k

  68. May M, Mehboob S, Mulhearn DC, Wang Z, Yu H, Thatcher GRJ, Santarsiero BD, Johnson ME, Mesecar AD (2006) Structural and functional analysis of two glutamate racemase isozymes from Bacillus anthracis and implications for inhibitor design. J Mol Biol 371:1219–1237. doi:10.1016/j.jmb.2007.05.093

  69. Williams R, Holyoak T, McDonald G, Gui C, Fenton AW (2006) Differentiating a ligand’s chemical requirements for allosteric interactions from those for protein binding. Phenylalanine inhibition of pyruvate kinase. Biochemistry (Mosc) 45:5421–5429. doi:10.1021/bi0524262

  70. Scrima A, Wittinghofer A (2006) Dimerisation-dependent GTPase reaction of MnmE: how potassium acts as GTPase-activating element. Embo J 25:2940–2951. doi:10.1038/sj.emboj.7601171

    Article  CAS  Google Scholar 

  71. Huang LS, Shen JT, Wang AC, Berry EA (2006) Crystallographic studies of the binding of ligands to the dicarboxylate site of Complex II, and the identity of the ligand in the “oxaloacetate-inhibited” state. Biochim Biophys Acta 1757:1073–1083. doi:10.1016/j.bbabio.2006.06.015

  72. Christensen CE, Kragelund BB, Von Wettstein-Knowles P, Henriksen A (2006) Structure of the human beta-ketoacyl [Acp] synthase from the mitochondrial type II fatty acid synthase. Protein Sci 16:261. doi:10.1110/PS.062473707

  73. Morrison SD, Roberts SA, Zegeer AM, Montfort WR, Bandarian V (2007) A new use for a familiar fold: the X-ray crystal structure of GTP-bound GTP cyclohydrolase III from Methanocaldococcus jannaschii reveals a two metal ion catalytic mechanism. Biochemistry (Mosc) 47:230–242. doi:10.1021/bi701782e

  74. Bottomley MJ, Lo Surdo P, Di Giovine P, Cirillo A, Scarpelli R, Ferrigno F, Jones P, Neddermann P, De Francesco R, Steinkuhler C, Gallinari P, Carfi A (2008) Structural and functional analysis of the human Hdac4 catalytic domain reveals a regulatory zinc-binding domain. J Biol Chem 283:26694–26704. doi:10.1074/jbc.M803514200

  75. Brás NF, Moura-Tamames SA, Fernandes PA, Ramos MJ (2008) Mechanistic studies on the formation of glycosidase-substrate and glycosidase-inhibitor covalent intermediates. J Comput Chem 29:2565–2574. doi:10.1002/jcc.21013

    Article  Google Scholar 

  76. Brás NF, Perez MAS, Fernandes PA, Silva PJ, Ramos MJ (2011) Accuracy of density functionals in the prediction of electronic proton affinities of amino acid side chains. J Chem Theory Comput 7:3898–3908. doi:10.1021/ct200309v

  77. Liao R-Z, Yu J-G, Himo F (2011) Quantum chemical modeling of enzymatic reactions: the case of decarboxylation. J Chem Theory Comput 7:1494–1501. doi:10.1021/ct200031t

    Article  CAS  Google Scholar 

  78. Becke AD (1993) Density‐functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648–5652. doi:10.1063/1.464913

    Article  CAS  Google Scholar 

  79. Lee C, Yang W, Parr RG (1988) Development of the Colle–Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 37:785–789. doi:10.1103/PhysRevB.37.785

  80. Ditchfield R, Hehre WJ, Pople JA (2003) Self‐consistent molecular‐orbital methods. IX. An extended Gaussian‐type basis for molecular‐orbital studies of organic molecules. J Chem Phys 54:724–728. doi:10.1063/1.1674902

  81. Andrae D, Häußermann U, Dolg M, Stoll H, Preuß H (1990) Energy-adjusted ab initio pseudopotentials for the second and third row transition elements. Theor Chim Acta 77:123–141. doi:10.1007/BF01114537

  82. Frisch M, Trucks G, Schlegel H, Scuseria G, Robb M, Cheeseman J, Scalmani G, Barone V, Mennucci B, Petersson G, Nakatsuji H, Caricato M, Li X, Hratchian H, Izmaylov A, Bloino J, Zheng G, Sonnenberg J, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Jr, Peralta J, Ogliaro F, Bearpark M, Heyd J, Brothers E, Kudin K, Staroverov V, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant J, Iyengar S, Tomasi J, Cossi M, Rega N, Millam J, Klene M, Knox J, Cross J, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann R, Yazyev O, Austin A, Cammi R, Pomelli C, Ochterski J, Martin R, Morokuma K, Zakrzewski V, Voth G, Salvador P, Dannenberg J, Dapprich S, Daniels A, Farkas, Foresman J, Ortiz J, Cioslowski J, Fox D (2009) Gaussian 09, revision A.02. Gaussian Inc., Wallingford

  83. Cossi M, Rega N, Scalmani G, Barone V (2003) Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J Comput Chem 24:669–681. doi:10.1002/jcc.10189

    Article  CAS  Google Scholar 

  84. Barone V, Cossi M (1998) Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model. J Phys Chem A 102:1995–2001. doi:10.1021/jp9716997

    Article  CAS  Google Scholar 

  85. Siegbahn PEM, Eriksson L, Himo F, Pavlov M (1998) Hydrogen atom transfer in ribonucleotide reductase (RNR). J Phys Chem B 102:10622–10629. doi:10.1021/jp9827835

    Article  CAS  Google Scholar 

  86. Siegbahn PEM (1998) Theoretical study of the substrate mechanism of ribonucleotide reductase. J Am Chem Soc 120:8417–8429. doi:10.1021/ja9736065

    Article  CAS  Google Scholar 

  87. Blomberg MRA, Siegbahn PEM, Babcock GT (1998) Modeling electron transfer in biochemistry: a quantum chemical study of charge separation in Rhodobacter sphaeroides and Photosystem II. J Am Chem Soc 120:8812–8824. doi:10.1021/ja9805268

  88. Odintsov SG, Sabala I, Bourenkov G, Rybin V, Bochtler M (2005) Staphylococcus aureus aminopeptidase S is a founding member of a new peptidase clan. J Biol Chem 280:27792–27799. doi:10.1074/jbc.M502023200

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Acknowledgments

The authors would like to acknowledge the program FEDER/COMPETE and the Fundação para a Ciência e Tecnologia (FCT) due to the financial support provided (project PTDC/QUI-QUI/103118/2008).

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  1. REQUIMTE, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre s/n, 4169-007, Porto, Portugal

    Natércia F. Brás, António J. M. Ribeiro, Marina Oliveira, Juan A. Tamames, Pedro A. Fernandes & Maria J. Ramos

  2. NEQC, Núcleo de Estudos em Química Computacional, Departamento de Química, Instituto de Ciências Exatas, Universidade Federal de Juiz de Fora, Juiz de Fora, MG, 36036-330, Brazil

    Nathália M. Paixão

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  1. Natércia F. Brás
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Correspondence to Maria J. Ramos.

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Natércia F. Brás and António J. M. Ribeiro contributed equally to this work.

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Brás, N.F., Ribeiro, A.J.M., Oliveira, M. et al. Analyses of cobalt–ligand and potassium–ligand bond lengths in metalloproteins: trends and patterns. J Mol Model 20, 2271 (2014). https://doi.org/10.1007/s00894-014-2271-z

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