Abstract
Manganese (Mn) is an important metal that is crucial in biological cell mechanism and function. However, its binding mechanism is poorly characterized. In the present study, we have carried out a detailed statistical analysis of the Mn-containing proteins through analysis of the metal coordination spheres of the vast number of protein crystal structures present in Protein Data Bank. These results reveal that Mn metal predominantly acquires the coordination number of six and five. In these predominant six and five coordination spheres, Mn metal is majorly stabilized with octahedral and square pyramidal geometries respectively. The water molecules, aspartic acid, and glutamic acid residues bonded frequently with Mn metal ions. These results provided useful insights to characterize the very important Mn-containing subset of the proteome. Quantum mechanical results showed that the complexes with coordination number six are predominantly having high interaction energy, which is in good agreement with statistical analysis.
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Harding MM, Nowicki MW, Walkinshaw MD (2010) Metals in protein structures: a review of their principal features. Crystallogr Rev 16:247–302
Lu Y (2006) Metalloprotein and metallo-DNA/RNAzyme design: current approaches, success measures, and future challenges. Inorg Chem 45:9930–9940
Pidcock E, Moore GR (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 6:479–489
Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96:2909–2926
Lipscomb WN, Strater N (1996) Recent advances in zinc enzymology. Chem Rev 96:2375–2434
Berg JM, Godwin HA (1997) Lessons from zinc-binding peptides. Annu Rev Biophys Biomol Struct 26:357–371
Dokmanić I, Sikić 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 Biol Crystallogr 64:257–263
Maret W (2010) Metalloproteomics, metalloproteomes, and the annotation of metalloproteins. Metallomics 2:117–125
Christianson DW (1997) Structural chemistry and biology of manganese metalloenzymes. Prog Biophys Mol Biol 67:217–252
Cotton FA, Wilkinson G (1980) Advanced inorganic chemistry. A comprehensive text4th edn. Wiley, New York
Frau’sto da Silva JJR, Williams RJP (1991) The biological chemistry of the elements. The Inorganic Chemistry of Life Clarendon Press, Oxford
Rulísek L, Vondrásek J (1998) Coordination geometries of selected transition metal ions (Co2+, Ni2+, Cu2+, Zn2+, Cd2+, and Hg2+) in metalloproteins. J Inorg Biochem 71:115–127
Harding MM (2004) The architecture of metal coordination groups in proteins. Acta Crystallogr D Biol Crystallogr 60:849–859
Harding MM (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 57:401–411
Harding MM (1999) The geometry of metal-ligand interactions relevant to proteins. Acta Crystallogr D Biol Crystallogr 55:1432–1443
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
Mahadevi AS, Sastry GN (2013) Cation-π interaction: its role and relevance in chemistry, biology and material science. Chem Rev 113:2100–2138
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
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
Tus A, Rakipovic A, Peretin G, Tomic S, Sikic M (2012) BioMe: biologically relevant metals. Nucleic Acids Res 40:W352–W357
Brylinski M, Skolnick J (2011) FINDSITE-metal: integrating evolutionary information and machine learning for structure based metal-binding site prediction at the proteome level. Proteins 79:735–751
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery Jr JA, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian09, Revision A02. Gaussian, Inc, Wallingford
Ziegler T (1991) Approximate density functional theory as a practical tool in molecular energetics and dynamics. Chem Rev 91:651–667
Andrae D, Haussermann U, Dolg M, Stoll H, Preuss H (1990). Theor Chim Acta 77:123–141
Dunning, TH, Hay PJ (1997) Modern Theoretical Chemistry Plenum New York
Dolg M, Wedig U, Stoll H, Preuss H (1987) Energy-adjusted ab initio pseudo potentials for the first row transition elements. J Chem Phys 86:866
Marenich AV, Cramer CJ, Truhlar DG (2009) Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J Phys Chem B 113:6378–6396
Purushotham U, Takenaka N, Nagaoka M (2016) Additive effect of fluoroethylene and difluoroethylene carbonates for the solid electrolyte interphase film formation in sodium-ion batteries: a quantum chemical study. RSC Adv 6:65232–65242
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
Siegbahn PEM (1998) Theoretical study of the substrate mechanism of Ribonucleotide Reductase. J Am Chem Soc 120:8417–8429
Purushotham U (2018) Exploration of conformations, Analysis of Protein and Biological Significance of Histidine Dimers. Chemistry Select 3:3070
Tanneeru K, Guruprasad L (2013) Structural basis for binding of aurora-AG198N-INCENP complex: MD simulations and free energy calculations. Protein Pept Lett 20:1246–1256
Tanneeru K, Sahu I, Guruprasad L (2013) Ligand-based drug design for human endothelin converting enzyme-1 inhibitors. Med Chem Res 22:4401–4409
Purushotham U, Zipse H, Sastry GN (2016) A first-principles investigation of histidine and its ionic counterparts. Theor Chem Acc 135:174–190
Kaufman Katz A, Shimoni-Livny L, Navon O, Navon N, Bock CW, Glusker JP (2003) Copper-binding motifs: Structural and theoretical aspects. Helv Chim Acta 86:1320–1338
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Authors wish to thank Management and Department of Chemistry, CKM Arts and Science College, Warangal, Qstatix Pvt. Ltd., Hyderabad and Osmania University, Hyderabad, for providing facilities.
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S., U., Gangula, M.R., K., R. et al. Investigation of manganese metal coordination in proteins: a comprehensive PDB analysis and quantum mechanical study. Struct Chem 31, 1057–1064 (2020). https://doi.org/10.1007/s11224-020-01488-x
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DOI: https://doi.org/10.1007/s11224-020-01488-x