Amide–π interactions in active centers of superoxide dismutase Scientific paper

Main Article Content

Srđan Stojanović
https://orcid.org/0000-0002-1847-9318
Zoran Petrović
https://orcid.org/0000-0002-8571-5210
Mario Zlatović
https://orcid.org/0000-0003-4311-1731

Abstract

In this work, we have analyzed the influence of amide–π interactions on stability and properties of superoxide dismutase (SOD) active centers. In the data set of 43 proteins, 5017 amide–π interactions were observed, and every active center forms 117 interactions, on the average. Most of the interactions belong to the backbone of proteins. The analysis of the geometry of the amide–π interactions revealed two preferred structures, parallel-displaced and T-shaped structure. The aim of this study was to investigate the energy contribution resulting from amide–π interactions, which were in the lower range of strong hydrogen bonds. The conservation patterns in the present study indicate that more than half of the residues involved in these interactions are evolutionarily conserved. Stabilization centers for these proteins showed that all residues involved in amide–π interactions were important in locating one or more of such centers. The results presented in this work can be very useful for understanding the contribution of amide–π interaction to the stability of SOD active centers.

Article Details

How to Cite
[1]
S. Stojanović, Z. Petrović, and M. Zlatović, “Amide–π interactions in active centers of superoxide dismutase: Scientific paper”, J. Serb. Chem. Soc., Jun. 2021.
Section
Theoretical Chemistry

References

E. A. Meyer, R. K. Castellano, F. Diederich, Angew. Chem., Int. Ed. Engl. 42 (2003) 1210 (https://doi.org/10.1002/anie.200390319)

L. M. Salonen, M. Ellermann, F. Diederich, Angew. Chem., Int. Ed. Engl. 50 (2011) 4808 (https://doi.org/10.1002/anie.201007560)

N. Acharjee, J. Serb. Chem. Soc. 85 (2020) 765 (https://doi.org/10.2298/JSC190914136A)

M. Levitt, M. F. Perutz, J. Mol. Biol. 201 (1988) 751 (https://doi.org/10.1016/0022-2836(88)90471-8)

J. Cheney, B. V. Cheney, W. G. Richards, Biochim. Biophys. Acta. 954 (1988) 137 (https://doi.org/10.1016/0167-4838(88)90063-5)

G. Duan, V. H. Smith, D. F. Weaver, Chem. Phys. Lett. 310 (1999) 323 (https://doi.org/10.1016/S0009-2614(99)00804-0)

M. Harder, B. Kuhn, F. Diederich, ChemMedChem. 8 (2013) 397 (https://doi.org/10.1002/cmdc.201200512)

S. Cotesta, M. Stahl, J. Mol. Model. 12 (2006) 436 (https://doi.org/10.1007/s00894-005-0067-x)

S. K. Burley, G. A. Petsko, Science 229 (1985) 23 (https://doi.org/10.1126/science.3892686)

S. K. Burley, G. A. Petsko, FEBS Lett. 203 (1986) 139 (https://doi.org/10.1016/0014-5793(86)80730-x)

S. K. Burley, G. A. Petsko, Adv. Protein Chem. 39 (1988) 125 (https://doi.org/10.1016/s0065-3233(08)60376-9)

T. Steiner, G. Koellner, J. Mol. Biol. 305 (2001) 535 (https://doi.org/10.1006/jmbi.2000.4301)

F. R. Ferreira de, M. Schapira, MedChemComm. 8 (2017) 1970 (https://doi.org/10.1039/c7md00381a)

M. Giroud, J. Ivkovic, M. Martignoni, M. Fleuti, N. Trapp, W. Haap, A. Kuglstatter, J. Benz, B. Kuhn, T. Schirmeister, F. Diederich, ChemMedChem. 12 (2017) 257 (https://doi.org/10.1002/cmdc.201600563)

S. Raghunathan, T. Jaganade, U. D. Priyakumar, Biophys. Rev. 12 (2020) 65 (https://doi.org/10.1007/s12551-020-00620-9)

M. Giroud, M. Harder, B. Kuhn, W. Haap, N. Trapp, W. B. Schweizer, T. Schirmeister, F. Diederich, ChemMedChem. 11 (2016) 1042 (https://doi.org/10.1002/cmdc.201600132)

L. M. Salonen, M. C. Holland, P. S. Kaib, W. Haap, J. Benz, J. L. Mary, O. Kuster, W. B. Schweizer, D. W. Banner, F. Diederich, Chemistry 18 (2012) 213 (https://doi.org/10.1002/chem.201102571)

B. S. Lauber, L. A. Hardegger, K. A. Alam, B. A. Lund, O. Dumele, M. Harder, B. Kuhn, R. A. Engh, F. Diederich, Chemistry 22 (2016) 211 (https://doi.org/10.1002/chem.201503552)

V. Ehmke, E. Winkler, D. W. Banner, W. Haap, W. B. Schweizer, M. Rottmann, M. Kaiser, C. Freymond, T. Schirmeister, F. Diederich, ChemMedChem. 8 (2013) 967 (https://doi.org/10.1002/cmdc.201300112)

G. R. De, E. Brodbeck-Persch, S. Bryson, N. B. Hentzen, M. Kaiser, E. F. Pai, R. L. Krauth-Siegel, F. Diederich, ChemMedChem. 13 (2018) 957 (https://doi.org/10.1002/cmdc.201800067)

M. W. Krone, C. R. Travis, G. Y. Lee, H. J. Eckvahl, K. N. Houk, M. L. Waters, J. Am. Chem. Soc. 142 (2020) 17048 (https://doi.org/10.1021/jacs.0c06568)

K. DeFrees, M. T. Kemp, X. ElHilali-Pollard, X. Zhang, A. Mohamed, Y. Chen, A. R. Renslo, Org. Chem. Front. 6 (2019) 1749 (https://doi.org/10.1039/c9qo00342h)

R. Meurisse, R. Brasseur, A. Thomas, Proteins 54 (2004) 478 (https://doi.org/10.1002/prot.10582)

P. W. Rose, B. Beran, C. Bi, W. F. Bluhm, D. Dimitropoulos, D. S. Goodsell, A. Prlic, M. Quesada, G. B. Quinn, J. D. Westbrook, J. Young, B. Yukich, C. Zardecki, H. M. Berman, P. E. Bourne, Nucleic Acids Res. 39 (2011) D392 (https://doi.org/10.1093/nar/gkq1021)

J. M. Word, S. C. Lovell, J. S. Richardson, D. C. Richardson, J. Mol. Biol. 285 (1999) 1735 (https://doi.org/10.1006/jmbi.1998.2401)

Accelrys Software Inc., (2020) Discovery Studio Visualizer, Release 2020. Accelrys Software Inc., San Diego.

M. R. Jackson, R. Beahm, S. Duvvuru, C. Narasimhan, J. Wu, H. N. Wang, V. M. Philip, R. J. Hinde, E. E. Howell, J. Phys. Chem. B. 111 (2007) 8242 (https://doi.org/10.1021/jp0661995)

V. Philip, J. Harris, R. Adams, D. Nguyen, J. Spiers, J. Baudry, E. E. Howell, R. J. Hinde, Biochemistry 50 (2011) 2939 (https://doi.org/10.1021/bi200066k)

V. R. Ribić, S. Đ. Stojanović, M. V. Zlatović, Int. J. Biol. Macromol. 106 (2018) 559 (https://doi.org/10.1016/j.ijbiomac.2017.08.050)

J. Hostaš, D. Jakubec, R. A. Laskowski, R. Gnanasekaran, J. Řezáč, J. Vondrášek, P. Hobza, J. Chem. Theory. Comput. 11 (2015) 4086 (http://dx.doi.org/10.1021/acs.jctc.5b00398)

Schrödinger Release 2018-1: Jaguar, Schrödinger, LLC, New York, NY, 2018

T. H. Dunning, J. Chem. Phys. 90 (1989) 1007 (https://doi.org/10.1063/1.456153)

T. Clark, J. Chandrasekhar, G. n. W. Spitznagel, P. V. R. Schleyer, J. Comput. Chem. 4 (1983) 294 (https://doi.org/10.1002/jcc.540040303)

A. D. Bochevarov, E. Harder, T. F. Hughes, J. R. Greenwood, D. A. Braden, D. M. Philipp, D. Rinaldo, M. D. Halls, J. Zhang, R. A. Friesner, Int. J. Quantum Chem. 113 (2013) 2110 (https://doi.org/10.1002/qua.24481)

G. J. Jones, A. Robertazzi, J. A. Platts, J. Phys. Chem. B. 117 (2013) 3315 (https://doi.org/10.1021/jp400345s)

K. E. Riley, J. A. Platts, J. Řezáč, P. Hobza, J. G. Hill, J. Phys. Chem. A 116 (2012) 4159 (https://doi.org/10.1021/jp211997b)

S. Saebø, W. Tong, P. Pulay, J. Chem. Phys. 98 (1993) 2170 (https://doi.org/10.1063/1.464195)

A. Reyes, L. Fomina, L. Rumsh, S. Fomine, Int. J. Quantum Chem. 104 (2005) 335 (https://doi.org/10.1002/qua.20558)

R. M. Balabin, J. Chem. Phys. 132 (2010) 231101 (https://doi.org/10.1063/1.3442466)

Z. Dosztányi, A. Fiser, I. Simon, J. Mol. Biol. 272 (1997) 597 (https://doi.org/10.1006/jmbi.1997.1242)

Z. Dosztányi, C. Magyar, G. Tusnady, I. Simon, Bioinformatics 19 (2003) 899 (https://doi.org/10.1093/bioinformatics/btg110)

H. Ashkenazy, E. Erez, E. Martz, T. Pupko, N. Ben-Tal, Nucleic Acids Res. 38 (2010) W529 (https://doi.org/10.1093/nar/gkq399)

B. Boeckmann, A. Bairoch, R. Apweiler, M. C. Blatter, A. Estreicher, E. Gasteiger, M. J. Martin, K. Michoud, C. O'Donovan, I. Phan, S. Pilbout, M. Schneider, Nucleic Acids Res. 31 (2003) 365 (https://doi.org/10.1093/nar/gkg095)

G. Toth, C. R. Watts, R. F. Murphy, S. Lovas, Proteins 43 (2001) 373 (https://doi.org/10.1002/prot.1050)

A. S. Mahadevi, G. N. Sastry, Chem. Rev. 116 (2016) 2775 (https://doi.org/10.1021/cr500344e)

G. B. McGaughey, M. Gagne, A. K. Rappe, J. Biol. Chem. 273 (1998) 15458 (https://doi.org/10.1074/jbc.273.25.15458)

B. P. Dimitrijević, S. Z. Borozan, S. Đ. Stojanović, RSC Adv. 2 (2012) 12963 (https://doi.org/10.1039/C2RA21937A)

G. R. Desiraju, T. Steiner, The Weak Hydrogen Bond, Oxford University Press, Oxford, England, 1999