Abstract
The kinetics and equilibrium of the hydride transfer reaction between lumiflavin and a number of substituted quinones was studied using density functional theory. The impact of electron withdrawing/donating substituents on the redox potentials of quinones was studied. In addition, the role of these substituents on the kinetics of the hydride transfer reaction with lumiflavin was investigated in detail under the transition state (TS) theory assumption. The hydride transfer reactions were found to be more favorable for an electron-withdrawing substituent. The activation barrier exhibited a quadratic relationship with the driving force of these reactions as derived under the formalism of modified Marcus theory. The present study found a significant extent of electron delocalization in the TS that is stabilized by enhanced electrostatic, polarization, and exchange interactions. Analysis of geometry, bond-orders, and energetics revealed a predominant parallel (Leffler-Hammond) effect on the TS. Closer scrutiny reveals that electron-withdrawing substituents, although located on the acceptor ring, reduce the N–H bond order of the donor fragment in the precursor complex. Carried out in the gas-phase, this is the first ever report of a theoretical study of flavin’s hydride transfer reactions with quinones, providing an unfiltered view of the electronic effect on the nuclear reorganization of donor–acceptor complexes.
Similar content being viewed by others
References
Leung KK, Shilton BH (2013) J Biol Chem 288:11242–11251
Song N, Gagliardi CJ, Binstead RA, Zhang MT, Thorp H et al (2012) J Am Chem Soc 134:18538–18541
Beheshti A, Norouzi P, Ganjali MR (2012) Int J Electrochem Sci 7:4811–4821
Sollner S, Deller S, Macheroux P, Palfey BA (2009) Biochemistry 48:8636–8643
Colucci MA, Moody CJ, Couch GD (2008) Org Biomol Chem 6:637–656
Frontana C, Vazquez-Mayagoitia A, Garza J, Vargas R, Gonzalez I (2006) J Phys Chem A 110:9411–9419
Celli CM, Tran N, Knox R, Jaiswal AK (2006) Biochem Pharmacol 72:366–376
Cenas N, Anusevicius Z, Nivinskas H, Miseviciene L, Sarlauskas J (2004) Methods Enzymol 382:258–277
Di Francesco AM, Ward TH, Butler J (2004) Methods Enzymol 382:174–193
Watanabe N, Dickinson DA, Liu RM, Forman HJ (2004) Methods Enzymol 378:319–340
Faig M, Bianchet MA, Winski S, Hargreaves R, Moody CJ et al (2001) Structure 9:659–667
Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ (2000) Chem Res Toxicol 13:135–160
Ross D, Siegel D (2004) Methods Enzymol 382:115–144
Cheng J, Sulpizi M, Sprik M (2009) J Chem Phys 131:154504
Namazian M, Almodarresieh HA (2004) J Mol Struct (Theochem) 686:97
Shamshipur M, Alizadeh K, Arshadi S (2006) J Mol Struct (Theochem) 758:71
Lee I-SH, Ostovic D, Kreevoy MM (1988) J Am Chem Soc 110:3989–3993
Marcus RA, Sutin N (1985) Biochim Biophys Acta 811
Kreevoy MM, Lee I-SH (1984) J Am Chem Soc 106:2550–2553
Lee I-SH, Jeoung EH, Kreevoy MM (1997) J Am Chem Soc 119:2722–2728
Bresnahan CG, Reinhardt CR, Bartholow TG, Rumpel JP, North M et al (2015) J Phys Chem A 119:172–182
Mueller RM, North MA, Yang C, Hati S, Bhattacharyya S (2011) J Phys Chem B 115:3632–3641
North MA, Bhattacharyya S, Truhlar DG (2010) J Phys Chem B 114:14907–14915
Rauschnot JCJ, Yang C, Yang V, Bhattacharyya S (2009) J Phys Chem B 113:8149–8157
Cui Q, Elstner M, Kaxiras E, Frauenheim T, Karplus M (2001) J Phys Chem B 105:569–585
Elstner M, Cui Q, Munih P, Kaxiras E, Frauenheim T et al (2003) J Comput Chem 24:565–581
Kohn W, Sham LJ (1965) Phys Rev A 140:1133–1138
Sinnokrot MO, Sherrill CD (2006) J Phys Chem A 110:10656–10668
Zhao Y, Truhlar DG (2006) Org Lett 8:5753–5755
Zhao Y, Truhlar DG (2006) J Chem Phys 125:194101
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA et al (2009) Gaussian 09, Revision A.1. Gaussian, Inc, Wallingford CT
Cossi M, Barone V (2000) J Chem Phys 112:2427–2435
Su P, Li H (2009) J Chem Phys 131:014102
Schmidt MW, Baldridge KK, Boatz JA, Elbert ST, Gordon MS et al (1993) J Comput Chem 14:1347–1363
Biondi C, Galeazzi R, Littarru G, Greci L (2002) Free Radic Res 36:399–404
Zhu Z, Gunner MR (2005) Biochemistry 44:82–96
Kelly CP, Cramer CJ, Truhlar DG (2007) J Phys Chem B 111:408–422
Abel B, Buck U, Sobolewski AL, Domcke W (2012) Phys Chem Chem Phys 14:22–34
Lewis A, Bumpus JA, Truhlar DG, Cramer CJ (2004) J Chem Educ 81:596–604
Peng C, Schlegel HB (1993) Israel J Chem 33:449–454
Kreevoy MM, Truhlar DG (1986) Transition state theory. In: Bernasconi CF (ed) Investigation of rates and mechanisms of reactions, 4th edn, vol 6, part 1. Wiley, New York,pp 13–95
Zhao Y, Schultz NE, Truhlar DG (2006) J Chem Theory Comput 2:364–382
Zhao Y, Truhlar D (2008) Theor Chem Acc 120:215–241
Leffler JE (1953) Science 117:340–341
Hammond GS (1955) J Am Chem Soc 77:334–338
Thornton ER (1967) J Am Chem Soc 89:2915–2927
Weinhold F, Landis CR (2001) Chem Educ Res Pract Eur 2001
Eyring H (1935) J Chem Phys 3:107–115
Sutcliffe MJ, Masgrau L, Roujeinikova A, Johannissen LO, Hothi P et al (2006) Phil Trans R Soc B Biol Sci 361:1375–1386
Klinman JP, Kohen A (2013) Annu Rev Biochem 82:471–496
Acknowledgments
This work was supported by XSEDE Grant (CHE-110018), Research Corporation grant (CCSA 23223), and the Office of Research and Sponsored Programs, University of Wisconsin Eau Claire. We gratefully acknowledge the computational support from the in-house Blugold Supercomputing Cluster and Learning and Technology Services of the University of Wisconsin Eau Claire. We also thank Dr. Fredrick King of University of Wisconsin Eau Claire for his helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work contains results from a Physical Chemistry-I class project assigned to undergraduate students. Clorice R. Reinhardt is the main contributory undergraduate author. Tanner C. Jaglinski, Ashly M. Kastenschmidt, Eun H. Song, Adam K. Gross, Alyssa J. Krause, Jonathan M. Gollmar, Kristin J. Meise, Zachary S. Stenerson, Tyler J. Weibel, Andrew Dison, Mackenzie R. Finnegan, Daniel S. Griesi, Michael D. Heltne, Tom G. Hughes, Connor D. Hunt, Kayla A. Jansen, Adam H. Xiong are students of 2014 Fall Physical Chemistry-1.
Rights and permissions
About this article
Cite this article
Reinhardt, C.R., Jaglinski, T.C., Kastenschmidt, A.M. et al. Insight into the kinetics and thermodynamics of the hydride transfer reactions between quinones and lumiflavin: a density functional theory study. J Mol Model 22, 199 (2016). https://doi.org/10.1007/s00894-016-3074-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00894-016-3074-1