Active-site dynamics and large-scale domain motions of sulfite oxidase: A molecular dynamics study

Journal of Physical Chemistry B

Volumn 114, Issue 9, 2010, Pages 3266-3275

  Pushie, M Jake ^a   George, Graham N ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC OXIDATION; CRYSTAL ORIENTATION; ELECTRON TRANSITIONS; ENZYMES; METAL IONS; MOLECULAR DYNAMICS; MOLYBDENUM; PORPHYRINS;

ACTIVE SITE; C-TERMINAL DOMAINS; CATALYTIC CYCLES; DOMAIN MOTIONS; ELECTRON TRANSFER; INTRA-MOLECULAR ELECTRON TRANSFER; MOLECULAR DYNAMICS SIMULATIONS; N-TERMINAL DOMAINS; SULFITE OXIDASE; SULFITE OXIDATION;

DYNAMICS;

EID: 77749316072     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp908731f     Document Type: Article

References (46)

1. McLeod, R. M.; Farkas, W.; Fridovitch, I.; Handler, P. Purification and properties of hepatic sulfite oxidase. J. Biol. Chem. 1961, 236, 1841-1852.
2. Rees, D. C.; Tezcan, A.; Hayes, C. A.; Walton, M. Y.; Andrade, S.; Einsle, O.; Howard, J. B. Structural basis of biological nitrogen fixation. Philos. Trans. R. Soc. London, Ser. A 2005, 263, 971-984.
3. Rajagopalan, K. V. Novel aspects of the biochemistry of the molybdenum cofactor. Adv. Enzymol, Relat. Areas Mol. Biol. 1991, 64, 215-290.
4. Rajagopalan, K. V.; Johnson, J. L. The pterin molybdenum cofactors. J. Biol. Chem. 1992, 267, 10199-10202.
5. (5) Eilers, T.; Schwarz, G.; Brinkmann, H.; Witt, C.; Richter, T.; Nieder, J.; Koch, B.; Hille, R.; Hänsen, R.; Mendel, R. R. Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism. J. Biol. Chem. 2001, 276, 46989-46994. (Pubitemid 37373072)
6. Kappler, U.; Bennett, B.; Rethmeier, J.; Schwarz, G.; Deutzmann, R.; McEwan, A. G.; Dahl, C. Sulfite:cytochrome c oxidoreductase from Thiobacillus novellus; purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J. Biol. Chem. 2000, 275, 13202-13212.
7. Seidahmed, M. Z.; Alyamani, E. A.; Rashed, M. S.; Saadallah, A. A.; Abdelbasit, O. B.; Saheed, M. M.; Rasheed, A.; Hamid, F. A.; Sabry, M. A. Total truncation of the molybdopterin/dimerization domains of SUOX protein in an Arab family with isolated sulfite oxidase deficiency. Am. J. Med. Genet. Part A 2005, 136A, 205-209.
8. Steinberg, K. K.; Relling, M. V.; Gallagher, M. L.; Greene, C. N.; Rubin, C. S.; French, D.; Holmes, A. K.; Carroll, W. L.; Koontz, D. A.; Sampson, E. J.; Satten, G. A. Genetic studies of a cluster of acute lymphoblastic leukemia cases in Churchill County, Nevada. Environ. Health. Perspect. 2007, 115, 158-164.
9. (9) Kisker, C.; Schindelin, H.; Pacheco, A.; Wehbi, W. A.; Garrett, R. M.; Rajagopalan, K. V.; Enemark, J. H.; Rees, D. C. Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell 1997, 91, 973-983. (Pubitemid 28027830)
10. Enroth, C.; Eger, B. T.; Okamoto, K.; Nishino, T.; Nishino, T.; Pai, E. F. Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: Structure-based mechanism of conversion. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 10723-10728.
11. Rebelo, J.; Macieira, S.; Dias, J. M.; Huber, R.; Ascenso, C. S.; Rusnak, F.; Moura, J. J.; Moura, I.; Romao, M. J. Gene sequence and crystal structure of the aldehyde oxidoreductase from Desulfovibrio desulfuricans ATCC 27774. J. Mol. Biol. 2000, 297, 135-146.
12. Feng, C.; Kedia, R. V.; Hazzard, J. T.; Hurley, J. K.; Tollin, G.; Enemark, J. H. Effect of Solution Viscosity on Intramolecular Electron Transfer in Sulfite Oxidase. Biochemistry 2002, 41, 5816-5821.
13. Kawatsu, T.; Beratan, D. N. Electron transfer between cofactors in protein domains linked by a flexible tether. Chem. Phys. 2006, 326, 259-269.
14. Johnson, J. L.; Rajagopalan, K. V. Tryptic cleavage of rat liver sulfite oxidase. Isolation and characterization of molybdenum, and heme domains. J. Biol. Chem. 1977, 252, 2017-2025.
15. (15) Feng, C.; Wilson, H. L.; Hurley, J. K.; Hazzard, J. T.; Tollin, G.; Rajagopalan, K. V.; Enemark, J. H. Essential role of conserved arginine 160 in intramolecular electron transfer in human sulfite oxidase. Biochemistry 2003, 42, 12235-12242. (Pubitemid 37296500)
16. Doonan, C. J.; Wilson, H. L.; Rajagopalan, K. V.; Garrett, R. M.; Bennett, B.; Prince, R. C.; George, G. N. Modified active site coordination in a clinical mutant of sulfite oxidase. J. Am. Chem. Soc. 2007, 129, 9421-9428.
17. Wilson, H. L.; Rajagopalan, K. V. The role of tyrosine 343 in. substrate binding and catalysis by human sulfite oxidase. J. Biol. Chem. 2004, 279, 15105-15113.
18. Lee, H. F.; Mak, B. S. C.; Chi, C. S.; Tsai, C. R.; Chen, C. H.; Shu, S. G. A. novel mutation in neonatal isolated sulfite oxidase deficiency. Ngtropediatrics 2002, 33, 174-179.
19. Pacheco, A.; Hazzard, J. T.; Tollin, G.; Enemark, J. H. The pH dependence of intramolecular electron transfer rates in sulfite oxidase at high and low anion concentrations. J. Biol. Inorg. Chem. 1999, 4, 390-401.
20. (20) Feng, C.; Wilson, H. L.; Hurley, J. K.; Hazzard, J. T.; Tollin, G.; Rajagopalan, K. V.; Enemark, J. H. Role of conserved tyrosine 343 in intramolecular electron transfer in human, sulfite oxidase. J. Biol. Chem. 2003, 278, 2913-2920. (Pubitemid 36801196)
21. Becke, A. D. Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 1993, 98, 5648-5652.
22. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, Jr., J. A.; Vreven, T.; Kudin, K. N. ; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Barone, V.; Mennucci, B.; Cossi, M.; Scalmani, G.; Rega, N.; Petersson, G. A.; Nakatsuji, H.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Klene, M.; Li, X.; Knox, J. E.; Hratchian, H. P.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Ayala, P. Y.; Morokuma, K.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich, S.; Daniels, A. D.; Strain, M.. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Clifford, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03, Revision E.01; Gaussian Inc.: Wallingford, CT, 2004.
23. Kaminski, G.; Duffy, E. M.; Matsui, T.; Jorgensen, W. L. Free energies of hydration and pure liquid properties of hydrocarbons from the OPLS all-atom model. J. Phys. Chem. 1994, 98, 13077-13082.
24. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 1996, 118, 1122511236.
25. George, G. N.; Kipke, C. A.; Prince, R. C.; Sunde, R. A.; Enemark, J. H.; Cramer, S. P. Structure of the active site of sulfite oxidase. X-ray absorption spectroscopy of the Mo(IV), Mo(V) and Mo(VI) oxidation states. Biochemistry 1989, 28, 5075-5080.
26. Harris, H. H.; George, G. N.; Rajagopalan, K. V. High resolution. EXAFS of the active site of sulfite oxidase: Comparison with, density functional and x-ray crystallographic results, Inorg. Chem. 2006, 45, 493-495.
27. Carlson, H. A.; Nguyen, T. B.; Orozco, M.; Jorgensen, W. L. Accuracy of free energies of hydration for organic molecules from 6-31g*derived partial charges. J. Comput. Chem. 1993, 14, 1240-1249.
28. Pushie, M. J.; Vogel, H. J. Molecular dynamics simulations of two tandem octa-repeat sites from the mammalian, prion protein in its metal free and fully copper-bound states. Biophys. J. 2007, 93, 3762-3774.
29. 2+-.mediated betacleavage. Biophys. J. 2008, 95, 5084-5091.
30. Brunier, T. M.; Drew, M. G. B.; Mitchell, P. C. H. Molecular mechanics study of the interaction of thiophene with a molybdenum disulfide catalyst, J. Chem. Soc., Faraday Trans. 1992, 88, 3225-3232.
31. Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. GROMACS: A message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 1995, 91, 43-56.
32. (32) Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A. package for molecular simulation and trajectory analysis. J. Mol. Model 2001, 7, 306-317. (Pubitemid 36153547)
33. Berendsen, H. J. C.; Postma, J. P. M.; DiNoIa, A.; Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684-3690.
34. Essman, U.; Perela, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle mesh Ewald method, J. Chem. Phys. 1995, 103, 8577-8592.
35. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 1997, 18, 1463-1472.
36. Berendsen, H. C.; Postma, J. P. M.; van Gunsteren, W. F.; Hermans, J. In lntermolecular Forces; Pullman, B., Ed.; Reidel: Dordrecht, The Netherlands, 1981; pp 331-342.
37. Miyamoto, S.; Kollman, P. A. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 1992, 13, 952-962.
38. Feenstra, K. A.; Hess, B.; Berendsen, H. J. C. Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems, J. Comput. Chem. 1999, 20, 786-798.
39. Aliste, M. P.; Tieleman, D. P. Computer simulation of partitioning of ten pentapeptides Ace-WLXLL at the cyclohexane/water and phospholipid/water interfaces. BMC Biochem. 2005, 6, 30.
40. Chan, D. I.; Stockner, T.; Tieleman, D. P.; Vogel, H. J. Molecular Dynamics Simulations of the Apo-, HoIo-, and Acyl-forms of Escherichia coli Acyl Carrier Protein. J. Biol. Chem. 2008, 283, 33620-33629.
41. van der Spoel, D.; Lindahl, E.; Hess, B.; van Buuren, A. R.; Apol, E., Meulenhoff, P. J.; Tieleman, D. P.; Sijbers, A. L. T. M.; Feenstra, K. A.; van Drunen, R.; Berendsen, H. J. C. Gromacs User Manual 3.3, www.gromacs. org, 2005.
42. http://lorentz.immstr.pasteur.fr/nomad-ref.php.
43. Tirion, M. M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 1996, 77, 19051908.
44. (44)Bahar,I.;Atilgan,A.R.;Erman,B. Directevaluationofthermalfluctuationsinproteinsusingasingleparameterharmonicpot ential.FoldingDes.1997,1,357-370.(Pubitemid127740467)
45. Friedrichs, M. S.; Eastman, P.; Vaidyanathan, V.; Houston, M.; Legrand, S.; Beberg, A. L.; Ensign, D. L.; Bruns, C. M.; Pande, V. S. Accelerating molecular dynamic simulation on graphics processing units. J. Comput. Chem. 2009, 30, 864-872.
46. Emesh, S.; Rapson, T. D.; Rajapakshe, A.; Kappler, U.; Bernhardt, P. V.; Tollin, G.; Enemark, J. H. Intramolecular Electron Transfer in SulfiteOxidizing Enzymes: Elucidating the Role of a Conserved Active Site Arginine. Biochemistry 2009, 48, 2156-2163.