Determination of enzyme mechanisms by molecular dynamics: Studies on quinoproteins, methanol dehydrogenase, and soluble glucose dehydrogenase

Protein Science

Volumn 13, Issue 8, 2004, Pages 1965-1978

  Reddy, Swarnalatha Y ^a   Bruice, Thomas C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hydride transfer mechanism; Methanol dehydrogenase; Molecular dynamics; PQQ; Quinoproteins; Soluble glucose dehydrogenase

Indexed keywords

ARGININE; ASPARTIC ACID; FORMALDEHYDE; GLUCOSE; GLUCOSE DEHYDROGENASE; HYDROXYL GROUP; LACTONE DERIVATIVE; METHANOL; METHANOL DEHYDROGENASE; OXIDOREDUCTASE; OXYGEN; PROTEIN DERIVATIVE; QUINOPROTEIN DERIVATIVE; UNCLASSIFIED DRUG; WATER;

CATALYSIS; CHEMICAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; GLUCOSE OXIDATION; HYDROGEN BOND; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTON TRANSPORT; REDUCTION; REVIEW;

ALCOHOL OXIDOREDUCTASES; ALLOSTERIC SITE; CATALYSIS; COENZYMES; GLUCOSE DEHYDROGENASES; MODELS, CHEMICAL; PROTEIN STRUCTURE, TERTIARY; QUINONES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 3342951743     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04673404     Document Type: Review

References (89)

1. Adachi, O., Matsushita, K., Shinagawa, E., and Ameyama, M. 1990. Calcium in quinoprotein methanol dehydrogenase can be replaced by strontium. Agric. Biol. Chem. 54: 2833-2837.
2. L. Biochemistry 40: 9799-9809.
3. Anthony, C. 1986. The bacterial oxidation of methane and methanol. Adv. Microbiol. Physiol. 27: 113-210.
4. -. 1992. The c-type cytochromes of methylotrophic bacteria. Biochim. Biophys. Acta 1099: 1-15.
5. -. 1996. Quinoprotein-catalysed reactions. Biochem. J. 320: 697-711.
6. -. 2001. Pyrroloquinoline quinone (PQQ) and quinoprotein enzymes. Antioxid. Redox Sign. 3: 757-774.
7. Anthony, C. and Ghosh, M. 1998. The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog. Biophys. Mol. Biol. 69: 1-21.
8. Anthony, C., Ghosh, M., and Blake, C.C.F. 1994. The structure and function of methanol dehydrogenase and related quinoproteins containing pyrroloquinoline quinone. Biochem. J. 304: 665-674.
9. Avezoux, A., Goodwin, M., and Anthony, C. 1995. The role of the novel disulphide ring in the active site of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens. Biochem. J. 307: 735-741.
10. Berendsen, H.J.C. and Hayward, S. 2000. Collective protein dynamics in relation to function. Curr. Opin. Struct. Biol. 10: 165-169.
11. Brooks III, C.L. and Karplus, M. 1989. Solvent effects on protein motion and protein effects on solvent motion. J. Mol. Biol. 208: 159-181.
12. Brooks III, C.L., Pettitt, M.B., and Karplus, M. 1985. Structural and energetic effects of truncating long range interactions in ionic and polar fluids. J. Chem. Phys. 83: 5897-5908.
13. Chen, Z.-W., Matsushita, K., Yamashita, T., Adachi, O., Beilamy, H.D., and Mathews, F.S. 2002. Structure at 1.9 A resolution of a quinohemoprotein alcohol dehydrogenase from Pseudomonas putida HK5. Structure 10: 837-848.
14. Cleton-Jansen, A.-M., Goosen, N., Wenzel, T.J., and van de Putte, P. 1988. Cloning of the gene encoding quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus: Evidence for the presence of a second enzyme. J. Bacteriol. 170: 2121-2125.
15. Crennell, S.J., Garman, E.F., Laver, W.G., Vimr, E.R., and Taylor, G.L. 1993. Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc. Natl. Acad. Sci. 90: 9852-9856.
16. Daggett, V. 2000. Long timescale simulations. Curr. Opin. Struct. Biol. 10: 160-164.
17. Datta, S., Mori, Y., Takagi, K., Kawaguchi, K., Chen, Z.-W., Okajima, T., Kuroda, S., Ikeda, T., Kano, K., Tanizawa, K., et al. 2000. Structure of a quinohemoprotein amine dehydrogenase with an uncommon redox cofactor and highly unusual crosslinking. Proc. Natl. Acad. Sci. 98: 14258-14273.
18. Davidson, V.L. 2001. Pyrroloquinoline quinone (PQQ) from methanol dehydrogenase and tryptophan tryptophylquinone (TTQ) from methylamine dehydrogenase. Adv. Prot. Chem. 58: 95-140.
19. Dekker, R.H., Duine, J.A., Frank, J., Verwiel, J., and Westerling, J. 1982. Covalent addition of H20, enzyme substrates and activators to pyrroloquinoline quinone, the coenzyme of quinoproteins. Eur. J. Biochem. 125: 69-73.
20. 2, in the oxidation of β-D-glucose by soluble, quinoprotein glucose dehydrogenase. Biochemistry 39: 9384-9392.
21. L, both purified from Hyphomicrobium X. Biochem. J. 257: 87-94.
22. Dodson, G. and Wlodawer, A. 1998. Catalytic triads and their relatives. Trends Biochem. Sci. 23: 347-352.
23. Dokter, P., Frank, J., and Duine, J.A. 1986. Purification and characterization of quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus. Biochem. J. 239: 163-167.
24. 562 from Acinetobacter calcoaceticus L.M.D. 79.41. Its characteristics and role as electron acceptor for quinoprotein glucose dehydrogenase. Biochem. J. 254: 131-138.
25. Duine, J.A. 1991. Quinoproteins: Enzymes containing the quinonoid factor pyrroloquinoline quinone, topaquinone, or tryptophan-tryptophan quinone. Eur. J. Biochem. 200: 271-284.
26. Duine, J.A. and Frank Jr., J. 1980. The prosthetic group of methanol dehydrogenase purification and some of its properties. Biochem. J. 187: 213-219.
27. Duine, J.A. and Frank Jzn, J. 1981. Quinoproteins: A novel class of dehydrogenases. Trends Biochem. Sci. 2: 278-280.
28. Faber, H.R., Groom, C.R., Baker, H.M., Morgan, W.T., Smith, A., and Baker, E.N. 1995. 1.8 A crystal structure of the C-terminal domain of rabbit serum hemopexin. Structure 3: 551-559.
29. Frank, J.J., Dijkstra, M., Duine, J.A., and Balny, C. 1988. Kinetic and spectral studies on the redox forms of methanol dehydrogenase from Hyphomicrobium X. Eur. J. Biochem. 174: 331-338.
30. 1. Cell 81: 369-377.
31. Garcia-Viloca, M., Gao, J., Karplus, M., and Truhlar, D.G. 2004. How enzymes work: Analysis by modern rate theory and computer simulations. Science 303: 186-195.
32. Geiger, O. and Gorisch, H. 1986. Crystalline quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus. Biochemistry 25:6043-6048.
33. Ghosh, M., Anthony, C., Harlos, K., Goodwin, M.G., and Blake, C.C.F. 1995. The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 Å. Structure 3: 177-187.
34. Gomis, R.F., Gohlke, U., Betz, M., Knauper, V., Murphy, G., Lopez, O.C., and Bode, W. 1996. The helping hand of collagenase-3 (MMP-13): 2.7 Å crystal structure of its C-terminal hemopexin-like domain. J. Mol. Biol. 264: 556-566.
35. Hansson, T., Oostenbrink, C., and van Gunsteren, W.F. 2002. Molecular dynamics simulations. Curr. Opin. Struct. Biol. 12: 190-196.
36. Harris, T.K. and Davidson, V.L. 1993a. Binding and electron transfer reactions between methanol dehydrogenase and its physiologic electron acceptor cytochrome-c-551: A kinetic and thermodynamic analysis. Biochemistry 32: 14145-14150.
37. -. 1993b. A new kinetic model for the steady-state reactions of the quinoprotein methanol dehydrogenase from Paracoccus denitrificans. Biochemistry 32: 4362-4368.
38. Inoue, T., Sunagawa, M., Mori, A., Imai, C., Fukuda, M., Takagi, M., and Yano, K. 1989. Cloning and sequencing of the gene encoding the 72 kilodalton dehydrogenase subunit of alcohol dehydrogenase from Acetobacter aceti. J. Bacteriol. 171: 3115-3122.
39. Ito, N., Phillips, S.E.V., Yadav, K.D.S., and Knowles, P.F. 1994. Crystal structure of a free radical enzyme, galactose oxidase. J. Mol. Biol. 238: 794-814.
40. Itoh, S., Ogino, M., Fukui, Y., Murao, H., Komatsu, M., Ohshiro, Y., Inoue, T., Kai, Y., and Kasai, N. 1993. C-4 and C-5 adducts of cofactor PQQ (pyrroloquinolinequinone). Model studies directed toward the action of quinoprotein methanol dehydrogenase. J. Am. Chem. Soc. 115: 9960-9967.
41. Itoh, S., Kawakami, H., and Fukuzumi, S. 1997. Modeling of the chemistry of quinoprotein methanol dehydrogenase. Oxidation of methanol by calcium complex of coenzyme PQQ via addition-elimination mechanism. J. Am. Chem. Soc. 119: 439-440.
42. Janes, S.M., Mu, D., Wemmer, D., Smith, A.J., Kaur, S., Maltby, D., Burlingame, A.L., and Klinman, J.P. 1990. A new redox cofactor in eukaryotic enzymes: 6-Hydroxydopa at the active site of bovine serum amine oxidase. Science 248: 981-987.
43. Jongejan, A., Jongejan, J.A., and Hagen, W.R. 2001. Direct hydride transfer in the reaction mechanism of quinoprotein alcohol dehydrogenases: A quantum mechanical investigation. J. Comp. Chem. 22: 1732-1749.
44. Jorgensen, W.L., Chandrasekhar, J., Madhura, J.D., Impey, R.W., and Klein, M.L. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79: 926-935.
45. Karplus, M. and McCammon, J.A. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:646-652.
46. Karplus, P.A. and Schulz, G.E. 1989. Substrate binding and catalysis by glutathione reductase as derived from refined enzyme: Substrate crystal structures at 2 Å resolution. J. Mol. Biol. 210: 163-180.
47. Keitel, T., Diehl, A., Knaute, T., Stezowski, J.J., Höhne, W., and Görisch, H. 2000. X-ray structure of the quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa: Basis of substrate specificity. J. Mol. Biol. 297: 961-974.
48. Kollman, P.A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., et al. 2000. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Acc. Chem. Res. 33: 889-897.
49. Lambright, D.G., Sondek, J., Bolm, A., Skiba, N.P., Hamm, H.E., and Sigler, P.B. 1996. The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379: 311-319.
50. Li, J., Brick, P., O'Hare, M.C., Skarzynski, T., Lloyd, L.F., Curry, V.A., Clark, I.M., Bigg, H.F., Hazleman, B.L., Cawston, T.E., et al. 1995. Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed β-propeller. J. Mol. Biol. 332: 319-333.
51. Libson, A.M., Gittis, A.G., Collier, I.E., Marmer, B.L., Goldberg, G.I., and Lattman, E.E. 1995. Crystal structure of the haemopexin-like C-terminal domain of gelatinase A. Nat. Struct. Biol. 2: 938-942.
52. Matsushita, K., Shinagawa, E., Adachi, O., and Ameyama, M. 1989. Quinoprotein D-glucose dehydrogenase of the Acinetobacter calcoaceticus respiratory chain: Membrane-bound and soluble forms are different molecular species. Biochemistry 28: 6276-6280.
53. Matsushita, K., Toyami, H., and Adachi, O. 1994. Respiratory chains and bioenergetics of acetic acid bacteria. Adv. Microbial Physiol. 36: 247-301.
54. Matsushita, K., Toyama, H., Yamada, M., and Adachi, O. 2002. Quinoproteins: Structure, function, and biotechnological applications. Appl. Microbiol. Biotechnol. 58: 13-22.
55. 2. Proc. Natl. Acad. Sci. 93: 7496-7501.
56. McIntire. W.S., Wemme, D.E., Chistoserdov, A., and Lidstrom, M.E. 1991. A new cofactor in a prokaryotic enzyme: Tryptophan tryptophylquinone as the redox prosethetic group in methylamine dehydrogenase. Science 253: 817-824.
57. Olsthoorn, A.J. and Duine, J.A. 1996. Production, characterization, and reconstitution of recombinant quinoprotein glucose dehydrogenase (soluble type; EC 1.1.99.17) apoenzyme of Acinetobacter calcoaceticus. Arch. Biochem. Biophys. 336: 42-48.
58. -. 1998a. Negative cooperativity on the steady state kinetics of sugar oxidation by soluble quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus. Eur. J. Biochem. 255: 255-261.
59. -. 1998b. On the mechanism and specificity of the soluble quinoprotein glucose dehydrogenase in the oxidation of aldose sugars. Biochemistry 37: 13854-13861.
60. 2+ and its substitutes have two different binding sites and roles in soluble quinoprotein glucose dehydrogenase. Eur. J. Biochem. 247: 659-665.
61. Oubrie, A. and Dijkstra, B.W. 2000. Structural requirements of pyrroloquinoline quinone dependent enzymatic reactions. Protein Sci. 9: 1265-1273.
62. Oubrie, A., Rozeboom, H.J., and Dijkstra, B.W. 1999a. Active-site structure of the soluble quinoprotein glucose dehydrogenase complexed with methylhydrazine: A covalent cofactor-inhibitor complex. Proc. Natl. Acad. Sci. 96: 11787-11791.
63. Oubrie, A., Rozeboom, H.J., Kalk, K.H., Duine, J.A., and Dijkstra, B.W. 1999b. The 1.7 Å crystal structure of the apo-form of the soluble quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus reveals a novel internal conserved sequence repeat. J. Mol. Biol. 289: 319-333.
64. Oubrie, A., Rozeboom, H.J., Kalk, K.H., Olsthoorn, A.J.J., Duine, J.A., and Dijkstra, B.W. 1999c. Structure and mechanism of soluble quinoprotein glucose dehydrogenase. EMBO J. 18: 5187-5194.
65. Oubrie, A., Rozeboom, H.J., Kalk, K.H., Huizinga, E.G., and Dijkstra, B.W. 2002. Crystal structure of quinohemoprotein alcohol dehydrogenase from Comamonas testosteroni: Structural basis for substrate oxidation. J. Biol. Chem. 277: 3727-3732.
66. + and substituted benzyl alcohols. Biochemistry 33: 5230-5237.
67. Reddy, S.Y. and Bruice, T.C. 2003. In silico studies of the mechanism of methanol oxidation by quinoprotein methanol dehydrogenase. J. Am. Chem. Soc. 125: 8141-8150.
68. -. 2004. Mechanism of glucose oxidation by quinoprotein soluble glucose dehydrogenase: Insights from molecular dynamics studies. J. Am. Chem. Soc. 126: 2431-2438.
69. Reddy, S.Y., Mathews, F.S., Zheng, Y.-J., and Bruice, T.C. 2003. Quinoprotein methanol dehydrogenase: A molecular dynamics study and comparison with crystal structure. J. Mol. Struct. 655: 269-277.
70. Renault, L., Nassar, N., Vetter, I., Becker, J., Klebe, C., Roth, M., and Wittinghofar, A. 1998. The 1.7 Å crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 392: 97-101.
71. Richardson, I.W. and Anthony, C. 1992. Characterization of mutant forms of the quinoprotein methanol dehydrogenase lacking an essential calcium ion. Biochem. J. 287: 709-715.
72. Salisbury, S.A., Forrest, H.S., Cruse, W.B.T., and Kennard, O. 1979. A novel coenzyme from bacterial primary alcohol dehydrogenases. Nature 280: 843-844.
73. Schiering, N., Kabsch, W., Moore, M.J., Distefano, M.D., Walsh, C.T., and Pai, E.F. 1991. Structure of the detoxification catalyst mercuric ion reductase from Bacillus sp. strain RC607. Nature 352: 168-171.
74. Springer, T.A. 1997. Folding of the N-terminal, ligand-binding region of integrin α-subunits into a β-propeller. Proc. Natl. Acad. Sci. 94: 65-72.
75. Stukey, J.A. and Dixon, J.E. 1999. Crystal structure of a phospholipase D family member. Nat. Struct. Biol. 6: 278-284.
76. ter Haar, E., Musacchio, A., Harrison, S.C., and Kirchhausen, T. 1998. Atomic structure of clathrin: A β propeller terminal domain joins an α zigzag linker. Cell 95: 563-573.
77. Tuckerman, M.E. and Martyna, G.J. 2000. Understanding modern molecular dynamics techniques and applications. J. Phys. Chem. 104: 159-178.
78. Varghese, J.N., Laver, W.G., and Colman, P.M. 1983. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303: 35-40.
79. Vellieux, F.M.D., Huitman, F., Groendijk, H., Kalk, K.H., Frank, J., Jongejan, J.A., Duine, J.A., Petrators, K., Drenth, J., and Hol, W.G.J. 1989. Structure of quinoprotein methylamine dehydrogenase at 2.25 Å resolution. EMBO J. 8: 2171-2178.
80. iαiβiγ2. Cell 83: 1047-1058.
81. Wang, S.X., Mure, M., Medzihradszky, K.F., Burlingame, A.L., Brown, D.E., Dooley, D.M., Smith, A.J., Kagan, H.M., and Klinman, J.P. 1996. A crosslinked cofactor in lysyl oxidase: Redox function for amino acid side chains. Science 274: 1078-1084.
82. Westheimer, F.H. 1987. Pyridine nucleotide enzymes. In Pyridine nucleotide coenzymes, Part A (eds. D. Dolphin et al.), p. 253. Wiley, New York.
83. Xia, Z.-X., Dai, W.-W., Zhang, Y.-F., White, S.A., Boyd, G.D., and Mathews, F.S. 1996. Determination of the gene sequence and the three-dimensional structure at 2.4 Å resolution of methanol dehydrogenase from Methylophilus W3A1. J. Mol. Biol. 259: 480-501.
84. Xia, Z.-X., He, Y.-N., Dai, W.-W., White, S.A., Boyd, G.D., and Mathews, F.S. 1999. Detailed active site configuration of a new crystal form of methanol dehydrogenase from Methylophilus W3A1 at 1.9 Å resolution. Biochemistry 38: 1214-1220.
85. Xia, Z.-X., Dai, W.-W., He, Y.-N., White, S.A., Mathews, F.S., and Davidson, V.L. 2003. X-ray structure of methanol dehydrogenase from Paracoccus denitrificans and molecular modeling of its interactions with cytochrome c-551i. J. Biol. Inorg. Chem. 8: 843-854.
86. Yamazaki, T., Kojima, K., and Sode, K. 2000. Extended-range glucose sensor employing engineered glucose dehydrogenase. Anal. Chem. 72: 4689-4693.
87. Ye, I., Hammeric, M., Olsthoorn, A.J.J., Schuhmann, W., Schmidth, H.L., and Duine, J.A. 1993. High current density "wired" quinoprotein glucose dehydrogenase electrode. Anal. Chem. 65: 238-241.
88. 2+ in the catalytic mechanism of quinoprotein methanol dehydrogenase. Proc. Natl. Acad. Sci. 94: 11881-11886.
89. Zheng, Y.-J., Xia, Z.-X., Chen, Z.-W., Mathews, F.S., and Bruice, T.C. 2001. Catalytic mechanism of quinoprotein methanol dehydrogenase: A theoretical and X-ray crystallographic investigation. Proc. Natl. Acad. Sci. 98: 432-434.