The conformational free energy landscape of β-D-glucopyranose. Implications for substrate preactivation in β-glucoside hydrolases

Journal of the American Chemical Society

Volumn 129, Issue 35, 2007, Pages 10686-10693

  Biarnés, Xevi ^a   Ardèvol, Albert ^a,b   Planas, Antoni ^b   Rovira, Carme ^a,c   Laio, Alessandro ^d   Parrinello, Michele ^e  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT QUÍMIC DE SARRIÀ   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d SISSA   (Italy)

^e ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CHARGE DISTRIBUTION; CONFORMATIONS; ELECTRONIC PROPERTIES; FREE ENERGY; GLUCOSE; SHRINKAGE;

CONFORMATIONAL FREE ENERGY; METADYNAMICS; X-RAY STRUCTURES;

ENZYMES;

GLUCOPYRANOSIDE; GLYCOSIDASE; DRUG DERIVATIVE; GLUCOSE;

AB INITIO CALCULATION; ARTICLE; CARBOHYDRATE ANALYSIS; ENERGY; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; STRUCTURE ANALYSIS; X RAY ANALYSIS; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; METABOLISM; THERMODYNAMICS;

CARBOHYDRATE CONFORMATION; COMPUTER SIMULATION; GLUCOSE; GLYCOSIDE HYDROLASES; THERMODYNAMICS;

EID: 34848879539     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja068411o     Document Type: Article

References (73)

1. Hurtley, S., Service, R., Szuromi, P., Eds. Science 2001, 291, 2263-2502.
2. Davies, G.; Henrissat, B. Structure 1995, 3, 853-859.
3. Sinnott, M. L. Chem. Rev. 1990, 90, 1171-1202.
4. Davies, G.; Sinnott, M. L.; Withers, S. G. Glycosyl Transfer. In Comprehensive Biological Catalysis; Sinnott, M. L., Ed.; Academic Press Ltd.: San Diego, CA, 1998; Chapter 3, pp 119-209.
5. Heightman, T. D.; Vasella, A. Angew. Chem., Int. Ed. 1999, 38, 750-770.
6. Zechel, D. L.; Withers, S. G. Acc. Chem. Res. 2000, 33, 11-18.
7. Carbohydrate-Active enZYmes. http://afmb.cnrs-mrs.fr/cazy/CAZY/ index.html.
8. Coutinho, P. M.; Henrissat, B. Carbohydrate-active enzymes: An integrated database approach. In Recent Advances in Carbohydrate Bioengineering. Gilbert, H. J., Davies, G. J., Henrissat, B., Svensson, B., Eds.; The Royal Society of Chemistry: Cambridge, U.K., 1999.
9. Yip, V. L. Y.; Varrot, A.; Davies, G. J.; Rajan, S. S.; Yang, X.; Thompson, J.; Anderson, W. F.; Withers, S. G. J. Am. Chem. Soc. 2004, 126, 8354-8355.
10. Davies, G. J.; Ducros, V. M.-A.; Varrot, A.; Zechel, D. L. Biochem. Soc. Trans. 2003, 31, 523-527.
11. Taylor, E. J.; Goyal, A.; Guerreiro, C. I. P. D.; Prates, J. A. M.; Money, V.; Ferry, N.; Morland, C.; Planas, A.; Macdonald, J. A.; Stick, R. V.; Gilbert, H. J.; Fontes, C. M. G. A.; Davies, G. J. J. Biol. Chem. 2005, 280, 32761-32767.
12. Money, V. A.; Smith, N. L.; Scaffidi, A.; Stick, R. V.; Gilbert, H. J.; Davies, G. J. Angew. Chem., Int. Ed. 2006, 45, 5136-5140.
13. Biarnés, X.; Nieto, J.; Planas, A.; Rovira, C. J. Biol. Chem. 2006, 281, 1432-1441 and references therein.
14. Nerinckx, W.; Desmet, T.; Claeyssens, M. Arkivoc 2006, 13, 90-116 and references therein.
15. Kirby, A. J. Stereoelectronic effects on acetal hydrolysis. Acc. Chem. Res. 1984, 17, 305-311.
16. Stoddart, J. F. In Stereochemistry of Carbohydrates; Wiley-Interscience: Toronto, Canada, 1971.
17. (a) IUPAC-IUP Joint Commission on Biochemical Nomenclature. Arch. Biochem. Biophys. 1981, 207, 469-472.
18. (b) The names C, B, S stand for chair, boat, and skew, respectively. Each ring structure has four atoms that approximately define a plane. The first numeral (sometimes written as superscript) indicates the number of the ring carbon atom above the plane, and the second numeral (subscript) indicates the number of the ring carbon atom below the plane.
19. 4 (projection from the south pole). In this work we focus on the North pole projection because the substrate distortions found in all the currently available structures of Michaelis complexes of β-glucoside hydrolases belong to this projection.
20. See for instance: (a) Jeffrey, G.; Taylor, R. J. Comput. Chem. 1980, 1, 99-109.
21. (b) Woods, R.; Szarek, W.; Smith, V. A. J. Chem. Soc., Chem. Commun. 1991, 5, 334-337.
22. (c) McNamara, J. P.; Muslim, A.-M.; Abdel-Aal, H.; Wang, H.; Mohr, M.; Hillier, I. H.; Bryce, R. A. Chem. Phys. Lett. 2004, 394, 429-436.
23. (d) Brady, J. W. J. Am. Chem. Soc. 1986, 108, 8153-8160.
24. (e) Ha, S.; Gao, J.; Tidor, B.; Brady, J. W.; Karplus, M. J. Am. Chem. Soc. 1991, 113, 1553-1557.
25. (f) Barrows, S. E.; Storer, J. W.; Cramer, C. J.; French, A. D.; Truhlar, D. G. J. Comput. Chem. 1998, 19, 1111-1129.
26. (g) Barrows, S. E.; Dulles, F. J.; Cramer, C. J.; French, A. D.; Truhlar, D. G. Carbohydr. Res. 1995, 276, 219-251.
27. (a) Tvaroska, I.; André, I.; Carver, J. P. J. Am. Chem. Soc. 2000, 122, 8762-8776.
28. (b) Molteni, C.; Parrinello, M. Chem. Phys. Lett. 1997, 275, 409-413.
29. (c) Molteni, C.; Parrinello, M. J. Am. Chem. Soc. 1998, 120, 2168-2171.
30. (d) Fernández-Alonso, M. C.; Cañada, J.; Jiménez-Barbero, J.; Cuevas, G. ChemPhysChem. 2005, 6, 671-680.
31. Cramer, C. J.; Truhlar, D. G. J. Am. Chem. Soc. 1993, 115, 5745-5753.
32. Concerning the difficulty of exploring all conformations of the exocyclic groups for other sugar rings see for instance: (a) Stortz, C. A. Carbohydr. Res. 1999, 322, 77-86.
33. (b) Schnupf, U.; Willett, J. L.; Bosma, W. B.; Momany, F. A. Carbohydr. Res. 2007, 342, 196-216.
34. O'Donoghue, P.; Luthey-Schulten, Z. A. J. Phys. Chem. B 2000, 104, 10398-10405.
35. Appell, M.; Strati, G.; Willett, J. L.; Momany, F. A. Carbohydr. Res. 2004, 339, 537-551.
36. Momany, F. A.; Appell, M.; Strati, G.; Willett, J. L. Carbohydr. Res. 2004, 339, 553-567.
37. (a) Ionescu, A. R.; Berces, A.; Zgierski, M. Z.; Whitfield, D. M.; Nukada, T. J. Phys. Chem. A 2005, 109, 8096-8105.
38. (b) Kurihara, Y.; Ueda, K. Carbohvd. Res. 2006, 341, 2565-2574.
39. (c) Momany, F. A.; Appell, M.; Willett, J. L.; Schnupt, U.; Bosma, W. B. Carbohydr. Res. 2006, 341, 525-537.
40. (d) Karamat, S.; Fabian, W. M. F. J. Phys. Chem. A 2006, 110, 7477-7484.
41. (e) French, A. D.; Dowd, M. K. J. Mol. Struct. (Theochem) 1997, 395-396, 271-287.
42. Joshi, N.; Rao, V. S. Biopolymers 1979, 18, 2993-3004.
43. Dowd, M. K.; French, A. D.; Reilly, P. J. Carbohydr. Res. 1994, 264, 1-19.
44. Cremer, D.; Pople, J. A. J. Am. Chem. Soc. 1975, 97, 1354-1358.
45. (a) Haasnoot, C. A. G. J. Am. Chem. Soc. 1992, 114, 882-887.
46. (b) Rao, V. S.; Chandrasekaran, R.; Qasba, P. K.; Balaji, P. V. Conformation of Carbohydrates; Harwood Academic Publishers: Amsterdam, The Netherlands, 1998; p 56.
47. (c) French, A. D.; Brady, J. W. ACS Symp. Ser. 1990, 430, 120-140.
48. (a) Ensing, B.; De Vivo, M.; Liu, Z. W.; Moore, P.; Klein, M. L. Acc. Chem. Res. 2006, 39, 73-81.
49. (b) Ensing, B.; Laio, A.; Parrinello, M.; Klein, M. L. J. Phys. Chem. 2005, 109, 6676-6687.
50. (c) Laio, A.; Rodriguez-Fortea, A.; Gervasio, F. L.; Ceccarelli, M.; Panrinello, M. J. Phys. Chem. B 2005, 109, 6714-6721.
51. Laio, A.; Parrinello, M. Proc. Nat. Acad. Sci. U.S.A. 2002, 99, 12562-12566.
52. Recent applications include: (a) Blumberger, J.; Ensing, B.; Klein, M. L. Angew. Chem., Int. Ed. 2006, 45, 2893-2897.
53. (b) Fiorin, G.; Pastore, A.; Carloni, P.; Parrinello, M. Biophys. J. 2006, 91, 2768-2777.
54. (c) Martoñak, R.; Donadio, D.; Oganov, A. R.; Parrinello, M. Nat. Mater. 2006, 5, 623-626.
55. (d) Oganov, A. R.; Martoñak, R.; Laio, A.; Raiteri, P.; Parrinello, M. Nature 2005, 438, 1142-1144.
56. (e) Rodriguez-Fortea, A.; Iannuzzi, M.; Parrinello, M. J. Phys. Chem. B 2006, 110, 3477-3484.
57. (f) Rodriguez-Fortea, A.; Iannuzzi, M.; Parrinello, M. J. Phys. Chem. C 2007, ASAP.
58. Iannuzzi, M.; Laio, A.; Parrinello, M. Phys. Rev. Lett. 2003, 90, 238302-(4).
59. Car, R.; Parrinello, M. Phys. Rev. Lett. 1985, 55, 2471-2474.
60. Troullier, M.; Martins, J. L. Phys. Rev. B 1991, 43, 1993-2006.
61. Perdew, J. P.; Burke, K.; Ernzerhof, M. Phys. Rev. Lett. 1996, 77, 3865-3868. Erratum: Phys. Rev. Lett. 1997, 78, 1396.
62. Ireta, J.; Neugebauer, J.; Sheffler, M. J. Phys. Chem. A 2004, 108, 5692-5698.
63. Papanikolau, Y.; Prag, G.; Tavias, G.; Vorgias, C. E.; Oppenheim, A. B.; Petratos, K. Biochemistry 2001, 40, 11338-11343.
64. Van Aalten, D. M. F.; Komander, D.; Synstad, B.; Gseidnes, S.; Peter, M. G.; Eijsink, V. G. H. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 8979-8984.
65. Markovic-Housley, Z.; Miglierini, G.; Soldatova, L.; Rizkallah, P. J.; Muller, U.; Schirmer, T. Struct. Fold. Des. 2000, 8, 1025-1035.
66. Sulzenbacher, G.; Driguez, H.; Henrissat, B.; Schulein, M.; Davies, G. J. Biochemistry 1996, 35, 15280-15287.
67. Verdoucq, L.; Moriniere, J.; Bevan, D. R.; Esen, A.; Vasella, A.; Henrissat, B.; Czjzek, M. J. Biol. Chem. 2004, 279, 31796-31803.
68. Davies, G. J.; Mackenzie, L.; Varrot, A.; Dauter, M.; Brzozowski, A. M.; Schulein, M.; Withers, S. G. Biochemistry 1998, 37, 11707-11713.
69. Czjzek, M.; Cicek, M.; Zamboni, V.; Bevan, D. R.; Henrissat, B.; Esen, A. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 13555-13560.
70. Sandgren, M.; Berglund, G. I.; Shaw, A.; Stahlberg, J.; Kenne, L.; Desmet, T.; Mitchinson, C. J. Mol. Biol. 2004, 342, 1505-1517.
71. Varrot, A.; Frandsen, T.; Driguez, H.; Davies, G. Acta Crystallogr., Sect. D 2002, 58, 2201-2204.
72. Varrot, A.; Macdonald, J.; Stick, R. V.; Pell, G.; Gilbert, H. J.; Davies, G. J. Chem. Commun. 2003, 21, 946-947.
73. Guerin, D. M.; Lascombe, M. B.; Costabel, M.; Souchon, H.; Lamzin, V.; Beguin, P.; Alzari, P. M. J. Mol. Biol. 2002, 316, 1061-1069.