Mutation of Tyr137 of the universal Escherichia coli fimbrial adhesin FimH relaxes the tyrosine gate prior to mannose binding

IUCrJ

Volumn 4, Issue , 2017, Pages 7-23

  Rabbani, Said ^a   Krammer, Eva Maria ^b,c   Roos, Goedele ^b,c   Zalewski, Adam ^a   Preston, Roland ^a   Eid, Sameh ^a   Zihlmann, Pascal ^a   Prévost, Martine ^c   Lensink, Marc F ^b   Thompson, Andrew ^d   Ernst, Beat ^a   Bouckaert, Julie ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIV LILLE   (France)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d SYNCHROTRON SOLEIL   (France)

Author keywords

biphenyl mannose; crystals; Escherichia coli infection; FimH adhesin; heptyl mannose; molecular dynamics; molecular recognition; mutations; peptide torsions; protein structure; thermodynamics; tyrosine gate; X ray crystallography

Indexed keywords

EID: 85009132048     PISSN: None     EISSN: 20522525     Source Type: Journal    
DOI: 10.1107/S2052252516016675     Document Type: Article

References (62)

1. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. & Terwilliger, T. C. (2002). Acta Cryst. D58, 1948-1954.
2. Andersen, H. C. (1983). J. Comput. Phys. 52, 24-34.
3. Anderson, G., Dodson, K., Hooton, T. & Hultgren, S. (2004). Trends Microbiol. 12, 424-430.
4. Aprikian, P., Tchesnokova, V., Kidd, B., Yakovenko, O., Yarov-Yarovoy, V., Trinchina, E., Vogel, V., Thomas, W. & Sokurenko, E. (2007). J. Biol. Chem. 282, 23437-23446.
5. Bas, D. C., Rogers, D.M. & Jensen, J. H. (2008). Proteins, 73, 765-783.
6. Bitsch, F., Aichholz, R., Kallen, J., Geisse, S., Fournier, B. & Schlaeppi, J.-M. (2003). Anal. Biochem. 323, 139-149.
7. Bouckaert, J. et al. (2005). Mol. Microbiol. 55, 441-455.
8. Bouckaert, J., Li, Z., Xavier, C., Almant, M., Caveliers, V., Lahoutte, T., Weeks, S. D., Kovensky, J. & Gouin, S. G. (2013). Chem. Eur. J. 19, 7847-7855.
9. Brument, S., Sivignon, A., Dumych, T. I., Moreau, N., Roos, G., Guérardel, Y., Chalopin, T., Deniaud, D., Bilyy, R. O., Darfeuille-Michaud, A., Bouckaert, J. & Gouin, S. G. (2013). J. Med. Chem. 56, 5395-5406.
10. Chalopin, T., Alvarez Dorta, D., Sivignon, A., Caudan, M., Dumych, T. I., Bilyy, R. O., Deniaud, D., Barnich, N., Bouckaert, J. & Gouin, S. G. (2016). Org. Biomol. Chem. 14, 3913-3925.
11. Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S. & Richardson, D. C. (2010). Acta Cryst. D66, 12-21.
12. Choudhury, D., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J., Hultgren, S. J. & Knight, S. D. (1999). Science, 285, 1061-1066.
13. Contreras-García, J., Johnson, E. R., Keinan, S., Chaudret, R., Piquemal, J.-P., Beratan, D. N. & Yang, W. (2011). J. Chem. Theory Comput. 7, 625-632.
14. Cusumano, C. K., Pinkner, J. S., Han, Z., Greene, S. E., Ford, B. A., Crowley, J. R., Henderson, J. P., Janetka, J. W. & Hultgren, S. J. (2011). Sci. Transl. Med. 3, 109ra115.
15. Darden, T., York, D. & Pedersen, L. (1993). J. Chem. Phys. 98, 10089.
16. Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A.-L., Barnich, N., Bringer, M.-A., Swidsinski, A., Beaugerie, L. & Colombel, J.-F. (2004). Gastroenterology, 127, 412-421.
17. Daura, X., Gademann, K., Jaun, B., Seebach, D., van Gunsteren, W. F. & Mark, A. E. (1999). Angew. Chem. Int. Ed. 38, 236-240.
18. Durka, M., Buffet, K., Iehl, J., Holler, M., Nierengarten, J.-F., Taganna, J., Bouckaert, J. & Vincent, S. P. (2011). Chem. Commun. 47, 1321-1323.
19. Fiege, B., Rabbani, S., Preston, R. C., Jakob, R. P., Zihlmann, P., Schwardt, O., Jiang, X., Maier, T. & Ernst, B. (2015). Chembiochem, 16, 1235-1246.
20. Firon, N., Ashkenazi, S., Mirelman, D., Ofek, I. & Sharon, N. (1987). Infect. Immun. 55, 472-476.
21. Frisch, M. J. et al. (2009). Gaussian 09. Gaussian Inc., Wallingford, Connecticut, USA.
22. Geerlings, S. E., Beerepoot, M. A. J. & Prins, J. M. (2014). Infect. Dis. Clin. North Am. 28, 135-147.
23. Goneau, L. W., Hannan, T. J., MacPhee, R. A., Schwartz, D. J., Macklaim, J. M., Gloor, G. B., Razvi, H., Reid, G., Hultgren, S. J. & Burton, J. P. (2015). mBio, 6, e00356-15.
24. Gouin, S. G., Roos, G. & Bouckaert, J. (2014). Top. Med Chem., 12, 123-168.
25. Guvench, O., Mallajosyula, S. S., Raman, E. P., Hatcher, E., Vanommeslaeghe, K., Foster, T. J., Jamison, F. W. & MacKerell, A. D. (2011). J. Chem. Theory Comput. 7, 3162-3180.
26. Han, Z., Pinkner, J. S., Ford, B., Chorell, E., Crowley, J. M., Cusumano, C. K., Campbell, S., Henderson, J. P., Hultgren, S. J. & Janetka, J. W. (2012). J. Med. Chem. 55, 3945-3959.
27. Han, Z., Pinkner, J. S., Ford, B., Obermann, R., Nolan, W., Wildman, S. A., Hobbs, D., Ellenberger, T., Cusumano, C. K., Hultgren, S. J. & Janetka, J. W. (2010). J. Med. Chem. 53, 4779-4792.
28. Hartmann, M. & Lindhorst, T. K. (2011). Eur. J. Org. Chem. 2011, 3583-3609.
29. Heinig, M. & Frishman, D. (2004). Nucleic Acids Res. 32, W500- W502.
30. Hooton, T. M. & Stamm, W. E. (1997). Infect. Dis. Clin. North Am. 11, 551-581.
31. Houtman, J. C. D., Brown, P. H., Bowden, B., Yamaguchi, H., Appella, E., Samelson, L. E. & Schuck, P. (2007). Protein Sci. 16, 30-42.
32. Humphrey, W., Dalke, A. & Schulten, K. (1996). J. Mol. Graph. 14, 33-38.
33. Hung, C.-S., Bouckaert, J., Hung, D., Pinkner, J., Widberg, C., DeFusco, A., Auguste, C. G., Strouse, R., Langermann, S., Waksman, G. & Hultgren, S. J. (2002). Mol. Microbiol. 44, 903-915.
34. Karplus, P. A. & Diederichs, K. (2015). Curr. Opin. Struct. Biol. 34, 60-68.
35. Kleeb, S. et al. (2015). J. Med. Chem. 58, 2221-2239.
36. Klein, T. et al. (2010). J. Med. Chem. 53, 8627-8641.
37. Le Trong, I., Aprikian, P., Kidd, B. A., Forero-Shelton, M., Tchesnokova, V., Rajagopal, P., Rodriguez, V., Interlandi, G., Klevit, R., Vogel, V., Stenkamp, R. E., Sokurenko, E. V. & Thomas, W. E. (2010). Cell, 141, 645-655.
38. Le Trong, I., Aprikian, P., Kidd, B. A., Thomas, W. E., Sokurenko, E. V. & Stenkamp, R. E. (2010). J. Struct. Biol. 172, 380-388.
39. MacKerell, A. D. et al. (1998). J. Phys. Chem. B, 102, 3586-3616.
40. MacKerell, A. D., Feig, M. & Brooks, C. L. (2004). J. Comput. Chem. 25, 1400-1415.
41. Mallajosyula, S. S. & MacKerell, A. D. (2011). J. Phys. Chem. B, 115, 11215-11229.
42. Meerman, H. J. & Georgiou, G. (1994). Biotechnology, 12, 1107-1110.
43. Mydock-McGrane, L. K., Cusumano, Z. T. & Janetka, J. W. (2016). Expert Opin. Ther. Pat. 26, 175-197.
44. Pace, C. N. (1986). Methods Enzymol. 131, 266-280.
45. Pang, L., Kleeb, S., Lemme, K., Rabbani, S., Scharenberg, M., Zalewski, A., Schädler, F., Schwardt, O. & Ernst, B. (2012). ChemMedChem, 7, 1404-1422.
46. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L. & Schulten, K. (2005). J. Comput. Chem. 26, 1781-1802.
47. Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B. & Lindahl, E. (2013). Bioinformatics, 29, 845-854.
48. Rabbani, S., Jiang, X., Schwardt, O. & Ernst, B. (2010). Anal. Biochem. 407, 188-195.
49. Roos, G., Wellens, A., Touaibia, M., Yamakawa, N., Geerlings, P., Roy, R., Wyns, L. & Bouckaert, J. (2013). ACS Med. Chem. Lett. 4, 1085-1090.
50. de Ruyck, J., Lensink, M. F. & Bouckaert, J. (2016). IUCrJ, 3, 163-167.
51. Sambrook, J. (1989). Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory.
52. Schüttelkopf, A. W. & van Aalten, D. M. F. (2004). Acta Cryst. D60, 1355-1363.
53. Singaravelu, M., Selvan, A. & Anishetty, S. (2014). Comput. Biol. Chem. 52, 18-24.
54. Sivignon, A., Yan, X., Alvarez Dorta, D., Bonnet, R., Bouckaert, J., Fleury, E., Bernard, J., Gouin, S. G., Darfeuille-Michaud, A. & Barnich, N. (2015). mBio, 6, e01298-15.
55. Smart, O. S., Womack, T. O., Flensburg, C., Keller, P., Paciorek, W., Sharff, A., Vonrhein, C. & Bricogne, G. (2012). Acta Cryst. D68, 368-380.
56. Thomas, W. E., Trintchina, E., Forero, M., Vogel, V. & Sokurenko, E. V. (2002). Cell, 109, 913-923.
57. Tuckerman, M., Berne, B. J. & Martyna, G. J. (1992). J. Chem. Phys. 97, 1990.
58. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I. & MacKerell, A. D. (2010). J. Comput. Chem. 31, 671-690.
59. Vetsch, M., Sebbel, P. & Glockshuber, R. (2002). J. Mol. Biol. 322, 827-840.
60. Wellens, A., Garofalo, C., Nguyen, H., Van Gerven, N., Slättegård, R., Hernalsteens, J.-P., Wyns, L., Oscarson, S., De Greve, H., Hultgren, S. & Bouckaert, J. (2008). PLoS One, 3, e2040.
61. Wellens, A., Lahmann, M., Touaibia, M., Vaucher, J., Oscarson, S., Roy, R., Remaut, H. & Bouckaert, J. (2012). Biochemistry, 51, 4790-4799.
62. Wiseman, T., Williston, S., Brandts, J. F. & Lin, L.-N. (1989). Anal. Biochem. 179, 131-137.