Crystal structures of penicillin-binding protein 2 from penicillin-susceptible and -resistant strains of neisseria gonorrhoeae reveal an unexpectedly subtle mechanism for antibiotic resistance

Journal of Biological Chemistry

Volumn 284, Issue 2, 2009, Pages 1202-1212

  Powell, Ailsa J ^a   Tomberg, Joshua ^b   Deacon, Ashley M ^c   Nicholas, Robert A ^b,c   Davies, Christopher ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITES; ANTIBIOTIC RESISTANCES; ASPARTATE; C TERMINUS; CONFORMATIONAL CHANGES; CONSERVED RESIDUES; GONORRHOEAE; HYDROGEN-BONDING NETWORKS; KINETIC ANALYSIS; MELTING CURVES; MOLECULAR MECHANISMS; MOLECULAR TARGETS; NEISSERIA GONORRHOEAE; PENICILLIN- BINDING PROTEINS; RESISTANT STRAINS; SECOND ORDERS; STRUCTURAL DIFFERENCES; THERMAL STABILITIES; WILD TYPES;

ACYLATION; ANTIBIOTICS; BINDING SITES; CHEMICAL REACTIONS; HYDROGEN; PLANTS (BOTANY); STRAIN; THERMODYNAMIC STABILITY;

CRYSTAL STRUCTURE;

ASPARTIC ACID; BETA LACTAM; CEFUROXIME; MUTANT PROTEIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 2; PENICILLIN G; UNCLASSIFIED DRUG;

ACYLATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG SENSITIVITY; HYDROGEN BOND; KINETICS; MOLECULAR MECHANICS; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TARGETING; THERMOSTABILITY; WILD TYPE;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEISSERIA GONORRHOEAE; PENICILLIN-BINDING PROTEINS; PENICILLINS; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE;

NEISSERIA GONORRHOEAE;

EID: 59449108342     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M805761200     Document Type: Article

References (74)

1. Centers for Disease Control. (2007) MMWR Morb. Mortal Wkly. Rep. 56, 332-336
2. Ameyama, S., Onodera, S., Takahata, M., Minami, S., Maki, N., Endo, K., Goto, H., Suzuki, H., and Oishi, Y. (2002) Antimicrob. Agents Chemother. 46, 3744-3749
3. Wang, S. A., Lee, M. V., O'Connor, N., Iverson, C. J., Ohye, R. G., Whiticar, P. M., Hale, J. A., Trees, D. L., Knapp, J.S., Effler, P. V., and Weinstock, H. S. (2003) Clin. Infect. Dis. 37, 849-852
4. Whiley, D. M., Limnios, E.A., Ray, S., Sloots, T.P., and Tapsall, J.W. (2007) Antimicrob. Agents Chemother. 51, 3111-3116
5. Lindberg, R., Fredlund, H., Nicholas, R., and Unemo, M. (2007) Antimicrob. Agents Chemother. 51, 2117-2122
6. Ghuysen, J. M. (1991) Annu. Rev. Microbiol. 45, 37-67
7. Ghuysen, J. M. (1994) Trends Microbiol. 2, 372-380
8. Holtje, J. V. (1998) Microbiol. Mol. Biol. Rev. 62, 181-203
9. Barbour, A. G. (1981) Antimicrob. Agents Chemother. 19, 316-322
10. Stefanova, M. E., Tomberg, J., Davies, C., Nicholas, R. A., and Gutheil, W. G. (2004) Eur. J. Biochem. 271, 23-32
11. Stefanova, M. E., Tomberg, J., Olesky, M., Holtje, J. V., Gutheil, W. G., and Nicholas, R. A. (2003) Biochemistry 42, 14614-14625
12. Ropp, P. A., and Nicholas, R. A. (1997) J. Bacteriol. 179, 2783-2787
13. Cannon, J. G., and Sparling, P. F. (1984) Annu. Rev. Microbiol. 38, 111-133
14. Faruki, H., and Sparling, P. F. (1986) Antimicrob. Agents Chemother. 30, 856-860
15. Spratt, B. G. (1988) Nature 332, 173-176
16. Ropp, P. A., Hu, M., Olesky, M., and Nicholas, R. A. (2002) Antimicrob. Agents Chemother. 46, 769-777
17. Gill, M. J., Simjee, S., Al-Hattawi, K., Robertson, B. D., Easmon, C. S., and Ison, C. A. (1998) Antimicrob. Agents Chemother. 42, 2799-2803
18. Olesky, M., Hobbs, M., and Nicholas, R. A. (2002) Antimicrob. Agents Chemother. 46, 2811-2820
19. Hagman, K. E., Pan, W., Spratt, B. G., Balthazar, J. T., Judd, R. C., and Shafer, W. M. (1995) Microbiology 141, 611-622
20. Veal, W. L., Nicholas, R. A., and Shafer, W. M. (2002) J. Bacteriol. 184, 5619-5624
21. Sparling, P. F., Sarubbi, F. A., Jr., and Blackman, E. (1975) J. Bacteriol. 124, 740-749
22. Dowson, C. G., Jephcott, A. E., Gough, K. R., and Spratt, B. G. (1989) Mol. Microbiol. 3, 35-41
23. Brannigan, J. A., Tirodimos, I. A., Zhang, Q. Y., Dowson, C. G., and Spratt, B. G. (1990) Mol. Microbiol. 4, 913-919
24. Tipper, D. J., and Strominger, J. L. (1965) Proc. Natl. Acad. Sci. U. S. A. 54, 1133-1141
25. Yocum, R. R., Waxman, D. J., Rasmussen, J. R., and Strominger, J. L. (1979) Proc. Natl. Acad. Sci. U. S. A. 76, 2730-2734
26. Mouz, N., Gordon, E., Di Guilmi, A. M., Petit, I., Petillot, Y., Dupont, Y., Hakenbeck, R., Vernet, T., and Dideberg, O. (1998) Proc. Natl. Acad. Sci. U.S.A. 95, 13403-13406
27. Dessen, A., Mouz, N., Gordon, E., Hopkins, J., and Dideberg, O. (2001) J. Biol. Chem. 276, 45106-45112
28. Lim, D., and Strynadka, N. C. (2002) Nat. Struct. Biol. 9, 870-876
29. Contreras-Martel, C., Job, V., Di Guilmi, A. M., Vernet, T., Dideberg, O., and Dessen, A. (2006) J. Mol. Biol. 355, 684-696
30. Carapito, R., Chesnel, L., Vernet, T., and Zapun, A. (2006) J. Biol. Chem. 281, 1771-1777
31. Job, V., Carapito, R., Vernet, T., Dessen, A., and Zapun, A. (2008) J. Biol. Chem. 283, 4886-4894
32. Gordon, E., Mouz, N., Duee, E., and Dideberg, O. (2000) J. Mol. Biol. 299, 477-485
33. Chesnel, L., Pernot, L., Lemaire, D., Champelovier, D., Croize, J., Dideberg, O., Vernet, T., and Zapun, A. (2003) J. Biol. Chem. 278, 44448-44456
34. Pernot, L., Chesnel, L., Le Gouellec, A., Croize, J., Vernet, T., Dideberg, O., and Dessen, A. (2004) J. Biol. Chem. 279, 16463-16470
35. Maness, M. J., and Sparling, P. F. (1973) J. Infect. Dis. 128, 321-330
36. Frere, J. M., Nguyen-Disteche, M., Coyette, J., and Joris, B. (1992) in The Chemistry of β-lactams (Page, M. I., ed) pp. 148-196, Chapman & Hall, Glasgow
37. Matthews, B. (1968) J. Mol. Biol. 33, 491-497
38. McPhillips, T. M., McPhillips, S. E., H. J. C., Cohen, A. E., Deacon, A. M., Ellis, P. J., Garman, E., Gonzalez, A., Sauter, N. K., Phizackerley, R. P., Soltis, S. M., and Kuhn, P. (2002) J. Synchrotron Radiat. 9, 401-406
39. Otwinowski, Z., and Minor, W. (1997) Methods Enzymol. 276, 307-326
40. Terwilliger, T., and Berendzen, J. (1999) Acta Crystallogr. Sect. D 55, 849-861
41. Terwilliger, T. (2000) Acta Crystallogr. D 56, 965-972
42. Terwilliger, T. C. (2002) Acta Cryst. D 58, 1937-1940
43. Leslie, A. G. W. (1992) Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography No. 26
44. CCP4 (1994) Acta Crystallogr. Sect. D 50, 760-763
45. Jones, T. A., Zou, J.-Y., Cowan, S. W., and Kjeldgaard, M. (1991) Acta Crystallogr. Sect. A 47, 110-119
46. Brünger, A. T. (1992) X-PLOR, Version 3.1, A System for X-ray Crystallography and NMR, Yale University, New Haven, CT
47. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Acta Crystallogr. Sect D 53, 240-255
48. Lamzin, V. S., and Wilson, K. S. (1993) Acta Crystallogr. Sect. D 49, 129-147
49. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) J.Appl. Crystallogr. 26, 283-291
50. Davies, C., White, S. W., and Nicholas, R. A. (2001) J.Biol. Chem. 276, 616-623
51. Marrec-Fairley, M., Piette, A., Gallet, X., Brasseur, R., Hara, H., Fraipont, C., Ghuysen, J. M., and Nguyen-Disteche, M. (2000) Mol. Microbiol. 37, 1019-1031
52. Mercer, K. L., and Weiss, D. S. (2002) J. Bacteriol. 184, 904-912
53. Morlot, C., Noirclerc-Savoye, M., Zapun, A., Dideberg, O., and Vernet, T. (2004) Mol. Microbiol. 51, 1641-1648
54. Wissel, M. C., and Weiss, D. S. (2004) J. Bacteriol. 186, 490-502
55. Pares, S., Mouz, N., Petillot, Y., Hakenbeck, R., and Dideberg, O. (1996) Nat. Struct. Biol. 3, 284-289
56. Mouz, N., Di Guilmi, A. M., Gordon, E., Hakenbeck, R., Dideberg, O., and Vernet, T. (1999) J. Biol. Chem. 274, 19175-19180
57. Graves-Woodward, K., and Pratt, R. F. (1998) Biochem. J. 332, 755-761
58. Nicholas, R. A., Krings, S., Tomberg, J., Nicola, G., and Davies, C. (2003) J. Biol. Chem. 278, 52826-52833
59. Schultz, D. E., Spratt, B. G., and Nicholas, R. A. (1991) Protein Expression Purif. 2, 339-349
60. Cruickshank, D. W. (1999) Acta. Crystallogr. D Biol. Crystallogr. 55, 583-601
61. Harel, M., Kryger, G., Rosenberry, T. L., Mallender, W. D., Lewis, T., Fletcher, R. J., Guss, J. M., Silman, I., and Sussman, J. L. (2000) Protein Sci. 9, 1063-1072
62. Muzammil, S., Ross, P., and Freire, E. (2003) Biochemistry 42, 631-638
63. Podust, L. M., Poulos, T. L., and Waterman, M. R. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 3068-3073
64. Kishida, H., Unzai, S., Roper, D. I., Lloyd, A., Park, S. Y., and Tame, J. R. (2006) Biochemistry 45, 783-792
65. Macheboeuf, P., Di Guilmi, A. M., Job, V., Vernet, T., Dideberg, O., and Dessen, A. (2005) Proc. Natl. Acad. Sci. U. S. A. 102, 577-582
66. Yamada, M., Watanabe, T., Baba, N., Takeuchi, Y., Ohsawa, F., and Gomi, S. (2008) Antimicrob. Agents Chemother. 52, 2053-2060
67. Garcia-Bustos, J., and Tomasz, A. (1990) Proc. Natl. Acad. Sci. U. S. A. 87, 5415-5419
68. Severin, A., Figueiredo, A. M., and Tomasz, A. (1996) J. Bacteriol. 178, 1788-1792
69. Antignac, A., Boneca, I. G., Rousselle, J. C., Namane, A., Carlier, J. P., Vazquez, J. A., Fox, A., Alonso, J. M., and Taha, M. K. (2003) J. Biol. Chem. 278, 31529-31535
70. Rybkine, T., Mainardi, J. L., Sougakoff, W., Collatz, E., and Gutmann, L. (1998) J. Infect. Dis. 178, 159-163
71. Sauvage, E., Kerff, F., Fonze, E., Herman, R., Schoot, B., Marquette, J. P., Taburet, Y., Prevost, D., Dumas, J., Leonard, G., Stefanic, P., Coyette, J., and Charlier, P. (2002) Cell. Mol. Life Sci. 59, 1223-1232
72. Ito, M., Deguchi, T., Mizutani, K. S., Yasuda, M., Yokoi, S., Ito, S., Taka-hashi, Y., Ishihara, S., Kawamura, Y., and Ezaki, T. (2005) Antimicrob. Agents Chemother. 49, 137-143
73. Takahata, S., Senju, N., Osaki, Y., Yoshida, T., and Ida, T. (2006) Antimi-crob. Agents Chemother. 50, 3638-3645
74. Spratt, B. G., and Cromie, K. D. (1988) Rev. Infect. Dis. 10, 699-711