Ultrahigh resolution and full-length pilin structures with insights for filament assembly, pathogenic functions, and vaccine potential

Journal of Biological Chemistry

Volumn 286, Issue 51, 2011, Pages 44254-44265

  Hartung, Sophia ^a   Arvai, Andrew S ^b   Wood, Timothy ^b   Kolappan, Subramaniapillai ^c   Shin, David S ^a   Craig, Lisa ^c   Tainer, John A ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY FORMATION; FILAMENT ASSEMBLY; FRANCISELLA TULARENSIS; HUMAN PATHOGENS; IV PILI; MEMBRANE PROTEINS; N-TERMINALS; SALT BRIDGES; SUB-DOMAINS; SUBDOMAIN; THERAPEUTIC TARGETS; TYPE IV PILIN; ULTRAHIGH RESOLUTION;

BIOLOGICAL MEMBRANES; PROTEINS;

VACCINES;

AMINE; BACTERIAL PROTEIN; BACTERIAL VACCINE; CARBOXYL GROUP; CYSTEINE; DIMER; DISULFIDE; EPITOPE; GLUTAMIC ACID; OXYGEN; PILIN; PROTEIN FIMA; PROTEIN PILE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DICHELOBACTER NODOSUS; FRANCISELLA TULARENSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEROTYPE; VACCINE PRODUCTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL VACCINES; CRYSTALLOGRAPHY, X-RAY; DICHELOBACTER NODOSUS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYMERS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 83755168835     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.297242     Document Type: Article

References (73)

1. Mattick, J. S. (2002) Annu. Rev. Microbiol. 56, 289-314
2. Pelicic, V. (2008) Mol. Microbiol. 68, 827-837
3. Craig, L., Pique, M. E., and Tainer, J. A. (2004) Nat. Rev. Microbiol. 2, 363-378
4. Craig, L., Taylor, R. K., Pique, M. E., Adair, B. D., Arvai, A. S., Singh, M., Lloyd, S. J., Shin, D. S., Getzoff, E. D., Yeager, M., Forest, K. T., and Tainer, J. A. (2003) Mol. Cell 11, 1139-1150
5. Parge, H. E., Forest, K. T., Hickey, M. J., Christensen, D. A., Getzoff, E. D., and Tainer, J. A. (1995) Nature 378, 32-38
6. Craig, L., Volkmann, N., Arvai, A. S., Pique, M. E., Yeager, M., Egelman, E. H., and Tainer, J. A. (2006) Mol. Cell 23, 651-662
7. Gil, H., Benach, J. L., and Thanassi, D. G. (2004) Infect. Immun. 72, 3042-3047
8. Xicohtencatl-Cortes, J., Monteiro-Neto, V., Saldaña, Z., Ledesma, M. A., Puente, J. L., and Girón, J. A. (2009) J. Bacteriol. 191, 411-421
9. Ayers, M., Howell, P. L., and Burrows, L. L. (2010) Future Microbiol. 5, 1203-1218
10. Craig, L., and Li, J. (2008) Curr. Opin. Struct. Biol. 18, 267-277
11. Källström, H., Liszewski, M. K., Atkinson, J. P., and Jonsson, A. B. (1997) Mol. Microbiol. 25, 639-647
12. Merz, A. J., So, M., and Sheetz, M. P. (2000) Nature 407, 98-102
13. Wolfgang, M., Lauer, P., Park, H. S., Brossay, L., Hébert, J., and Koomey, M. (1998) Mol. Microbiol. 29, 321-330
14. Maier, B., Potter, L., So, M., Long, C. D., Seifert, H. S., and Sheetz, M. P. (2002) Proc. Natl. Acad. Sci. U.S.A. 99, 16012-16017
15. Criss, A. K., Kline, K. A., and Seifert, H. S. (2005) Mol. Microbiol. 58, 510-519
16. Forest, K. T., Bernstein, S. L., Getzoff, E. D., So, M., Tribbick, G., Geysen, H. M., Deal, C. D., and Tainer, J. A. (1996) Infect. Immun. 64, 644-652
17. Virji, M., and Heckels, J. E. (1984) J. Gen. Microbiol. 130, 1089-1095
18. Kennan, R. M., Dhungyel, O. P., Whittington, R. J., Egerton, J. R., and Rood, J. I. (2001) J. Bacteriol. 183, 4451-4458
19. Egerton, J. R., Roberts, D. S., and Parsonson, I. M. (1969) J. Comp. Pathol. 79, 207-215
20. Kennan, R. M., Han, X., Porter, C. J., and Rood, J. I. (2011) Vet. Microbiol. 153, 59-66
21. Han, X., Kennan, R. M., Davies, J. K., Reddacliff, L. A., Dhungyel, O. P., Whittington, R. J., Turnbull, L., Whitchurch, C. B., and Rood, J. I. (2008) J. Bacteriol. 190, 3323-3335
22. Han, X., Kennan, R. M., Parker, D., Davies, J. K., and Rood, J. I. (2007) J. Bacteriol. 189, 5022-5033
23. Kirn, T. J., Bose, N., and Taylor, R. K. (2003) Mol. Microbiol. 49, 81-92
24. Claxton, P. D., Ribeiro, L. A., and Egerton, J. R. (1983) Aust. Vet. J. 60, 331-334
25. Mattick, J. S., Anderson, B. J., Cox, P. T., Dalrymple, B. P., Bills, M. M., Hobbs, M., and Egerton, J. R. (1991) Mol. Microbiol. 5, 561-573
26. Sjöstedt, A. (2007) Ann. N.Y. Acad. Sci. 1105, 1-29
27. Ellis, J., Oyston, P. C., Green, M., and Titball, R. W. (2002) Clin. Microbiol. Rev. 15, 631-646
28. Larsson, P., Oyston, P. C., Chain, P., Chu, M. C., Duffield, M., Fuxelius, H. H., Garcia, E., Hälltorp, G., Johansson, D., Isherwood, K. E., Karp, P. D., Larsson, E., Liu, Y., Michell, S., Prior, J., Prior, R., Malfatti, S., Sjöstedt, A., Svensson, K., Thompson, N., Vergez, L., Wagg, J. K., Wren, B. W., Lindler, L. E., Andersson, S. G., Forsman, M., and Titball, R. W. (2005) Nat. Genet. 37, 153-159
29. Oyston, P. C., Sjostedt, A., and Titball, R. W. (2004) Nat. Rev. Microbiol. 2, 967-978
30. Dennis, D. T., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Friedlander, A. M., Hauer, J., Layton, M., Lillibridge, S. R., McDade, J. E., Osterholm, M. T., O'Toole, T., Parker, G., Perl, T. M., Russell, P. K., and Tonat, K. (2001) JAMA 285, 2763-2773
31. Petersen, J. M., and Schriefer, M. E. (2005) Vet. Res. 36, 455-467
32. Forslund, A. L., Kuoppa, K., Svensson, K., Salomonsson, E., Johansson, A., Byström, M., Oyston, P. C., Michell, S. L., Titball, R. W., Noppa, L., Frithz-Lindsten, E., Forsman, M., and Forsberg, A. (2006) Mol. Microbiol. 59, 1818-1830
33. Ark, N. M., and Mann, B. J. (2011) Microb. Pathog. 51, 110-120
34. Forslund, A. L., Salomonsson, E. N., Golovliov, I., Kuoppa, K., Michell, S., Titball, R., Oyston, P., Noppa, L., Sjöstedt, A., and Forsberg, A. (2010) BMC Microbiol. 10, 227
35. Salomonsson, E. N., Forslund, A. L., and Forsberg, A. (2011) Front. Microbiol. 2, 1-7
36. Zogaj, X., Chakraborty, S., Liu, J., Thanassi, D. G., and Klose, K. E. (2008) Microbiology 154, 2139-2150
37. Salomonsson, E., Forsberg, A., Roos, N., Holz, C., Maier, B., Koomey, M., and Winther-Larsen, H. C. (2009) Microbiology 155, 2546-2559
38. Hager, A. J., Bolton, D. L., Pelletier, M. R., Brittnacher, M. J., Gallagher, L. A., Kaul, R., Skerrett, S. J., Miller, S. I., and Guina, T. (2006) Mol. Microbiol. 62, 227-237
39. Bradley, D. E. (1974) Virology 58, 149-163
40. Mattick, J. S., Bills, M. M., Anderson, B. J., Dalrymple, B., Mott, M. R., and Egerton, J. R. (1987) J. Bacteriol. 169, 33-41
41. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) J. Appl. Crystallogr. 40, 658-674
42. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
43. Emsley, P., and Cowtan, K. (2004) Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
44. Terwilliger, T. (2004) J. Synchrotron Radiat. 11, 49-52
45. Terwilliger, T. C., and Berendzen, J. (1999) Acta Crystallogr. D Biol. Crystallogr. 55, 849-861
46. Navaza, J. (2001) Acta Crystallogr. D Biol. Crystallogr. 57, 1367-1372
47. Brunger, A. T. (2007) Nat. Protoc. 2, 2728-2733
48. Jia-xing, Y., Woolfson, M. M., Wilson, K. S., and Dodson, E. J. (2005) Acta Crystallogr. D Biol. Crystallogr. 61, 1465-1475
49. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) J. Comput. Chem. 25, 1605-1612
50. Audette, G. F., Irvin, R. T., and Hazes, B. (2004) Biochemistry 43, 11427-11435
51. Keizer, D. W., Kalisiak, M., Crump, M. P., Suh, J. Y., Irvin, R. T., and Sykes, B. D. (2001) J. Biomol. NMR 19, 385-386
52. Ghosh, A., Hartung, S., van der Does, C., Tainer, J. A., and Albers, S. V. (2011) Biochem. J. 437, 43-52
53. Yamagata, A., and Tainer, J. A. (2007) EMBO J. 26, 878-890
54. Lemkul, J. A., and Bevan, D. R. (2011) J. Phys. Chem. B 115, 8004-8008
55. Schwartzkoff, C. L., Egerton, J. R., Stewart, D. J., Lehrbach, P. R., Elleman, T. C., and Hoyne, P. A. (1993) Aust. Vet. J. 70, 123-126
56. Dhungyel, O. P., and Whittington, R. J. (2009) Vaccine 28, 470-473
57. Emery, D. L., Rothel, J. S., Kirkpatrick, A., and Maclaren, J. A. (1989) Vet. Immunol. Immunopathol. 21, 339-349
58. Emery, D. L., Stewart, D. J., and Clark, B. L. (1984) Aust. Vet. J. 61, 237-238
59. McKern, N. M., Stewart, D. J., and Strike, P. M. (1988) J. Protein Chem. 7, 157-164
60. Cagatay, T. I., and Hickford, J. G. (2008) Vet. Microbiol. 126, 160-167
61. Kirn, T. J., Lafferty, M. J., Sandoe, C. M., and Taylor, R. K. (2000) Mol. Microbiol. 35, 896-910
62. Hobbs, M., and Mattick, J. S. (1993) Mol. Microbiol. 10, 233-243
63. Sandkvist, M. (2001) Mol. Microbiol. 40, 271-283
64. Shevchik, V. E., Robert-Baudouy, J., and Condemine, G. (1997) EMBO J. 16, 3007-3016
65. Tainer, J. A., Getzoff, E. D., Alexander, H., Houghten, R. A., Olson, A. J., Lerner, R. A., and Hendrickson, W. A. (1984) Nature 312, 127-134
66. Tainer, J. A., Getzoff, E. D., Paterson, Y., Olson, A. J., and Lerner, R. A. (1985) Annu. Rev. Immunol. 3, 501-535
67. Hansen, J. K., and Forest, K. T. (2006) J. Mol. Microbiol. Biotechnol. 11, 192-207
68. Köhler, R., Schäfer, K., Müller, S., Vignon, G., Diederichs, K., Philippsen, A., Ringler, P., Pugsley, A. P., Engel, A., and Welte, W. (2004) Mol. Microbiol. 54, 647-664
69. Alphonse, S., Durand, E., Douzi, B., Waegele, B., Darbon, H., Filloux, A., Voulhoux, R., and Bernard, C. (2010) J. Struct. Biol. 169, 75-80
70. Korotkov, K. V., Gray, M. D., Kreger, A., Turley, S., Sandkvist, M., and Hol, W. G. (2009) J. Biol. Chem. 284, 25466-25470
71. Franz, L. P., Douzi, B., Durand, E., Dyer, D. H., Voulhoux, R., and Forest, K. T. (2011) Acta Crystallogr. D Biol. Crystallogr. 67, 124-130
72. Hagblom, P., Segal, E., Billyard, E., and So, M. (1985) Nature 315, 156-158
73. Lim, M. S., Ng, D., Zong, Z., Arvai, A. S., Taylor, R. K., Tainer, J. A., and Craig, L. (2010) Mol. Microbiol. 77, 755-770