Preclusion of irreversible destruction of Dr adhesin structures by a high activation barrier for the unfolding stage of the fimbrial DraE subunit

Biochemistry

Volumn 48, Issue 49, 2009, Pages 11807-11816

  Pia̧tek, Rafał ^a   Bruździak, Piotr ^a   Zalewska Pia̧tek, Beata ^a   Kur, Józef ^a   Stangret, Janusz ^a  

^a GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ADHESIVE STRUCTURE; COMPLEMENTATION; ENERGY OF ACTIVATION; HIGH RESISTANCE; HIGH STABILITY; HIGH-ACTIVATION; KINETIC STABILITY; MICRO-CALORIMETRY; OUTER MEMBRANE; PERIPLASMIC CHAPERONE; PROTEIN CORE; PROTEIN DENATURATION; THERMAL DENATURATIONS; TWO-STATE MODEL; UNFOLDING PROCESS; UROPATHOGENIC;

ACTIVATION ENERGY; DENATURATION; PYROLYSIS; RATE CONSTANTS;

PROTEINS;

ADHESIN;

ARTICLE; FIMBRIA; KINETICS; MICROCALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN STRUCTURE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ENERGY METABOLISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FIMBRIAE, BACTERIAL; KINETICS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMODYNAMICS;

EID: 71649107217     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900920k     Document Type: Article

References (51)

1. Jonson, A. B., Normark, S., and Rhen, M. (2005) Fimbriae, pili, flagella and bacterial virulence. Contrib. Microbiol. 12, 67-89.
2. Le Bouguénec, C. (2005) Adhesins and invasins of pathogenic Escherichia coli. Int. J. Med. Microbiol. 295, 471-478.
3. Hung, D. L., and Hultgren, S. J. (1998) Pilus biogenesis via the chaperone/usher pathway: an integration of structure and function. J. Struct. Biol. 124, 201-220.
4. Sauer, F. G., Futterer, K., Pinkner, J. S., Dodson, K. W., Hultgren, S. J., and Waksman, G. (1999) Structural basis of chaperone function and pilus biogenesis. Science 285, 1058-1061. (Pubitemid 129515449)
5. Sauer, F. G., Barnhart, M., Choudhury, D., Knight, S. D., Waksman, G., and Hultgren, S. J. (2000) Chaperone-assisted pilus assembly and bacterial attachment. Curr. Opin. Struct. Biol. 10, 548-556.
6. Vetsch, M., Erilov, D., Moliere, N., Nishiyama, M., Ignatov, O., and Glockshuber, R. (2006) Mechanism of fibre assembly through the chaperone-usher pathway. EMBO Rep. 7, 734-738. (Pubitemid 43986272)
7. Remaut, H., Tang, C., Henderson, N. S., Pinkner, J. S., Wang, T., Hultgren, S. J., Thanassi, D. G., Waksman, G., and Li, H. (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133, 640-652. (Pubitemid 351636304)
8. Swanson, T. N., Bilge, S. S., Nowicki, B., and Moseley, S. L. (1991) Molecular structure of the Dr adhesin: nucleotide sequence and mapping of receptor-binding domain by use of fusion constructs. Infect. Immun. 59, 261-268.
9. Nowicki, B., Barrish, J. P., Korhonen, T., Hull, R. A., and Hull, S. I. (1987) Molecular cloning of the Escherichia coli O75X adhesin. Infect. Immun. 55, 3168-3173.
10. Piatek, R., Zalewska, B., Kolaj, O., M., F., Nowicki, B., and Kur, J. (2005) Molecular aspects of biogenesis of Escherichia coli Dr Fimbriae: characterization of DraB-DraE complexes. Infect. Immun. 73, 135-145.
11. Cota, E., Jones, C., Simpson, P., Altroff, H., Anderson, K. L., du Merle, L., Guignot, J., Servin, A., Le Bouguénec, C., Mardon, H., and S., M. (2006) The solution structure of the invasive tip complex from Afa/Dr fibrils. Mol. Microbiol. 62, 356-366.
12. Anderson, K. L., Billington, J., Pettigrew, D., Cota, E., Simpson, P., Roversi, P., Chen, H. A., Urvil, P., du Merle, L., Barlow, P. N., Medof, M. E., Smith, R. A., Nowicki, B., Le Bouguénec, C., Lea, S. M., and Matthews, S. (2004) An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol. Cell 15, 647-657.
13. Zavialov, A., Zav'yalova, G., Korpela, T., and Zav'yalov, V. (2007) FGL chaperone-assembled fimbrial polyadhesins: anti-immune armament of Gram-negative bacterial pathogens. FEMS Microbiol Rev. 31, 478-514.
14. Nowicki, B., Moulds, J., Hull, R., and Hull, S. (1988) A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect. Immun. 56, 1057-1060.
15. Pham, T., Kaul, A., Hart, A., Goluszko, P., Moulds, J., Nowicki, S., Lublin, D. M., and Nowicki, B. J. (1995) dra-related X adhesins of gestational pyelonephritis-associated Escherichia coli recognize SCR-3 and SCR-4 domains of recombinant decay-accelerating factor. Infect. Immun. 63, 1663-1668.
16. Selvarangan, R., Goluszko, P., Singhal, J., Carnoy, C., Moseley, S., Hudson, B., Nowicki, S., and Nowicki, B. (2004) Interaction of Dr adhesin with collagen type IV is a critical step in Escherichia coli renal persistence. Infect. Immun. 72, 4827-4835.
17. Servin, A. L. (2005) Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Int. J. Med. Microbiol. 295, 471-478.
18. Korotkova, N., Yarova-Yarovaya, Y., Tchesnokova, V., Yazvenko, N., Carl, M. A., Stapleton, A. E., and Moseley, S. L. (2008) Escherichia coli DraE adhesin-associated bacterial internalization by epithelial cells is promoted independently by decay-accelerating factor and carcinoembryonic antigen-related cell adhesion molecule binding and does not require the DraD invasin. Infect. Immun. 76, 3869-3880.
19. Choudhury, D., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J., Hultgren, S. J., and Knight, S. D. (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285, 1061-1066. (Pubitemid 129515450)
20. Sauer, F. G., Pinkner, J. S., Waksman, G., and Hultgren, S. J. (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111, 543-551. (Pubitemid 35356559)
21. Zavialov, A. V., Berglund, J., Pudney, A. F., Fooks, L. J., Ibrahim, T. M., MacIntyre, S., and Knight, S. D. (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113, 587-596. (Pubitemid 36694184)
22. Korotkova, N., Le Trong, I., Samudrala, R., Korotkov, K., Van Loy, C. P., Bui, A. L., Moseley, S. L., and Stenkamp, R. E. (2006) Crystal structure and mutational analysis of the DaaE adhesin of Escherichia coli. J. Biol. Chem. 281, 22367-22377.
23. Verger, D., Bullitt, E., Hultgren, S. J., and Waksman, G. (2007) Crystal structure of the P pilus rod subunit PapA. PLoS Pathog. 3, 73. (Pubitemid 46827953)
24. Gossert, A. D., Bettendorff, P., Puorger, C., Vetsch, M., Herrmann, T., Glockshuber, R., and Wüthrich, K. (2008) NMR structure of the Escherichia coli type 1 pilus subunit FimF and its interactions with other pilus subunits. J. Mol. Biol. 375, 752-763.
25. Hung, D. L., Knight, S. D., Woods, R. M., Pinkner, J. S., and Hultgren, S. J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 15, 3792-3805.
26. Barnhart, M. M., Pinkner, J. S., Soto, G. E., Sauer, F. G., Langermann, S., Waksman, G., Frieden, C., and Hultgren, S. J. (2000) PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl. Acad. Sci. U.S.A. 97, 7709-7714.
27. Zavialov, A. V., Kersley, J., Korpela, T., Zav'yalov, V. P., MacIntyre, S., and Knight, S. D. (2002) Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol. Microbiol. 45, 983-995.
28. Pettigrew, D., Anderson, K. L., Billington, J., Cota, E., Simpson, P., Urvil, P., Rabuzin, F., Roversi, P., Nowicki, B., du Merle, L., Le Bouguénec, C., Matthews, S., and Lea, S. M. (2004) High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J. Biol. Chem. 279, 46851-46867.
29. Jedrzejczak, R., Dauter, Z., Dauter, M., Piatek, R., Zalewska, B., Mróz, M., Bury, K., Nowicki, B., and Kur, J. (2006) Structure of DraD invasin from uropathogenic Escherichia coli: a dimer with swapped beta-tails. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 157-164.
30. Zavialov, A. V., Tischenko, V. M., Fooks, L. J., Brandsdal, B. O., Aqvist, J., Zav'yalov, V. P., Macintyre, S., and Knight, S. D. (2005) Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem. J. 389, 685-694.
31. Vetsch, M., Sebbel, P., and Glockshuber, R. (2002) Chaperone-independent folding of type 1 pilus domains. J. Mol. Biol. 322, 827-840.
32. Erilov, D., Puorger, C., and Glockshuber, R. (2007) Quantitative analysis of nonequilibrium, denaturant-dependent protein folding transitions. J. Am. Chem. Soc. 129, 8938-8939.
33. Puorger, C., Eidam, O., Capitani, G., Erilov, D., Grütter, M. G., and Glockshuber, R. (2008) Infinite kinetic stability against dissociation of supramolecular protein complexes through donor strand complementation. Structure 16, 631-642.
34. Eshdat, Y., Silverblatt, F. J., and Sharon, N. (1981) Dissociation and reassembly of Escherichia coli type 1 pili. J. Bacteriol. 148, 308-314. (Pubitemid 12209428)
35. Orndorff, P. E., and Falkow, S. (1984) Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J. Bacteriol. 159, 736-744. (Pubitemid 14055371)
36. Zav'yalov, V. P., Chernovskaya, T. V., Chapman, D. A., Karlyshev, A. V., MacIntyre, S., Zavialov, A. V., Vasiliev, A. M., Denesyuk, A. I., Zav'yalova, G. A., Dudich, I. V., Korpela, T., and Abramov, V. M. (1997) Influence of the conserved disulphide bond, exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like molecular chaperone Caf1M of Yersinia pestis. Biochem. J. 324, 571-578.
37. Zalewska, B., Piatek, R., Konopa, G., Nowicki, B., Nowicki, S., and Kur, J. (2003) Chimeric Dr fimbriae with a herpes simplex virus type 1 epitope as a model for a recombinant vaccine. Infect. Immun. 71, 5505-5513.
38. Mark, H., and Workman, J., Jr. (2007) Chemometrics in spectroscopy, Academic Press, New York.
39. Savitzky, A., and Golay, M. J. E. (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36, 1627-1639.
40. Kurganov, B. I., Lyubarev, A. E., Sanchez-Ruiz, J. M., and Shnyrov, V. L. (1997) Analysis of differential scanning calorimetry data for proteins. Criteria of validity of one-step mechanism of irreversible protein denaturation. Biophys. Chem. 69, 125-135.
41. Sanchez-Ruiz, J. M. (1992) Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys. J. 61, 921-935.
42. Arrondo, J. L. R., Muga, A., Castresana, J., and Goni, F. M. (1993) Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy. Prog. Biochem. Mol. Biol. 59, 23-56.
43. Arrondo, J. L. R., and Goni, F. M. (1999) Structure and dynamics of membrane proteins as studied by infrared spectroscopy. Prog. Biochem. Mol. Biol. 72, 367-405.
44. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430.
45. Herberhold, H., Royer, C. A., and Winter, R. (2004) Effects of chaotropic and kosmotropic cosolvents on the pressure-iduced unfolding and denaturation of proteins: an FT-IR study on staphylococcal nuclease. Biochemistry 43, 3336-3345. (Pubitemid 38391690)
46. Weert, M. v. d., Haris, P. I., Hannink, W. E., and Crommelin, D. J. A. (2001) Fourier transform infrared spectrometric analysis of protein conformation: effect of sampling method and stress factors. Anal. Biochem. 297, 160-169.
47. Malinowski, E. R., Cox, R. A., and Haldna, U. L. (1984) Factor analysis for isolation of the Raman spectra of aqueous sulfuric acid components. Anal. Chem. 56, 778-781.
48. Sturgis, J., Robert, B., and Goormaghtigh, E. (1998) Transmembrane helix stability: the effect of helix-helix interactions studied by Fourier transform infrared spectroscopy. Biophys. J. 74, 988-994. (Pubitemid 28345292)
49. Meersman, F., Smeller, L., and Heremans, K. (2002) Comparative Fourier transform Infrared spectroscopy study of cold-, pressure-, and heat-induced unfolding and aggregation of myoglobin. Biophys. J. 82, 2635-2644. (Pubitemid 34441301)
50. Meersman, F., and Heremans, K. (2003) Temperature-induced dissociation of protein aggregates: accessing the denatured state. Biochemistry 42, 14234-14241. (Pubitemid 37499420)
51. Plaza del Pino, I. M., Ibarra-Molero, B., and Sanchez-Ruiz, J. M. (2000) Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases. Proteins 40, 58-70. (Pubitemid 30368582)