Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4882-4894

  Alamuri, Praveen ^a,d   Löwer, Martin ^b   Hiss, Jan A ^c   Himpsl, Stephanie D ^a   Schneider, Gisbert ^c   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b GOETHE UNIVERSITY   (Germany)

^c ETH ZURICH   (Switzerland)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AGGLUTININ; AIPA PROTEIN; BACTERIAL PROTEIN; INVASIN; SCLEROPROTEIN; TAAP PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; BETA SHEET; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL AGGLUTINATION; CELL FUNCTION; CELL INVASION; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ESCHERICHIA COLI; FEMALE; GENOME; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEUS MIRABILIS; THREE DIMENSIONAL IMAGING; YERSINIA ENTEROCOLITICA;

ADHESINS, BACTERIAL; AGGLUTINATION; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; DIMERIZATION; FEMALE; FIMBRIAE, BACTERIAL; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED CBA; MOLECULAR SEQUENCE DATA; PROTEUS INFECTIONS; PROTEUS MIRABILIS; URINARY TRACT INFECTIONS;

EID: 78049447494     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00718-10     Document Type: Article

References (60)

1. Alamuri, P., K. A. Eaton, S. D. Himpsl, S. N. Smith, and H. L. Mobley. 2009. Vaccination with proteus toxic agglutinin, a hemolysin-independent cytotoxin in vivo, protects against Proteus mirabilis urinary tract infection. Infect. Immun. 77:632-641.
2. Alamuri, P., and H. L. Mobley. 2008. A novel autotransporter of uropathogenic Proteus mirabilis is both a cytotoxin and an agglutinin. Mol. Microbiol. 68:997-1017.
3. Allison, C., N. Coleman, P. L. Jones, and C. Hughes. 1992. Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect. Immun. 60:4740-4746.
4. Altman, E., B. A. Harrison, R. K. Latta, K. K. Lee, J. F. Kelly, and P. Thibault. 2001. Galectin-3-mediated adherence of Proteus mirabilis to Madin-Darby canine kidney cells. Biochem. Cell Biol. 79:783-788.
5. Barenkamp, S. J., and J. W. St. Geme III. 1996. Identification of a second family of high-molecular-weight adhesion proteins expressed by non-typable Haemophilus influenzae. Mol. Microbiol. 19:1215-1223.
6. Belas, R., J. Manos, and R. Suvanasuthi. 2004. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect. Immun. 72:5159-5167.
7. Coker, C., C. A. Poore, X. Li, and H. L. Mobley. 2000. Pathogenesis of Proteus mirabilis urinary tract infection. Microbes Infect. 2:1497-1505.
8. Cole, C., J. D. Barber, and G. J. Barton. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36:W197-W201.
9. Cotter, S. E., N. K. Surana, S. Grass, and J. W. St. Geme III. 2006. Trimeric autotransporters require trimerization of the passenger domain for stability and adhesive activity. J. Bacteriol. 188:5400-5407.
10. Cotter, S. E., N. K. Surana, and J. W. St. Geme III. 2005. Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol. 13:199-205.
11. Desvaux, M., N. J. Parham, and I. R. Henderson. 2004. The autotransporter secretion system. Res. Microbiol. 155:53-60.
12. Eberhard, T., R. Virkola, T. Korhonen, G. Kronvall, and M. Ullberg. 1998. Binding to human extracellular matrix by Neisseria meningitidis. Infect. Immun. 66:1791-1794.
13. Fink, D. L., L. D. Cope, E. J. Hansen, and J. W. St. Geme III. 2001. The Hemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J. Biol. Chem. 276:39492-39500.
14. Girard, V., and M. Mourez. 2006. Adhesion mediated by autotransporters of Gram-negative bacteria: structural and functional features. Res. Microbiol. 157:407-416.
15. Grant, J. A., B. T. Pickup, and A. Nicholls. 2001. A smooth permittivity function for Poisson-Boltzmann solvation methods. J. Comput. Chem. 22:608-640.
16. Grosskinsky, U., M. Schutz, M. Fritz, Y. Schmid, M. C. Lamparter, P. Szczesny, A. N. Lupas, I. B. Autenrieth, and D. Linke. 2007. A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport. J. Bacteriol. 189:9011-9019.
17. Henderson, I. R., R. Cappello, and J. P. Nataro. 2000. Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8:529-532.
18. Henderson, I. R., and J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-1243.
19. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
20. Hooft, R. W., G. Vriend, C. Sander, and E. E. Abola. 1996. Errors in protein structures. Nature 381:272.
21. Hoopman, T. C., W. Wang, C. A. Brautigam, J. L. Sedillo, T. J. Reilly, and E. J. Hansen. 2008. Moraxella catarrhalis synthesizes an autotransporter that is an acid phosphatase. J. Bacteriol. 190:1459-1472.
22. Jacobsen, S. M., D. J. Stickler, H. L. Mobley, and M. E. Shirtliff. 2008. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21:26-59.
23. Johnson, D. E., R. G. Russell, C. V. Lockatell, J. C. Zulty, J. W. Warren, and H. L. Mobley. 1993. Contribution of Proteus mirabilis urease to persistence, urolithiasis, and acute pyelonephritis in a mouse model of ascending urinary tract infection. Infect. Immun. 61:2748-2754.
24. Jose, J. 2006. Autodisplay: efficient bacterial surface display of recombinant proteins. Appl. Microbiol. Biotechnol. 69:607-614.
25. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
26. Li, X., C. V. Lockatell, D. E. Johnson, M. C. Lane, J. W. Warren, and H. L. Mobley. 2004. Development of an intranasal vaccine to prevent urinary tract infection by Proteus mirabilis. Infect. Immun. 72:66-75.
27. Li, X., and H. L. Mobley. 2002. Vaccines for Proteus mirabilis in urinary tract infection. Int. J. Antimicrob. Agents 19:461-465.
28. Liu, D. F., K. W. Mason, M. Mastri, M. Pazirandeh, D. Cutter, D. L. Fink, J. W. St. Geme III, D. Zhu, and B. A. Green. 2004. The C-terminal fragment of the internal 110-kilodalton passenger domain of the Hap protein of nontypeable Haemophilus influenzae is a potential vaccine candidate. Infect. Immun. 72:6961-6968.
29. Martinez, J. J., M. A. Mulvey, J. D. Schilling, J. S. Pinkner, and S. J. Hultgren. 2000. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 19:2803-2812.
30. McMichael, J. C., M. J. Fiske, R. A. Fredenburg, D. N. Chakravarti, K. R. VanDerMeid, V. Barniak, J. Caplan, E. Bortell, S. Baker, R. Arumugham, and D. Chen. 1998. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66:4374-4381.
31. Meng, G., N. K. Surana, J. W. St. Geme III, and G. Waksman. 2006. Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J. 25:2297-2304.
32. Moayeri, N., C. M. Collins, and P. O'Hanley. 1991. Efficacy of a Proteus mirabilis outer membrane protein vaccine in preventing experimental Proteus pyelonephritis in a BALB/c mouse model. Infect. Immun. 59:3778-3786.
33. Mobley, H. L., M. D. Island, and G. Massad. 1994. Virulence determinants of uropathogenic Escherichia coli and Proteus mirabilis. Kidney Int. Suppl. 47:S129-S136.
34. Nielubowicz, G. R., S. N. Smith, and H. L. Mobley. 2008. Outer membrane antigens of the uropathogen Proteus mirabilis recognized by the humoral response during experimental murine urinary tract infection. Infect. Immun. 76:4222-4321.
35. Nielubowicz, G. R., S. N. Smith, and H. L. Mobley. 2010. Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect. Immun. 78:2823-2833.
36. Pearson, M. M., M. Sebaihia, C. Churcher, M. A. Quail, A. S. Seshasayee, N. M. Luscombe, Z. Abdellah, C. Arrosmith, B. Atkin, T. Chillingworth, H. Hauser, K. Jagels, S. Moule, K. Mungall, H. Norbertczak, E. Rabbinowitsch, D. Walker, S. Whithead, N. R. Thomson, P. N. Rather, J. Parkhill, and H. L. Mobley. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol. 190:4027-4037.
37. Phan, V., R. Belas, B. F. Gilmore, and H. Ceri. 2008. ZapA, a virulence factor in a rat model of Proteus mirabilis-induced acute and chronic prostatitis. Infect. Immun. 76:4859-4864.
38. Rocha, S. P., W. P. Elias, A. M. Cianciarullo, M. A. Menezes, J. M. Nara, R. M. Piazza, M. R. Silva, C. G. Moreira, and J. S. Pelayo. 2007. Aggregative adherence of uropathogenic Proteus mirabilis to cultured epithelial cells. FEMS Immunol. Med. Microbiol. 51:319-326.
39. Rocha, S. P., J. S. Pelayo, and W. P. Elias. 2007. Fimbriae of uropathogenic Proteus mirabilis. FEMS Immunol. Med. Microbiol. 51:1-7.
40. Roggenkamp, A., N. Ackermann, C. A. Jacobi, K. Truelzsch, H. Hoffmann, and J. Heesemann. 2003. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J. Bacteriol. 185:3735-3744. (Pubitemid 36735923)
41. Rózalski, A., Z. Sidorczyk, and K. Kotelko. 1997. Potential virulence factors of Proteus bacilli. Microbiol. Mol. Biol. Rev. 61:65-89.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Sareneva, T., H. Holthofer, and T. K. Korhonen. 1990. Tissue-binding affinity of Proteus mirabilis fimbriae in the human urinary tract. Infect. Immun. 58:3330-3336.
44. Scarselli, M., D. Serruto, P. Montanari, B. Capecchi, J. Adu-Bobie, D. Veggi, R. Rappuoli, M. Pizza, and B. Arico. 2006. Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol. Microbiol. 61:631-644.
45. Scavone, P., A. Miyoshi, A. Rial, A. Chabalgoity, P. Langella, V. Azevedo, and P. Zunino. 2007. Intranasal immunisation with recombinant Lactococcus lactis displaying either anchored or secreted forms of Proteus mirabilis MrpA fimbrial protein confers specific immune response and induces a significant reduction of kidney bacterial colonisation in mice. Microbes Infect. 9:821-828.
46. Scavone, P., V. Sosa, R. Pellegrino, U. Galvalisi, and P. Zunino. 2004. Mucosal vaccination of mice with recombinant Proteus mirabilis structural fimbrial proteins. Microbes Infect. 6:853-860.
47. Schütz, M., E. M. Weiss, M. Schindler, T. Hallstrom, P. F. Zipfel, D. Linke, and I. B. Autenrieth. 2010. Trimer stability of YadA is critical for virulence of Yersinia enterocolitica. Infect. Immun. 78:2677-2690.
48. Stathopoulos, C., D. R. Hendrixson, D. G. Thanassi, S. J. Hultgren, J. W. St. Geme III, and R. Curtiss III. 2000. Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: an evolving story. Microbes Infect. 2:1061-1072. (Pubitemid 30664220)
49. Stenger, R. M., M. C. Poelen, E. E. Moret, B. Kuipers, S. C. Bruijns, P. Hoogerhout, M. Hijnen, A. J. King, F. R. Mooi, C. J. Boog, and C. A. van Els. 2009. Immunodominance in mouse and human CD4+ T-cell responses specific for the Bordetella pertussis virulence factor P.69 pertactin. Infect. Immun. 77:896-903.
50. Stickler, D., L. Ganderton, J. King, J. Nettleton, and C. Winters. 1993. Proteus mirabilis biofilms and the encrustation of urethral catheters. Urol. Res. 21:407-411.
51. Surana, N. K., D. Cutter, S. J. Barenkamp, and J. W. St. Geme III. 2004. The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J. Biol. Chem. 279:14679-14685.
52. Tahir, Y. E., P. Kuusela, and M. Skurnik. 2000. Functional mapping of the Yersinia enterocolitica adhesin YadA. Identification of eight NSVAIG-S motifs in the amino-terminal half of the protein involved in collagen binding. Mol. Microbiol. 37:192-206.
53. Tamm, A., A. M. Tarkkanen, T. K. Korhonen, P. Kuusela, P. Toivanen, and M. Skurnik. 1993. Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica. Mol. Microbiol. 10:995-1011.
54. Tiyawisutsri, R., M. T. Holden, S. Tumapa, S. Rengpipat, S. R. Clarke, S. J. Foster, W. C. Nierman, N. P. Day, and S. J. Peacock. 2007. Burkholderia Hep-Hag autotransporter (BuHA) proteins elicit a strong antibody response during experimental glanders but not human melioidosis. BMC Microbiol. 7:19.
55. Valle, J., A. N. Mabbett, G. C. Ulett, A. Toledo-Arana, K. Wecker, M. Totsika, M. A. Schembri, J. M. Ghigo, and C. Beloin. 2008. UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J. Bacteriol. 190:4147-4161. (Pubitemid 351812861)
56. Walker, K. E., S. Moghaddame-Jafari, C. V. Lockatell, D. Johnson, and R. Belas. 1999. ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol. Microbiol. 32:825-836.
57. Wells, T., J. J. Tree, G. L. Ulett, and M. A. Schembi. 2007. Autotransporter proteins: novel targets at the bacterial cell surface. FEMS Microbiol. Lett. 274:163-172.
58. Yen, Y. T., A. Karkal, M. Bhattacharya, R. C. Fernandez, and C. Stathopoulos. 2007. Identification and characterization of autotransporter proteins of Yersinia pestis KIM. Mol. Membr. Biol. 24:28-40.
59. Zhao, H., X. Li, D. E. Johnson, I. Blomfield, and H. L. Mobley. 1997. In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Mol. Microbiol. 23:1009-1019.
60. Zunino, P., C. Piccini, and C. Legnani-Fajardo. 1999. Growth, cellular differentiation and virulence factor expression by Proteus mirabilis in vitro and in vivo. J. Med. Microbiol. 48:527-534.