Merging mythology and morphology: The multifaceted lifestyle of Proteus mirabilis

Nature Reviews Microbiology

Volumn 10, Issue 11, 2012, Pages 743-754

  Armbruster, Chelsie E ^a   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; HAEMIN RECEPTOR; HEMOLYSIN; INVASIN; METALLOPROTEINASE; PROTEOBACTIN; SERRALYSIN; UNCLASSIFIED DRUG; UREASE; ZINC; ZINC UPTAKE PROTEIN C;

ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BLADDER; FIMBRIA; FLAGELLUM; GENE SEQUENCE; HORIZONTAL GENE TRANSFER; HUMAN; KIDNEY; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEUS INFECTION; PROTEUS MIRABILIS; REVIEW; SIGNAL TRANSDUCTION; SPLEEN; URINARY TRACT INFECTION;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CATHETER-RELATED INFECTIONS; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; HUMANS; IMMUNE EVASION; PROTEUS INFECTIONS; PROTEUS MIRABILIS; URINARY TRACT INFECTIONS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); PROTEUS MIRABILIS;

EID: 84867893471     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2890     Document Type: Review

References (139)

1. Hauser, G. Über Fäulnissbacterien und deren Beziehungen zur Septicämie; ein Beitrag zur Morphologie der Spaltpilze (Vogel, 1885).
2. Hoeniger, J. F. M. Development of flagella by Proteus mirabilis. J. Gen. Microbiol. 40, 29-42 (1965).
3. Wenner, J. J. & Rettger, L. F. A. Systematic Study of the Proteus group of bacteria. J. Bacteriol. 4, 331-353 (1919).
4. Jacobsen, S. M., Stickler, D. J., Mobley, H. L. T. & Shirtliff, M. E. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21, 26-59 (2008). (Pubitemid 351160009)
5. Nicolle, L. E. Catheter-related urinary tract infection. Drugs Aging 22, 627-639 (2005). (Pubitemid 41138976)
6. O'Hara, C. M., Brenner, F. W. & Miller, J. M. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin. Microbiol. Rev. 13, 534-546 (2000).
7. Hooton, T. M. et al. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin. Infect. Dis. 50, 625-663 (2010).
8. Morris, N. S., Stickler, D. J. & McLean, R. J. The development of bacterial biofilms on indwelling urethral catheters. World J. Urol. 17, 345-350 (1999).
9. Mathur, S., Sabbuba, N. A., Suller, M. T., Stickler, D. J. & Feneley, R. C. Genotyping of urinary and fecal Proteus mirabilis isolates from individuals with long-term urinary catheters. Eur. J. Clin. Microbiol. Infect. Dis. 24, 643-644 (2005). (Pubitemid 41456150)
10. Wazait, H. D. et al. Catheter-associated urinary tract infections: prevalence of uropathogens and pattern of antimicrobial resistance in a UK hospital (1996-2001). BJU Int. 91, 806-809 (2003). (Pubitemid 36724064)
11. Stickler, D. J. & Feneley, R. C. The encrustation and blockage of long-term indwelling bladder catheters: a way forward in prevention and control. Spinal Cord 48, 784-790 (2010).
12. Macleod, S. M. & Stickler, D. J. Species interactions in mixed-community crystalline biofilms on urinary catheters. J. Med. Microbiol. 56, 1549-1557 (2007). (Pubitemid 350175083)
13. Breitenbucher, R. B. Bacterial changes in the urine samples of patients with long-term indwelling catheters. Arch. Intern. Med. 144, 1585-1588 (1984). (Pubitemid 14054479)
14. Rahav, G., Pinco, E., Silbaq, F. & Bercovier, H. Molecular epidemiology of catheter-associated bacteriuria in nursing home patients. J. Clin. Microbiol. 32, 1031-1034 (1994). (Pubitemid 24100082)
15. Siegman-Igra, Y., Kulka, T., Schwartz, D. & Konforti, N. Polymicrobial and monomicrobial bacteraemic urinary tract infection. J. Hospital Infect. 28, 49-56 (1994). (Pubitemid 24297792)
16. Dedeic-Ljubovic, A. & Hukic, M. Catheter-related urinary tract infection in patients suffering from spinal cord injuries. Bosn. J. Basic Med. Sci. 9, 2-9 (2009).
17. Ronald, A. The etiology of urinary tract infection: traditional and emerging pathogens. Dis. Mon. 49, 71-82 (2003). (Pubitemid 36350776)
18. Kunin, C. M. Blockage of urinary catheters: role of microorganisms and constituents of the urine on formation of encrustations. J. Clin. Epidemiol. 42, 835-842 (1989). (Pubitemid 19231949)
19. Coker, C., Poore, C. A., Li, X. & Mobley, H. L. T. Pathogenesis of Proteus mirabilis urinary tract infection. Microbes Infect. 2, 1497-1505 (2000).
20. Pearson, M. M. et al. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol. 190, 4027-4037 (2008). (Pubitemid 351732882)
21. Himpsl, S. D., Lockatell, C. V., Hebel, J. R., Johnson, D. E. & Mobley, H. L. T. Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J. Med. Microbiol. 57, 1068-1078 (2008).
22. Zhao, H., Li, X., Johnson, D. E. & Mobley, H. L. T. Identification of protease and rpoN-associated genes of uropathogenic Proteus mirabilis by negative selection in a mouse model of ascending urinary tract infection. Microbiology 145, 185-195 (1999). (Pubitemid 29043591)
23. Burall, L. S. et al. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect. Immun. 72, 2922-2938 (2004). (Pubitemid 38542423)
24. Williams, G. J. & Stickler, D. J. Some observations on the migration of Proteus mirabilis and other urinary tract pathogens over foley catheters. Infect. Control Hosp. Epidemiol. 29, 443-445 (2008). (Pubitemid 351589981)
25. Stickler, D., Ganderton, L., King, J., Nettleton, J. & Winters, C. Proteus mirabilis biofilms and the encrustation of urethral catheters. Urol. Res. 21, 407-411 (1993). (Pubitemid 24053899)
26. Morris, N. S., Stickler, D. J. & Winters, C. Which indwelling urethral catheters resist encrustation by Proteus mirabilis biofilms? Br. J. Urol. 80, 58-63 (1997). (Pubitemid 28316710)
27. Stickler, D. J. et al. Observations on the adherence of Proteus mirabilis onto polymer surfaces. J. Appl. Microbiol. 100, 1028-1033 (2006).
28. Morris, N. S. & Stickler, D. J. Encrustation of indwelling urethral catheters by Proteus mirabilis biofilms growing in human urine. J. Hosp. Infect. 39, 227-234 (1998). (Pubitemid 28362389)
29. Rocha, S. P. D., Pelayo, J. S. & Elias, W. P. Fimbriae of uropathogenic Proteus mirabilis. FEMS Immunol. Med. Microbiol. 51, 1-7 (2007). (Pubitemid 47387485)
30. Mobley, H. L. et al. MR/K hemagglutination of Providencia stuartii correlates with adherence to catheters and with persistence in catheter-associated bacteriuria. J. Infect. Dis. 157, 264-271 (1988). (Pubitemid 18061238)
31. Yakubu, D. E., Old, D. C. & Senior, B. W. The haemagglutinins and fimbriae of Proteus penneri. J. Med. Microbiol. 30, 279-284 (1989). (Pubitemid 20023712)
32. Massad, G., Bahrani, F. K. & Mobley, H. L. Proteus mirabilis fimbriae: identification, isolation, and characterization of a new ambient-temperature fimbria. Infect. Immun. 62, 1989-1994 (1994). (Pubitemid 24137006)
33. Zunino, P., Geymonat, L., Allen, A. G., Legnani-Fajardo, C. & Maskell, D. J. Virulence of a Proteus mirabilis ATF isogenic mutant is not impaired in a mouse model of ascending urinary tract infection. FEMS Immunol. Med. Microbiol. 29, 137-143 (2000).
34. Sabbuba, N., Hughes, G. & Stickler, D. J. The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int. 89, 55-60 (2002). (Pubitemid 34117765)
35. Stickler, D. & Hughes, G. Ability of Proteus mirabilis to swarm over urethral catheters. Eur. J. Clin. Microbiol. Infect. Dis. 18, 206-208 (1999). (Pubitemid 29527957)
36. Jones, B. V., Young, R., Mahenthiralingam, E. & Stickler, D. J. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect. Immun. 72, 3941-3950 (2004). (Pubitemid 38821908)
37. Jones, S. M., Yerly, J., Hu, Y., Ceri, H. & Martinuzzi, R. Structure of Proteus mirabilis biofilms grown in artificial urine and standard laboratory media. FEMS Microbiol. Lett. 268, 16-21 (2007). (Pubitemid 46192830)
38. Belas, R. & Suvanasuthi, R. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J. Bacteriol. 187, 6789-6803 (2005). (Pubitemid 41356253)
39. Rather, P. N. Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol. 7, 1065-1073 (2005). (Pubitemid 41026508)
40. Morgenstein, R. M., Szostek, B. & Rather, P. N. Regulation of gene expression during swarmer cell differentiation in Proteus mirabilis. FEMS Microbiol. Rev. 34, 753-763 (2010).
41. Calvo, J. M. & Matthews, R. G. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58, 466-490 (1994).
42. Hart, B. R. & Blumenthal, R. M. Unexpected coregulator range for the global regulator Lrp of Escherichia coli and Proteus mirabilis. J. Bacteriol. 193, 1054-1064 (2011).
43. Allison, C., Lai, H. C., Gygi, D. & Hughes, C. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol. 8, 53-60 (1993). (Pubitemid 23114821)
44. Tan, I. K. & Gajra, B. Plasma and urine amino acid profiles in a healthy adult population of Singapore. Ann. Acad. Med. Singap. 35, 468-475 (2006). (Pubitemid 44450151)
45. Thomas, V. J. & Collins, C. M. Identification of UreR binding sites in the Enterobacteriaceae plasmid-encoded and Proteus mirabilis urease gene operons. Mol. Microbiol. 31, 1417-1428 (1999). (Pubitemid 29110100)
46. Coker, C., Bakare, O. O. & Mobley, H. L. H-NS is a repressor of the Proteus mirabilis urease transcriptional activator gene ureR. J. Bacteriol. 182, 2649-2653 (2000). (Pubitemid 30212930)
47. Poore, C. A. & Mobley, H. L. T. Differential regulation of the Proteus mirabilis urease gene cluster by UreR and H-NS. Microbiology 149, 3383-3394 (2003). (Pubitemid 38016667)
48. Jones, B. D. & Mobley, H. L. Proteus mirabilis urease: nucleotide sequence determination and comparison with jack bean urease. J. Bacteriol. 171, 6414-6422 (1989). (Pubitemid 20006917)
49. D'Orazio, S. E., Thomas, V. & Collins, C. M. Activation of transcription at divergent urea-dependent promoters by the urease gene regulator UreR. Mol. Microbiol. 21, 643-655 (1996). (Pubitemid 26323786)
50. D'Orazio, S. E. & Collins, C. M. The plasmid-encoded urease gene cluster of the family Enterobacteriaceae is positively regulated by UreR, a member of the AraC family of transcriptional activators. J. Bacteriol. 175, 3459-3467 (1993). (Pubitemid 23163390)
51. Island, M. D. & Mobley, H. L. Proteus mirabilis urease: operon fusion and linker insertion analysis of ure gene organization, regulation, and function. J. Bacteriol. 177, 5653-5660 (1995). (Pubitemid 26028877)
52. Nicholson, E. B., Concaugh, E. A., Foxall, P. A., Island, M. D. & Mobley, H. L. Proteus mirabilis urease: transcriptional regulation by UreR. J. Bacteriol. 175, 465-473 (1993). (Pubitemid 23032008)
53. Griffith, D. P., Musher, D. M. & Itin, C. Urease. The primary cause of infection-induced urinary stones. Invest. Urol. 13, 346-350 (1976).
54. Nicholson, E. B., Concaugh, E. A. & Mobley, H. L. Proteus mirabilis urease: use of a ureA-lacZ fusion demonstrates that induction is highly specific for urea. Infect. Immun. 59, 3360-3365 (1991).
55. Sabbuba, N. A., Mahenthiralingam, E. & Stickler, D. J. Molecular epidemiology of Proteus mirabilis infections of the catheterized urinary tract. J. Clin. Microbiol. 41, 4961-4965 (2003). (Pubitemid 37429902)
56. Kunin, C. M. Urinary Tract Infections: Detection, Prevention, and Management (Williams & Wilkins, 1997).
57. Zhao, H., Thompson, R. B., Lockatell, V., Johnson, D. E. & Mobley, H. L. T. Use of green fluorescent protein to assess urease gene expression by uropathogenic Proteus mirabilis during experimental ascending urinary tract infection. Infect. Immun. 66, 330-335 (1998). (Pubitemid 28018837)
58. Johnson, D. E. et al. 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 (1993). (Pubitemid 23182265)
59. Jones, B. D., Lockatell, C. V., Johnson, D. E., Warren, J. W. & Mobley, H. L. Construction of a urease-negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect. Immun. 58, 1120-1123 (1990). (Pubitemid 20117050)
60. Dattelbaum, J. D., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. T. UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster, is required for urease activity and virulence in experimental urinary tract infections. Infect. Immun. 71, 1026-1030 (2003). (Pubitemid 36150803)
61. Alamuri, P. et al. Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis. Infect. Immun. 78, 4882-4894 (2010).
62. Zunino, P. et al. Mannose-resistant proteus-like and P. mirabilis fimbriae have specific and additive roles in P. mirabilis urinary tract infections. FEMS Immunol. Med. Microbiol. 51, 125-133 (2007). (Pubitemid 47387486)
63. Sareneva, T., Holthofer, H. & Korhonen, T. K. Tissue-binding affinity of Proteus mirabilis fimbriae in the human urinary tract. Infect. Immun. 58, 3330-3336 (1990). (Pubitemid 20293444)
64. Lee, K. K., Harrison, B. A., Latta, R. & Altman, E. The binding of Proteus mirabilis nonagglutinating fimbriae to ganglio-series asialoglycolipids and lactosyl ceramide. Can. J. Microbiol. 46, 961-966 (2000).
65. Massad, G., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. Proteus mirabilis fimbriae: construction of an isogenic pmfA mutant and analysis of virulence in a CBA mouse model of ascending urinary tract infection. Infect. Immun. 62, 536-542 (1994). (Pubitemid 24033773)
66. Zunino, P. et al. Proteus mirabilis fimbriae (PMF) are important for both bladder and kidney colonization in mice. Microbiology 149, 3231-3237 (2003). (Pubitemid 37442006)
67. Pearson, M. M., Yep, A., Smith, S. N. & Mobley, H. L. T. Transcriptome of Proteus mirabilis in the murine urinary tract: virulence and nitrogen assimilation gene expression. Infect. Immun. 79, 2619-2631 (2011).
68. Zunino, P. et al. New aspects of the role of MR/P fimbriae in Proteus mirabilis urinary tract infection. FEMS Immunol. Med. Microbiol. 31, 113-120 (2001). (Pubitemid 32822875)
69. Bahrani, F. K. et al. Construction of an MR/P fimbrial mutant of Proteus mirabilis: role in virulence in a mouse model of ascending urinary tract infection. Infect. Immun. 62, 3363-3371 (1994). (Pubitemid 24232122)
70. Zhao, H., Li, X., Johnson, D. E., Blomfield, I. & Mobley, H. L. In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Mol. Microbiol. 23, 1009-1019 (1997). (Pubitemid 27096736)
71. Li, X., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. T. Identification of MrpI as the sole recombinase that regulates the phase variation of MR/P fimbria, a bladder colonization factor of uropathogenic Proteus mirabilis. Mol. Microbiol. 45, 865-874 (2002). (Pubitemid 34989191)
72. Jansen, A. M., Lockatell, V., Johnson, D. E. & Mobley, H. L. T. Mannose-resistant proteus-like fimbriae are produced by most Proteus mirabilis strains infecting the urinary tract, dictate the in vivo localization of bacteria, and contribute to biofilm formation. Infect. Immun. 72, 7294-7305 (2004). (Pubitemid 39552401)
73. Latta, R. K., Grondin, A., Jarrell, H. C., Nicholls, G. R. & Berube, L. R. Differential expression of nonagglutinating fimbriae and MR/P Pili in swarming colonies of Proteus mirabilis. J. Bacteriol. 181, 3220-3225 (1999). (Pubitemid 29236929)
74. Mobley, H. et al. Construction of a flagellum-negative mutant of Proteus mirabilis: effect on internalization by human renal epithelial cells and virulence in a mouse model of ascending urinary tract infection. Infect. Immun. 64, 5332-5340 (1996). (Pubitemid 26404000)
75. Li, X., Rasko, D. A., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. T. Repression of bacterial motility by a novel fimbrial gene product. EMBO J. 20, 4854-4862 (2001). (Pubitemid 32848637)
76. Pearson, M. M. & Mobley, H. L. T. Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis. Mol. Microbiol. 69, 548-558 (2008). (Pubitemid 351988024)
77. Lane, M. C., Li, X., Pearson, M. M., Simms, A. N. & Mobley, H. L. T. Oxygen-limiting conditions enrich for fimbriate cells of uropathogenic Proteus mirabilis and Escherichia coli. J. Bacteriol. 191, 1382-1392 (2009).
78. Jansen, A. M., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. T. Visualization of Proteus mirabilis morphotypes in the urinary tract: the elongated swarmer cell is rarely observed in ascending urinary tract infection. Infect. Immun. 71, 3607-3613 (2003). (Pubitemid 36637591)
79. Allison, C., Emödy, L., Coleman, N. & Hughes, C. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J. Infect. Dis. 169, 1155-1158 (1994). (Pubitemid 24303248)
80. Li, X. et al. Visualization of Proteus mirabilis within the matrix of urease-induced bladder stones during experimental urinary tract infection. Infect. Immun. 70, 389-394 (2002). (Pubitemid 34028639)
81. Miles, A. A. & Khimji, P. L. Enterobacterial chelators of iron: their occurrence, detection, and relation to pathogenicity. J. Med. Microbiol. 8, 477-490 (1975).
82. Lima, A., Zunino, P., D'Alessandro, B. & Piccini, C. An iron-regulated outer-membrane protein of Proteus mirabilis is a haem receptor that plays an important role in urinary tract infection and in in vivo growth. J. Med. Microbiol. 56, 1600-1607 (2007). (Pubitemid 350276508)
83. Nielubowicz, G. R., Smith, S. N. & Mobley, H. L. T. Outer membrane antigens of the uropathogen Proteus mirabilis recognized by the humoral response during experimental murine urinary tract infection. Infect. Immun. 76, 4222-4231 (2008).
84. Himpsl, S. D. et al. Proteobactin and a yersiniabactin-related siderophore mediate iron acquisition in Proteus mirabilis. Mol. Microbiol. 78, 138-157 (2010).
85. Gaisser, S. & Hughes, C. A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming-defective Proteus mirabilis strain. Mol. Gen. Genet. 253, 415-427 (1997).
86. Flannery, E. L., Mody, L. & Mobley, H. L. T. Identification of a modular pathogenicity island that is widespread among urease-producing uropathogens and shares features with a diverse group of mobile elements. Infect. Immun. 77, 4887-4894 (2009).
87. Nielubowicz, G. R., Smith, S. N. & Mobley, H. L. T. Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect. Immun. 78, 2823-2833 (2010).
88. Wang, S., Fleming, R. T., Westbrook, E. M., Matsumura, P. & McKay, D. B. Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J. Mol. Biol. 355, 798-808 (2006). (Pubitemid 41817637)
89. Peerbooms, P. G., Verweij, A. M. & MacLaren, D. M. Vero cell invasiveness of Proteus mirabilis. Infect. Immun. 43, 1068-1071 (1984). (Pubitemid 14192001)
90. Chippendale, G. R., Warren, J. W., Trifillis, A. L. & Mobley, H. L. Internalization of Proteus mirabilis by human renal epithelial cells. Infect. Immun. 62, 3115-3121 (1994). (Pubitemid 24232090)
91. Mobley, H. L., Chippendale, G. R., Swihart, K. G. & Welch, R. A. Cytotoxicity of the HpmA hemolysin and urease of Proteus mirabilis and Proteus vulgaris against cultured human renal proximal tubular epithelial cells. Infect. Immun. 59, 2036-2042 (1991).
92. Alamuri, P., Eaton, K. A., Himpsl, S. D., Smith, S. N. & Mobley, H. L. T. Vaccination with proteus toxic agglutinin, a hemolysin-independent cytotoxin in vivo, protects against Proteus mirabilis urinary tract infection. Infect. Immun. 77, 632-641 (2009).
93. Swihart, K. G. & Welch, R. A. Cytotoxic activity of the Proteus hemolysin HpmA. Infect. Immun. 58, 1861-1869 (1990). (Pubitemid 20176384)
94. Alamuri, P. & Mobley, H. L. T. A novel autotransporter of uropathogenic Proteus mirabilis is both a cytotoxin and an agglutinin. Mol. Microbiol. 68, 997-1017 (2008). (Pubitemid 351581060)
95. Pearson, M. M. & Mobley, H. L. T. The type III secretion system of Proteus mirabilis HI4320 does not contribute to virulence in the mouse model of ascending urinary tract infection. J. Med. Microbiol. 56, 1277-1283 (2007). (Pubitemid 350105592)
96. Bahrani, F. K. & Mobley, H. L. Proteus mirabilis MR/P fimbrial operon: genetic organization, nucleotide sequence, and conditions for expression. J. Bacteriol. 176, 3412-3419 (1994). (Pubitemid 24166740)
97. Klemm, P., Jorgensen, B. J., Kreft, B. & Christiansen, G. The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs. J. Bacteriol. 177, 621-627 (1995).
98. Belas, R. Expression of multiple flagellin-encoding genes of Proteus mirabilis. J. Bacteriol. 176, 7169-7181 (1994). (Pubitemid 24364042)
99. Murphy, C. A. & Belas, R. Genomic rearrangements in the flagellin genes of Proteus mirabilis. Mol. Microbiol. 31, 679-690 (1999). (Pubitemid 29046108)
100. Senior, B. W., Loomes, L. M. & Kerr, M. A. The production and activity in vivo of Proteus mirabilis IgA protease in infections of the urinary tract. J. Med. Microbiol. 35, 203-207 (1991).
101. Belas, R., Manos, J. & Suvanasuthi, R. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect. Immun. 72, 5159-5167 (2004). (Pubitemid 39223401)
102. Walker, K. E., Moghaddame-Jafari, S., Lockatell, C. V., Johnson, D. & Belas, R. ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol. Microbiol. 32, 825-836 (1999). (Pubitemid 29241522)
103. Mathoera, R. B., Kok, D. J., Verduin, C. M. & Nijman, R. J. M. Pathological and therapeutic significance of cellular invasion by Proteus mirabilis in an enterocystoplasty infection stone model. Infect. Immun. 70, 7022-7032 (2002). (Pubitemid 35387938)
104. Dienes, L. Reproductive processes in Proteus cultures. Proc. Soc. Exp. Biol. Med. 63, 265-270 (1946).
105. Budding, A. E., Ingham, C. J., Bitter, W., Vandenbroucke-Grauls, C. M. & Schneeberger, P. M. The dienes phenomenon: competition and territoriality in swarming Proteus mirabilis. J. Bacteriol. 191, 3892-3900 (2009).
106. Senior, B. W. Typing of Proteus strains by proticine production and sensitivity. J. Med. Microbiol. 10, 7-17 (1977). (Pubitemid 8039336)
107. Gibbs, K. A., Urbanowski, M. L. & Greenberg, E. P. Genetic determinants of self identity and social recognition in bacteria. Science 321, 256-259 (2008). (Pubitemid 351989098)
108. Gibbs, K. A., Wenren, L. M. & Greenberg, E. P. Identity gene expression in Proteus mirabilis. J. Bacteriol. 193, 3286-3292 (2011).
109. MacIntyre, D. L., Miyata, S. T., Kitaoka, M. & Pukatzki, S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl Acad. Sci. USA 107, 19520-19524 (2010).
110. Snyder, J. A. et al. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect. Immun. 72, 6373-6381 (2004). (Pubitemid 39425418)
111. Flannery, E. L., Antczak, S. M. & Mobley, H. L. T. Self-transmissibility of the integrative and conjugative element ICEPm1 between clinical isolates requires a functional integrase, relaxase, and type IV secretion system. J. Bacteriol. 193, 4104-4112 (2011).
112. Boyer, M. & Wisniewski-Dye, F. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70, 1-19 (2009).
113. Belas, R., Schneider, R. & Melch, M. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J. Bacteriol. 180, 6126-6139 (1998). (Pubitemid 28544242)
114. Bainton, N. J. et al. A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116, 87-91 (1992).
115. Holden, M. T. G. et al. Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol. Microbiol. 33, 1254-1266 (1999). (Pubitemid 29433630)
116. Stankowska, D. et al. Influence of quorum sensing signal molecules on biofilm formation in Proteus mirabilis O18. Folia Microbiol. (Praha) 57, 53-60 (2012).
117. Stankowska, D., Kwinkowski, M. & Kaca, W. Quantification of Proteus mirabilis virulence factors and modulation by acylated homoserine lactones. J. Microbiol. Immunol. Infect. 41, 243-253 (2008).
118. Liaw, S.-J., Lai, H.-C. & Wang, W.-B. Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect. Immun. 72, 6836-6845 (2004). (Pubitemid 39552351)
119. Schneider, R., Lockatell, C. V., Johnson, D. & Belas, R. Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148, 773-782 (2002). (Pubitemid 34232861)
120. Sturgill, G. & Rather, P. N. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol. Microbiol. 51, 437-446 (2004). (Pubitemid 38142132)
121. Vinogradov, E. & Perry, M. B. Structural analysis of the core region of lipopolysaccharides from Proteus mirabilis serotypes O6, O48 and O57. Eur. J. Biochem. 267, 2439-2447 (2000).
122. Scavone, P., Sosa, V., Pellegrino, R., Galvalisi, U. & Zunino, P. Mucosal vaccination of mice with recombinant Proteus mirabilis structural fimbrial proteins. Microbes Infect. 6, 853-860 (2004). (Pubitemid 39055546)
123. Scavone, P. et al. 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 (2007). (Pubitemid 46901040)
124. Pellegrino, R., Galvalisi, U., Scavone, P., Sosa, V. & Zunino, P. Evaluation of Proteus mirabilis structural fimbrial proteins as antigens against urinary tract infections. FEMS Immunol. Med. Microbiol. 36, 103-110 (2003). (Pubitemid 36515091)
125. Li, X. et al. Use of translational fusion of the MrpH fimbrial adhesin-binding domain with the cholera toxin A2 domain, coexpressed with the cholera toxin B subunit, as an intranasal vaccine to prevent experimental urinary tract infection by Proteus mirabilis. Infect. Immun. 72, 7306-7310 (2004). (Pubitemid 39552402)
126. Li, X. et al. Development of an intranasal vaccine to prevent. urinary tract infection by Proteus mirabilis. Infect. Immun. 72, 66-75 (2004). (Pubitemid 38018162)
127. Armitage, J. P. Changes in metabolic activity of Proteus mirabilis during swarming. J. Gen. Microbiol. 125, 445-450 (1981). (Pubitemid 12238801)
128. Pearson, M. M., Rasko, D. A., Smith, S. N. & Mobley, H. L. T. Transcriptome of swarming Proteus mirabilis. Infect. Immun. 78, 2834-2845 (2010).
129. Majdalani, N., Heck, M., Stout, V. & Gottesman, S. Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J. Bacteriol. 187, 6770-6778 (2005). (Pubitemid 41356251)
130. Clemmer, K. M. & Rather, P. N. Regulation of flhDC expression in Proteus mirabilis. Res. Microbiol. 158, 295-302 (2007). (Pubitemid 46484024)
131. Cusick, K., Lee, Y. Y., Youchak, B. & Belas, R. Perturbation of FliL interferes with Proteus mirabilis swarmer cell gene expression and differentiation. J. Bacteriol. 194, 437-447 (2011).
132. Morgenstein, R. M. & Rather, P. N. Role of the Umo proteins and the Rcs phosphorelay in the swarming motility of wild-type and an O-antigen (waaL) mutant of Proteus mirabilis. J. Bacteriol. 194, 669-676 (2012).
133. Hatt, J. K. & Rather, P. N. Characterization of a novel gene, wosA, regulating FlhDC expression in Proteus mirabilis. J. Bacteriol. 190, 1946-1955 (2008). (Pubitemid 351355317)
134. Dufour, A., Furness, R. B. & Hughes, C. Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol. Microbiol. 29, 741-751 (1998). (Pubitemid 28365461)
135. Clemmer, K. M. & Rather, P. N. The Lon protease regulates swarming motility and virulence gene expression in Proteus mirabilis. J. Med. Microbiol. 57, 931-937 (2008).
136. Jiang, S.-S. et al. Characterization of UDP-glucose dehydrogenase and UDP-glucose pyrophosphorylase mutants of Proteus mirabilis: defectiveness in polymyxin B resistance, swarming, and virulence. Antimicrob. Agents Chemother. 54, 2000-2009 (2010).
137. Wang, W.-B. et al. Role of RppA in the regulation of polymyxin B susceptibility, swarming, and virulence factor expression in Proteus mirabilis. Infect. Immun. 76, 2051-2062 (2008). (Pubitemid 351656138)
138. Stevenson, L. G. & Rather, P. N. A. Novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis. J. Bacteriol. 188, 7830-7839 (2006). (Pubitemid 44764520)
139. Liaw, S.-J., Lai, H.-C., Ho, S.-W., Luh, K.-T. & Wang, W.-B. Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J. Med. Microbiol. 52, 19-28 (2003). (Pubitemid 36106364)