Establishment of systemic Brucella melitensis infection through the digestive tract requires urease, the type IV secretion system, and lipopolysaccharide O antigen

Infection and Immunity

Volumn 77, Issue 10, 2009, Pages 4197-4208

  Paixão, Tatiane A ^a,b   Roux, Christelle M ^a   Den Hartigh, Andreas B ^a   Sankaran Walters, Sumathi ^a   Dandekar, Satya ^a   Santos, Renato L ^b   Tsolis, Renée M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL ENZYME; BACTERIUM LIPOPOLYSACCHARIDE; BILE SALT; O ANTIGEN; PHOSPHOMANNOMUTASE; UREASE; VIRB PROTEIN; VIRULENCE FACTOR;

ACIDITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BRUCELLA MELITENSIS; BRUCELLOSIS; COLON; CONTROLLED STUDY; DIGESTIVE SYSTEM; EPITHELIUM CELL; FEMALE; GENETIC SIMILARITY; ILEUM; IN VITRO STUDY; INOCULATION; INTESTINE; INTESTINE CELL; LIVER; LYMPHOEPITHELIAL CEL; LYMPHOID TISSUE; MESENTERY LYMPH NODE; MICROBIAL ATTENUATION; MONOLAYER CULTURE; MOUSE; MOUTH INFECTION; MUCOSA ASSOCIATED LYMPHOID TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; SPECIES COMPARISON; SPLEEN; TYPE IV SECRETION SYSTEM; URE1 GENE; UREABC GENE; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; BRUCELLA MELITENSIS; CELL LINE; COLON; COLONY COUNT, MICROBIAL; ENTEROCYTES; FEMALE; GASTROINTESTINAL TRACT; GENE DELETION; ILEUM; LIPOPOLYSACCHARIDES; LIVER; LYMPH NODES; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; O ANTIGENS; SPLEEN; UREASE; VIRULENCE FACTORS;

EID: 70349428439     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00417-09     Document Type: Article

References (61)

1. Ackermann, M. R., N. F. Cheville, and B. L. Deyoe. 1988. Bovine ileal dome lymphoepithelial cells: endocytosis and transport of Brucella abortus strain 19. Vet. Pathol. 25:28-35.
2. Allen, C. A., L. G. Adams, and T. A. Ficht. 1998. Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect. Immun. 66:1008-1016.
3. Alton, G. G., L. M. Jones, R. D. Angus, and J. M. Verger. 1988. Techniques for the brucellosis laboratory. INRA Publications, Paris, France.
4. Bandara, A. B., A. Contreras, A. Contreras-Rodriguez, A. M. Martins, V. Dobrean, S. Poff-Reichow, P. Rajasekaran, N. Sriranganathan, G. G. Schurig, and S. M. Boyle. 2007. Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol. 7:57.
5. Barnes, P. D., M. A. Bergman, J. Mecsas, and R. R. Isberg. 2006. Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J. Exp. Med. 203:1591-1601.
6. Barquero-Calvo, E., E. Chaves-Olarte, D. S. Weiss, C. Guzman-Verri, C. Chacon-Diaz, A. Rucavado, I. Moriyon, and E. Moreno. 2007. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS One 2:e631.
7. Billard, E., C. Cazevieille, J. Dornand, and A. Gross. 2005. High susceptibility of human dendritic cells to invasion by the intracellular pathogens Brucella suis, B. abortus, and B. melitensis. Infect. Immun. 73:8418-8424. (Pubitemid 41740335)
8. Borriello, S. P. 1984. Bacteria and gastrointestinal secretion and motility. Scand. J. Gastroenterol. Suppl. 93:115-121.
9. Boschiroli, M. L., S. Ouahrani-Bettache, V. Foulongne, S. Michaux-Charachon, G. Bourg, A. Allardet-Servent, C. Cazevieille, J. P. Lavigne, J. P. Liautard, M. Ramuz, and D. O'Callaghan. 2002. Type IV secretion and Brucella virulence. Vet. Microbiol. 90:341-348.
10. Carvalho Neta, A. V., A. P. Stynen, T. A. Paixão, K. L. Miranda, F. L. Silva, C. M. Roux, R. M. Tsolis, R. E. Everts, H. A. Lewin, L. G. Adams, A. F. Carvalho, A. P. Lage, and R. L. Santos. 2008. Modulation of the bovine trophoblastic innate immune response by Brucella abortus. Infect. Immun. 76:1897-1907.
11. Chain, P. S., D. J. Comerci, M. E. Tolmasky, F. W. Larimer, S. A. Malfatti, L. M. Vergez, F. Aguero, M. L. Land, R. A. Ugalde, and E. Garcia. 2005. Whole-genome analyses of speciation events in pathogenic brucellae. Infect. Immun. 73:8353-8361.
12. Cirl, C., A. Wieser, M. Yadav, S. Duerr, S. Schubert, H. Fischer, D. Stappert, N. Wantia, N. Rodriguez, H. Wagner, C. Svanborg, and T. Miethke. 2008. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 14:399-406.
13. Collins, C. M., and S. E. D'Orazio. 1993. Bacterial ureases: structure, regulation of expression and role in pathogenesis. Mol. Microbiol. 9:907-913.
14. Contreras-Rodriguez, A., J. Quiroz-Limon, A. M. Martins, H. Peralta, E. Avila-Calderon, N. Sriranganathan, S. M. Boyle, and A. Lopez-Merino. 2008. Enzymatic, immunological and phylogenetic characterization of Brucella suis urease. BMC Microbiol. 8:121.
15. Corbel, M. J. 1997. Brucellosis: an overview. Emerg. Infect. Dis. 3:213-221.
16. Corbel, M. J., and D. M. Hendry. 1985. Urease activity of Brucella species. Res. Vet. Sci. 38:252-253.
17. Dean, P., and B. Kenny. 2004. Intestinal barrier dysfunction by enteropathogenic Escherichia coli is mediated by two effector molecules and a bacterial surface protein. Mol. Microbiol. 54:665-675.
18. Delpino, M. V., M. I. Marchesini, S. M. Estein, D. J. Comerci, J. Cassataro, C. A. Fossati, and P. C. Baldi. 2007. A bile salt hydrolase of Brucella abortus contributes to the establishment of a successful infection through the oral route in mice. Infect. Immun. 75:299-305.
19. den Hartigh, A. B., Y. H. Sun, D. Sondervan, N. Heuvelmans, M. O. Reinders, T. A. Ficht, and R. M. Tsolis. 2004. Differential requirements for VirB1 and VirB2 during Brucella abortus infection. Infect. Immun. 72:5143-5149.
20. Enright, F. M., L. N. Araya, P. H. Elzer, G. E. Rowe, and A. J. Winter. 1990. Comparative histopathology in BALB/c mice infected with virulent and attenuated strains of Brucella abortus. Vet. Immunol. Immunopathol. 26:171-182.
21. Ficht, T. A. 2003. Intracellular survival of Brucella: defining the link with persistence. Vet. Microbiol. 2516:1-11.
22. Fleischner, E. C., M. Vecki, E. B. Shaw, and K. F. Meyer. 1921. The pathogenicity of B. abortus and B. melitensis for monkeys. Studies on the genus Brucella nov. gen. III. J. Infect. Dis. 29:663-705.
23. Godfroid, J., A. Cloeckaert, J. P. Liautard, S. Kohler, D. Fretin, K. Walravens, B. Garin-Bastuji, and J. J. Letesson. 2005. From the discovery of the Malta fever's agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis. Vet. Res. 36:313-326.
24. Gorvel, J. P., and E. Moreno. 2002. Brucella intracellular life: from invasion to intracellular replication. Vet. Microbiol. 90:281-297.
25. Gullberg, E., M. Leonard, J. Karlsson, A. M. Hopkins, D. Brayden, A. W. Baird, and P. Artursson. 2000. Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem. Biophys. Res. Commun. 279:808-813.
26. Hong, P. C., R. M. Tsolis, and T. A. Ficht. 2000. Identification of genes required for chronic persistence of Brucella abortus in mice. Infect. Immun. 68:4102-4107.
27. Izadjoo, M. J., M. G. Mense, A. K. Bhattacharjee, T. L. Hadfield, R. M. Crawford, and D. L. Hoover. 2008. A study on the use of male animal models for developing a live vaccine for brucellosis. Transbound. Emerg. Dis. 55:145-151.
28. Jenner, R. G., and R. A. Young. 2005. Insights into host responses against pathogens from transcriptional profiling. Nat. Rev. Microbiol. 3:281-294.
29. Jiménez De Bagüés, M. P., A. Terraza, A. Gross, and J. Dornand. 2004. Different responses of macrophages to smooth and rough Brucella spp.: relationship to virulence. Infect. Immun. 72:2429-2433.
30. Jorens, P. G., P. P. Michielsen, E. J. Van den Enden, N. H. Bourgeois, E. A. Van Marck, G. R. Krueger, A. M. Ramon, and Y. M. Van Maercke. 1991. A rare cause of colitis-Brucella melitensis. Report of a case. Dis. Colon Rectum 34:194-196.
31. Kerneis, S., A. Bogdanova, J. P. Kraehenbuhl, and E. Pringault. 1997. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277:949-952. (Pubitemid 27366679)
32. Lapaque, N., I. Moriyon, E. Moreno, and J. P. Gorvel. 2005. Brucella lipopolysaccharide acts as a virulence factor. Curr. Opin. Microbiol. 8:60-66.
33. -ΔΔCT method 25:402-408.
34. Luna-Martinez, J. E., and C. Mejia-Teran. 2002. Brucellosis in Mexico: current status and trends. Vet. Microbiol. 90:19-30.
35. Magalhaes, J. G., I. Tattoli, and S. E. Girardin. 2007. The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens. Semin. Immunol. 19:106-115.
36. Mantur, B. G., S. K. Amarnath, and R. S. Shinde. 2007. Review of clinical and laboratory features of human brucellosis. Indian J. Med. Microbiol. 25:188-202.
37. Martinez-Argudo, I., and M. A. Jepson. 2008. Salmonella translocates across an in vitro M cell model independently of SPI-1 and SPI-2. Microbiology 154:3887-3894.
38. Meador, V. P., L. B. Tabatabai, W. A. Hagemoser, and B. L. Deyoe. 1986. Identification of Brucella abortus in formalin-fixed, paraffin-embedded tissues of cows, goats, and mice with an avidin-biotin-peroxidase complex immunoenzymatic staining technique. Am. J. Vet. Res. 47:2147-2150.
39. Mense, M. G., L. L. Van De Verg, A. K. Bhattacharjee, J. L. Garrett, J. A. Hart, L. E. Lindler, T. L. Hadfield, and D. L. Hoover. 2001. Bacteriologic and histologic features in mice after intranasal inoculation of Brucella melitensis. Am. J. Vet. Res. 62:398-405.
40. Miller, C. P., and M. Bohnhoff. 1963. Changes in the mouse's enteric microflora associated with enhanced susceptibility to Salmonella infection following streptomycin treatment. J. Infect. Dis. 113:59-66.
41. Morales Otero, P. 1948. Studies of Brucella infection in Puerto Rico. University of Puerto Rico, San Juan.
42. O'Callaghan, D., C. Cazevieille, A. Allardet-Servent, M. L. Boschiroli, G. Bourg, V. Foulongne, P. Frutos, Y. Kulakov, and M. Ramuz. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1210-1220.
43. Pappas, G., and P. Papadimitriou. 2007. Challenges in Brucella bacteraemia. Int. J. Antimicrob. Agents 30(Suppl. 1):S29-S31.
44. Pappas, G., P. Papadimitriou, N. Akritidis, L. Christou, and E. V. Tsianos. 2006. The new global map of human brucellosis. Lancet Infect. Dis. 6:91-99.
45. Pasquali, P., A. Rosanna, C. Pistoia, P. Petrucci, and F. Ciuchini. 2003. Brucella abortus RB51 induces protection in mice orally infected with the virulent strain B. abortus 2308. Infect. Immun. 71:2326-2330. (Pubitemid 36519842)
46. Pasquali, P., R. Adone, L. C. Gasbarre, C. Pistoia, and F. Ciuchini. 2001. Mouse cytokine profiles associated with Brucella abortus RB51 vaccination or B. abortus 2308 infection. Infect. Immun. 69:6541-6544.
47. Paulsen, I. T., R. Seshadri, K. E. Nelson, J. A. Eisen, J. F. Heidelberg, T. D. Read, R. J. Dodson, L. Umayam, L. M. Brinkac, M. J. Beanan, S. C. Daugherty, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, W. C. Nelson, B. Ayodeji, M. Kraul, J. Shetty, J. Malek, S. E. Van Aken, S. Riedmuller, H. Tettelin, S. R. Gill, O. White, S. L. Salzberg, D. L. Hoover, L. E. Lindler, S. M. Halling, S. M. Boyle, and C. M. Fraser. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99:13148-13153.
48. Petrella, R., and E. J. Young. 1988. Acute brucella ileitis. Am. J. Gastroenterol. 83:80-82.
49. Potasman, I., L. Even, M. Banai, E. Cohen, D. Angel, and M. Jaffe. 1991. Brucellosis: an unusual diagnosis for a seronegative patient with abscesses, osteomyelitis, and ulcerative colitis. Rev. Infect. Dis. 13:1039-1042.
50. Raffatellu, M., D. Chessa, R. P. Wilson, R. Dusold, S. Rubino, and A. J. Bäumler. 2005. The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect. Immun. 73:3367-3374.
51. Raffatellu, M., R. L. Santos, D. Chessa, R. P. Wilson, S. E. Winter, C. A. Rossetti, S. D. Lawhon, H. Chu, T. Lau, C. L. Bevins, L. G. Adams, and A. J. Bäumler. 2007. The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect. Immun. 75:4342-4350. (Pubitemid 47378091)
52. Raffatellu, M., R. P. Wilson, D. Chessa, H. Andrews-Polymenis, Q. T. Tran, S. Lawhon, S. Khare, L. G. Adams, and A. J. Bäumler. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73:146-154.
53. Ragnarsson, E. G., I. Schoultz, E. Gullberg, A. H. Carlsson, F. Tafazoli, M. Lerm, K. E. Magnusson, J. D. Soderholm, and P. Artursson. 2008. Yersinia pseudotuberculosis induces transcytosis of nanoparticles across human intestinal villus epithelium via invasin-dependent macropinocytosis. Lab. Investig. 88:1215-1226.
54. Rolán, H. G., and R. M. Tsolis. 2007. Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization. Infect. Immun. 75:2965-2973.
55. Roux, C. M., H. G. Rolan, R. L. Santos, P. D. Beremand, T. L. Thomas, L. G. Adams, and R. M. Tsolis. 2007. Brucella requires a functional type IV secretion system to elicit innate immune responses of mice. Cell. Microbiol. 9:1851-1869.
56. Salcedo, S. P., M. I. Marchesini, H. Lelouard, E. Fugier, G. Jolly, S. Balor, A. Muller, N. Lapaque, O. Demaria, L. Alexopoulou, D. J. Comerci, R. A. Ugalde, P. Pierre, and J. P. Gorvel. 2008. Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog. 4:e21.
57. Sangari, F. J., A. Seoane, M. C. Rodriguez, J. Aguero, and J. M. Garcia Lobo. 2007. Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infect. Immun. 75:774-780.
58. Sieira, R., D. J. Comerci, D. O. Sanchez, and R. A. Ugalde. 2000. A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J. Bacteriol. 182:4849-4855.
59. Stermer, E., N. Levy, I. Potasman, M. Jaffe, and J. Boss. 1991. Brucellosis as a cause of severe colitis. Am. J. Gastroenterol. 86:917-919.
60. Tsolis, R. M., G. M. Young, J. V. Solnick, and A. J. Bäumler. 2008. From bench to bedside: stealth of enteroinvasive pathogens. Nat. Rev. Microbiol. 6:883-892.
61. Winter, S. E., M. Raffatellu, R. P. Wilson, H. Russmann, and A. J. Bäumler. 2008. The Salmonella enterica serotype Typhi regulator TviA reduces interleukin-8 production in intestinal epithelial cells by repressing flagellin secretion. Cell. Microbiol. 10:247-261.