The predicted ABC transporter AbcEDCBA is required for type IV secretion system expression and lysosomal evasion by Brucella ovis

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Silva, Teane M A ^a   Mol, Juliana P S ^a   Winter, Maria G ^b   Atluri, Vidya ^b   Xavier, Mariana N ^b   Pires, Simone F ^a   Paixão, Tatiane A ^a   Andrade, Hélida M ^a   Santos, Renato L ^a   Tsolis, Renee M ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER EDCBA; BACTERIAL PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; UNCLASSIFIED DRUG; VIRB11 PROTEIN; VIRB8 PROTEIN; TYPE IV SECRETION SYSTEM;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BRUCELLA OVIS; CELL FUSION; CELL MIGRATION; CELL SURVIVAL; CELLULAR PARAMETERS; CONTROLLED STUDY; GENE LOCUS; HELA CELL LINE; HUTC GENE; IN VITRO STUDY; LYSOSOMAL EVASION; NONHUMAN; PHAGOSOME; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PSEUDOGENE; TRANSCRIPTION REGULATION; TYPE IV SECRETION SYSTEM; VIRB1 GENE; VIRB8 GENE; VJBR GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; HUMAN; LYSOSOME; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY;

BRUCELLA MELITENSIS BIOVAR OVIS;

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BRUCELLA OVIS; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LYSOSOMES; MICROBIAL VIABILITY; PHAGOSOMES; TYPE IV SECRETION SYSTEMS;

EID: 84915819043     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114532     Document Type: Article

References (65)

1. Burgess GW (1982) Ovine contagious epididymitis: a review. Vet Microbiol 7: 551-575.
2. Blasco JM (1990) Brucella ovis. In: Nielsen K, Duncan JR, eds. Animal Brucellosis. Boca Raton: CRC Press. pp 351-378.
3. Ficapal A, Jordana J, Blasco J, Moriyon I (1998) Diagnosis and epidemiology of Brucella ovis infection in rams. Small Rumin Res 29: 13-19.
4. Carpenter TE, Berry SL, Glenn JS (1987) Economics of Brucella ovis control in sheep: epidemiologic simulation model. J Am Vet Med Assoc 190: 977-982.
5. Godfroid J, Cloeckaert A, Liautard JP, Kohler S, Fretin D, et al. (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.
6. Thoen CO, Enright F, Cheville NF (1993) Brucella. In: Gyles CL, Thoen CO, eds. Pathogenesis of bacterial infections in animals. Ames: Iowa State University Press. pp. 236-247.
7. Gorvel JP, Moreno E (2002) Brucella intracellular life: from invasion to intracellular replication. Vet Microbiol 90: 281-297.
8. O'Callaghan D, Cazevieille C, Allardet-Servent A, Boschiroli ML, Bourg G, et al. (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.
9. Hong PC, Tsolis RM, Ficht TA (2000) Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68: 4102-4107.
10. Sieira R, Comerci DJ, Sanchez DO, Ugalde RA (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: 849-855.
11. Rosinha GMS, Freitas DA, Miyoshi A, Azevedo V, Campos E, et al. (2002) Identification and characterization of a Brucella abortus ATP-binding cassette transporter homolog to Rhizobium meliloti ExsA and its role in virulence and protection in mice. Infect Immun 70: 5036-5044.
12. den Hartigh AB, Sun YH, Sondervan D, Marjolein N, Reinders O et al. (2004) Differential requirements for VirB1 and VirB2 during Brucella abortus infection. Infect Immun 72: 143-149.
13. Rolan HG, Tsolis RM (2007) Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization. Infect Immun 75: 2965-2973.
14. Paixão TA, Roux CM, den Hartigh AB, Sankaran-Walters S, Dandekar S, et al. (2009) Establishment of systemic Brucella melitensis infection through the digestive tract requires urease, the type IV secretion system, and lipopolysaccharide O antigen. Infect Immun 77: 4197-4208.
15. Zhong Z, Wang Y, Qiao F, Wang Z, Du X, et al. (2009) Cytotoxicity of Brucella smooth strains for macrophages is mediated by increased secretion of the type IV secretion system. Microbiol 155: 3392-3402.
16. Sá JC, Silva TMA, Costa EA, Silva APC, Tsolis RM, et al. (2012) The virB encode type IV secretion system is critical for establishment of infection and persistence of Brucella ovis infection in mice. PloS ONE 159: 130-140.
17. Celli J, de Chastellier C, Franchini D-M, Pizarro-Cerda J, Moreno E, et al. (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198: 545-556.
18. Tsolis RM, Seshadri R, Santos RL, Sangari FJ, Lobo JMG, et al. (2009) Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism. PloS ONE 4: e5519.
19. Silva TMA, Paixão TA, Costa EA, Xavier MN, Sá JC, et al. (2011) Putative ATP-binding cassette transporter is essential for Brucella ovis pathogenesis in mice. Infect Immun 79: 1706-1717.
20. Tam R, Saier MH (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57: 320-346.
21. Ko J, Splitter GA (2000) Brucella abortus tandem repeated ATP-binding proteins, BapA and BapB, homologs of Haemophilus influenzae LktB, are not necessary for intracellular survival. Microb Pathog 29: 245-253.
22. Danese I, Haine V, Delrue R, Lestrate P, Stevaux O, et al. (2004) The Ton system, an ABC transporter, and a universally conserved GTPase are involved in iron utilization by Brucella melitensis 16M. Infect Immun 72: 5783-5790.
23. Jenner DC, Dassa E, Whatmore AM, Atkins HS (2009) ATP-Binding cassette systems of Brucella. Comp Funct Genomics 2009: 354649.
24. Copin R, Vitry M-A, Hanot Mambres D, Machelart A, De Trez C, et al. (2012) In situ microscopy analysis reveals local innate immune response developed around Brucella infected cells in resistant and susceptible mice. PLoS Pathogens 8: e1002575.
25. Alton GG, Jones LM, Angus RD, Verger JM (1988) Techniques for the brucellosis laboratory. Paris: Institut National de la Recherche Agronomique. 190p.
26. Plommet M (1991) Minimal requirements for growth of Brucella suis and other Brucella species. Zentralbl Bakteriol 275: 436-450.
27. Garza E, Finan C, Inverson A, Zhou S (2011) Extension temperature of 60°C required for PCR amplification of large DNA fragments (>5kb) from a low GC bacterium Clostridium acetobutylicum. Wolrd J Microbiol Biotechnol 27: 449-451.
28. Gonzalez P, Zigler Jr JS, Epstein DL, Borrás T (1999) Increasing DNA transfer efficiency by temporary inactivation of host restriction. Biotechniques 26: 892-900.
29. Gibson MM, Price M, Higgins CF (1984) Genetic characterization and molecular cloning of the tripeptide permease (tpp) genes of Salmonella typhimurium. J Bacteriol 160: 122-130.
30. Hiles ID, Gallagher MP, Jamieson DJ, Higgins CF (1987) Molecular characterization of the oligopeptide permease of Salmonella typhimurium. J Mol Biol 195: 125-142.
31. Abouhamad WN, Manson M, Gibson MM, Higgins CF (1991) Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol Microbiol 5: 1035-2047.
32. Andrews JC, Short SA (1985) Genetic analysis of Escherichia coli oligopeptide transport mutants. J Bacteriol 161: 484-492.
33. Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
34. Vieira HGS, Grynberg P, Bitar M, Pires SF, Hilario HO, et al. (2014) Proteomic analysis of Trypanosoma cruzi response to ionizing radiation stress. PloS One 9: e97526.
35. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, et al. (2013) STRING v9.1: proteinprotein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: 808-815.
36. Pizarro-Cerdá J, Méresse S, Parton RG, van der Goot G, Sola-Landa A, et al. (1998) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66: 5711-5724.
37. Kulakov YK, Guigue-Talet PG, Ramuz MR, O'Callaghan D (1997) Response of Brucella suis 1330 and B. canis RM6/66 to growth at acid pH and induction of an adaptive acid tolerance response. Res Microbiol 148: 145-151.
38. de Jong MF, Sun Y-H, den Hartigh AB, van Dijl JM, Tsolis RM (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70: 1378-1396.
39. Arocena GM, Zorreguieta A, Sieira R (2012) Expression of VjbR under nutrient limitation conditions is regulated at the post-transcriptional level by specific acidic pH values and urocanic acid. PLoS ONE 7: e35394.
40. Moreno E, Moriyón I (2006) The genus Brucella. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, eds. Prokaryotes. New York: Springer New York. pp. 315-456.
41. Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J (2008) Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 9: 678-694.
42. Rouot B, Alvarez-Martinez M-T, Marius C, Menanteau P, Guilloteau L, et al. (2003) Production of the Type IV Secretion System differs among Brucella species as revealed with VirB5- and VirB8-specific antisera. Infect Immun 71: 1075-1082.
43. Sieira R, Arocena GM, Bukata L, Comerci DJ, Ugalde RA (2010) Metabolic control of virulence genes in Brucella abortus: HutC coordinates virB expression and the histidine utilization pathway by direct binding to both promoters. J Bacteriol 192: 217-224.
44. Sieira R (2013) Regulation of virulence in Brucella: an eclectic repertoire of transcription factors defines the complex architecture of the virB promoter. Future Microbiol 8: 1193-1208.
45. Jubier-Maurin V, Rodrigue A, Ouahrani-Bettache S, Layssac M, Köhler S, et al. (2001) Identification of the nik gene cluster of Brucella suis: regulation and contribution to urease activity. J Bacteriol 183: 426-434.
46. Sangari FJ, Cayón AM, Seoane A, García-lobo JM (2010) Brucella abortus ure2 contains an acidactivated urea transporter and a nickel transport system. BMC Microbiol 10: 1-12.
47. Naider F, Becker JM (1975) Multiplicity of oligopeptide transport systems in Escherichia coli. J Bacteriol 122: 1208-1215.
48. Martín-Martín AI, Sancho P, Tejedor C, Fernandez-Lago L, Vizcaíno N (2011) Differences in the outer membrane- related properties of the six classical Brucella species. Vet. J. 189: 103-105.
49. Lamontagne J, Béland M, Forest A, Côté -Martin A, Nassif N, et al. (2010) Proteomics-based confirmation of protein expression and correction of annotation errors in the Brucella abortus genome. BMC Genomics 11: 1-10.
50. Cloeckaert A, Vizcaino N, Paquet JY, Bowden RA, Elzer PH (2002). Major outer membrane proteins of Brucella spp.: past, present and future. Vet Microbiol 90: 229-247.
51. Ko J, Splitter GA (2003) Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans. Clin Microbiol Rev 16:65-78.
52. Gee JM, Valderas MW, Kovach ME (2005) The Brucella abortus Cu,Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect Immun 73: 2873-2880.
53. Rossetti CA, Galindo CL, Lawhon SD, Garner HR, Adams LG (2009) Brucella melitensis global gene expression study provides novel information on growth phase-specific gene regulation with potential insights for understanding Brucella: host initial interactions. BMC Microbiol 9: 81.
54. Caro-Hernández P, Fernández-Lago L, de Miguel M-J, Martín-Martín AI, Cloeckaert A, et al. (2007) Role of the Omp25/Omp31 family in outer membrane properties and virulence of Brucella ovis. Infect Immun 75: 4050-4061.
55. Martín-Martín AI, Caro-Hernández P, Orduña A, Vizcaíno N, Fernández-Lago L (2008) Importance of the Omp25/Omp31 family in the internalization and intracellular replication of virulent B. ovis in murine macrophages and HeLa cells. Microbes Infect 10: 706-710.
56. Wang Y, Chen Z, Qiao F, Zhong Z, Xu J, et al. (2010) The type IV secretion system affects the expression of Omp25/Omp31 and the outer membrane properties of Brucella melitensis. FEMS Microbiol Lett 303: 92-100.
57. Wang Y, Chen Z, Qiao F, Ying T, Yuan J, et al. (2009) Comparative proteomics analyses reveal the virB of B. melitensis affects expression of intracellular survival related proteins. PLoS One 4: e5368.
58. Silva APC, Macêdo AA, Costa LF, Turchetti AP, Bull V, et al. (2013) Brucella ovis lacking a speciesspecific putative ATP-binding cassette transporter is attenuated but immunogenic in rams. Vet Microbiol 167: 546-553.
59. Pizarro-Cerdá J, Moreno E, Gorvel JP (2000) Invasion and intracellular trafficking of Brucella abortus in nonphagocytic cells. Microbes Infect 2: 829-835.
60. Celli J (2006) Surviving inside a macrophage: the many ways of Brucella. Res Microbiol 157: 93-98.
61. Starr T, Child R, Wehrly TD, Hansen B, Hwang S, et al. (2012) Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11: 33-45.
62. Rittig MG, Kaufmann A, Robins A, Shaw B, Sprenger H, et al. (2003) Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74: 1045-1055.
63. Covert J, Mathison AJ, Eskra L, Banai M, Splitter G (2010) Brucella melitensis, B. neotomae and B. ovis elicit common and distinctive macrophage defense transcriptional responses. Exp Biol Med 234: 1450-1467.
64. Porte F, Liautard JP, Köhler S (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect Immun 67: 4041-4047.
65. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, et al. (2002) The Brucella suis virB operon is induced intracellularly in macrophages. Proc Natl Acad Sci USA 99: 1544-1549.