1887

Journal of Medical Microbiology logo

Volume 62, Issue 2

survival and trafficking within macrophages Free

Abstract

Cystic fibrosis (CF) patients are at great risk of opportunistic lung infection, particularly by members of the complex (Bcc). This group of bacteria can cause damage to the lung tissue of infected patients and are difficult to eradicate due to their high levels of antibiotic resistance. Although the highly virulent has been the focus of virulence research for the past decade, is emerging as the most prevalent Bcc species infecting CF patients in North America. Despite several studies detailing the intramacrophage trafficking and survival of , no such data exist for . The results of this study demonstrated that the clinical CF isolates C5568 and C0514 and an environmental isolate, ATCC 17616, were able to replicate and survive within murine macrophages in a manner similar to that of strain K56-2. These strains were also able to survive but were unable to replicate within human THP-1 macrophages. Differences in macrophage uptake were observed among all three strains; these variances were attributed to major differences in O-antigen production. Unlike containing vacuoles, which delay phagosomal maturation in murine macrophages by 6 h, all -containing vacuoles co-localized with lysosome-associated membrane protein-1, a late endosome/lysosomal marker, and the lysosomal marker dextran within 2 h of uptake. Together, these results indicated that, whilst both Bcc species were able to survive and replicate within macrophages, they utilized different intramacrophage survival strategies. To observe differences in virulence, the strains were compared using the (wax worm) model. When compared with the strains tested, K56-2 was highly virulent in this model and killed all worms within 24 h when injected at 10 c.f.u. clinical isolates C5568 and C0514 were significantly more virulent than the soil isolate ATCC 17616, which was avirulent even when worms were injected with 10 c.f.u. These results suggest strain differences in the virulence of isolates.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.051243-0
2013-02-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/2/173.html?itemId=/content/journal/jmm/10.1099/jmm.0.051243-0&mimeType=html&fmt=ahah

References

  1. Aaron S. D., Ferris W., Henry D. A., Speert D. P., Macdonald N. E. 2000; Multiple combination bactericidal antibiotic testing for patients with cystic fibrosis infected with Burkholderia cepacia . Am J Respir Crit Care Med 161:1206–1212[PubMed] [CrossRef]
     [Google Scholar]
  2. Abrami L., Fivaz M., Glauser P. E., Parton R. G., van der Goot F. G. 1998; A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J Cell Biol 140:525–540 [View Article][PubMed]
     [Google Scholar]
  3. Al-Younes H. M., Rudel T., Meyer T. F. 1999; Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell Microbiol 1:237–247 [View Article][PubMed]
     [Google Scholar]
  4. Andrade G., Mihara K. L., Linderman R. G., Bethlenfalvay G. J. 1997; Bacteria from the rhizoshpere and hyphosphere soils of different arbuscular–mycorrhizal fungi. Plant Soil 192:71–79 [View Article]
     [Google Scholar]
  5. Aperis G., Fuchs B. B., Anderson C. A., Warner J. E., Calderwood S. B., Mylonakis E. 2007; Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain. Microbes Infect 9:729–734 [View Article][PubMed]
     [Google Scholar]
  6. Arjcharoen S., Wikraiphat C., Pudla M., Limposuwan K., Woods D. E., Sirisinha S., Utaisincharoen P. 2007; Fate of a Burkholderia pseudomallei lipopolysaccharide mutant in the mouse macrophage cell line RAW 264.7: possible role for the O-antigenic polysaccharide moiety of lipopolysaccharide in internalization and intracellular survival. Infect Immun 75:4298–4304 [View Article][PubMed]
     [Google Scholar]
  7. Azegami K., Nishiyama K., Watanabe Y., Kadota I., Ohuchi A., Fukazawa C. 1987; Pseudomonas plantarii sp. nov., the causal agent of rice seedling blight. Int J Syst Bacteriol 37:144–152 [View Article]
     [Google Scholar]
  8. Boucher R. C. 2007; Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 13:231–240 [View Article][PubMed]
     [Google Scholar]
  9. Bumford A. A., Spilker T., LiPuma J. 2010; Epidemiology of Burkholderia infection in U.S. CF Patients . International Burkholderia cepacia Working Group, Seattle, WA, USA
    [Google Scholar]
  10. Burkholder W. H. 1950; Sour skin, a bacterial rot of onion bulbs. Phytopathology 40:115–117
     [Google Scholar]
  11. Cardona S. T., Wopperer J., Eberl L., Valvano M. A. 2005; Diverse pathogenicity of Burkholderia cepacia complex strains in the Caenorhabditis elegans host model. FEMS Microbiol Lett 250:97–104 [View Article][PubMed]
     [Google Scholar]
  12. Carvalho A. P. D., Ventura G. M. C., Pereira C. B., Leão R. S., Folescu T. W., Higa L., Teixeira L. M., Plotkowski M. C. M., Merquior V. L. C. other authors 2007; Burkholderia cenocepacia, B. multivorans, B. ambifaria and B. vietnamiensis isolates from cystic fibrosis patients have different profiles of exoenzyme production. APMIS 115:311–318 [View Article][PubMed]
     [Google Scholar]
  13. Chu K. K., Davidson D. J., Halsey T. K., Chung J. W., Speert D. P. 2002; Differential persistence among genomovars of the Burkholderia cepacia complex in a murine model of pulmonary infection. Infect Immun 70:2715–2720 [View Article][PubMed]
     [Google Scholar]
  14. Chu K. K., MacDonald K. L., Davidson D. J., Speert D. P. 2004; Persistence of Burkholderia multivorans within the pulmonary macrophage in the murine lung. Infect Immun 72:6142–6147 [View Article][PubMed]
     [Google Scholar]
  15. Coenye T., Vandamme P. 2003; Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729 [View Article][PubMed]
     [Google Scholar]
  16. Compant S., Nowak J., Coenye T., Clément C., Ait Barka E. 2008; Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626 [View Article][PubMed]
     [Google Scholar]
  17. Craig F. F., Coote J. G., Parton R., Freer J. H., Gilmour N. J. 1989; A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J Gen Microbiol 135:2885–2890[PubMed]
     [Google Scholar]
  18. Duff C., Murphy P. G., Callaghan M., McClean S. 2006; Differences in invasion and translocation of Burkholderia cepacia complex species in polarised lung epithelial cells in vitro . Microb Pathog 41:183–192 [View Article][PubMed]
     [Google Scholar]
  19. Eissenberg L. G., Schlesinger P. H., Goldman W. E. 1988; Phagosome–lysosome fusion in P388D1 macrophages infected with Histoplasma capsulatum . J Leukoc Biol 43:483–491[PubMed]
     [Google Scholar]
  20. Fehlner-Gardiner C. C., Hopkins T. M. H., Valvano M. A. 2002; Identification of a general secretory pathway in a human isolate of Burkholderia vietnamiensis (formerly B. cepacia complex genomovar V) that is required for the secretion of hemolysin and phospholipase C activities. Microb Pathog 32:249–254 [View Article][PubMed]
     [Google Scholar]
  21. Fernandez-Prada C. M., Zelazowska E. B., Nikolich M., Hadfield T. L., Roop R. M. II, Robertson G. L., Hoover D. L. 2003; Interactions between Brucella melitensis and human phagocytes: bacterial surface O-polysaccharide inhibits phagocytosis, bacterial killing, and subsequent host cell apoptosis. Infect Immun 71:2110–2119 [View Article][PubMed]
     [Google Scholar]
  22. Figueroa-Arredondo P., Heuser J. E., Akopyants N. S., Morisaki J. H., Giono-Cerezo S., Enríquez-Rincón F., Berg D. E. 2001; Cell vacuolation caused by Vibrio cholerae hemolysin. Infect Immun 69:1613–1624 [View Article][PubMed]
     [Google Scholar]
  23. Figurski D. H., Helinski D. R. 1979; Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans . Proc Natl Acad Sci U S A 76:1648–1652 [View Article][PubMed]
     [Google Scholar]
  24. Flannagan R. S., Linn T., Valvano M. A. 2008; A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. . Environ Microbiol 10:1652–1660 [View Article][PubMed]
     [Google Scholar]
  25. Garbaye J., Bowen G. D. 1989; Stimulation of ectomycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388 [View Article]
     [Google Scholar]
  26. Gavrilin M. A., Abdelaziz D. H. A., Mostafa M., Abdulrahman B. A., Grandhi J., Akhter A., Abu Khweek A., Aubert D. F., Valvano M. A. other authors 2012; Activation of the pyrin inflammasome by intracellular Burkholderia cenocepacia . J Immunol 188:3469–3477 [View Article][PubMed]
     [Google Scholar]
  27. Govan J. R. W., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev 60:539–574[PubMed]
     [Google Scholar]
  28. Govan J. R., Brown A. R., Jones A. M. 2007; Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2:153–164 [View Article][PubMed]
     [Google Scholar]
  29. Hamad M. A., Skeldon A. M., Valvano M. A. 2010; Construction of aminoglycoside-sensitive Burkholderia cenocepacia strains for use in studies of intracellular bacteria with the gentamicin protection assay. Appl Environ Microbiol 76:3170–3176 [View Article][PubMed]
     [Google Scholar]
  30. Hendrickson E. L., Plotnikova J., Mahajan-Miklos S., Rahme L. G., Ausubel F. M. 2001; Differential roles of the Pseudomonas aeruginosa PA14 rpoN gene in pathogenicity in plants, nematodes, insects, and mice. J Bacteriol 183:7126–7134 [View Article][PubMed]
     [Google Scholar]
  31. Hewlett L. J., Prescott A. R., Watts C. 1994; The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 124:689–703 [View Article][PubMed]
     [Google Scholar]
  32. Hmama Z., Sendide K., Talal A., Garcia R., Dobos K., Reiner N. E. 2004; Quantitative analysis of phagolysosome fusion in intact cells: inhibition by mycobacterial lipoarabinomannan and rescue by an 1α,25-dihydroxyvitamin D3-phosphoinositide 3-kinase pathway. J Cell Sci 117:2131–2140 [View Article][PubMed]
     [Google Scholar]
  33. Hoffmann J. A. 1995; Innate immunity of insects. Curr Opin Immunol 7:4–10 [View Article][PubMed]
     [Google Scholar]
  34. Howe D., Shannon J. G., Winfree S., Dorward D. W., Heinzen R. A. 2010; Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect Immun 78:3465–3474 [View Article][PubMed]
     [Google Scholar]
  35. Huynh K. K., Plumb J. D., Downey G. P., Valvano M. A., Grinstein S. 2010; Inactivation of macrophage Rab7 by Burkholderia cenocepacia . J Innate Immun 2:522–533 [View Article][PubMed]
     [Google Scholar]
  36. Izumi H., Moore E. R. B., Killham K., Alexander I. J., Anderson I. C. 2007; Characterisation of endobacterial communities in ectomycorrhizas by DNA- and RNA-based molecular methods. Soil Biol Biochem 39:891–899 [View Article]
     [Google Scholar]
  37. Jander G., Rahme L. G., Ausubel F. M. 2000; Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182:3843–3845 [View Article][PubMed]
     [Google Scholar]
  38. Jeong Y., Kim J., Kim S., Kang Y., Nagamatsu T., Hwang I. 2003; Toxoflavin produced by Burkholderia glumae causing rice grain rot is responsible for inducing bacterial wilt in many field crops. Plant Dis 87:890–895 [View Article]
     [Google Scholar]
  39. Jones A. M., Dodd M. E., Govan J. R., Barcus V., Doherty C. J., Morris J., Webb A. K. 2004; Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 59:948–951 [View Article][PubMed]
     [Google Scholar]
  40. Kavanagh K., Reeves E. P. 2004; Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev 28:101–112 [View Article][PubMed]
     [Google Scholar]
  41. Kikuchi Y., Meng X. Y., Fukatsu T. 2005; Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol 71:4035–4043 [View Article][PubMed]
     [Google Scholar]
  42. Lamothe J., Valvano M. A. 2008; Burkholderia cenocepacia-induced delay of acidification and phagolysosomal fusion in cystic fibrosis transmembrane conductance regulator (CFTR)-defective macrophages. Microbiology 154:3825–3834 [View Article][PubMed]
     [Google Scholar]
  43. Lamothe J., Thyssen S., Valvano M. A. 2004; Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga . Cell Microbiol 6:1127–1138 [View Article][PubMed]
     [Google Scholar]
  44. Lamothe J., Huynh K. K., Grinstein S., Valvano M. A. 2007; Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol 9:40–53 [View Article][PubMed]
     [Google Scholar]
  45. Landers P., Kerr K. G., Rowbotham T. J., Tipper J. L., Keig P. M., Ingham E., Denton M. 2000; Survival and growth of Burkholderia cepacia within the free-living amoeba Acanthamoeba polyphaga . Eur J Clin Microbiol Infect Dis 19:121–123 [View Article][PubMed]
     [Google Scholar]
  46. Lesse A. J., Campagnari A. A., Bittner W. E., Apicella M. A. 1990; Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J Immunol Methods 126:109–117 [View Article][PubMed]
     [Google Scholar]
  47. Lessie T. G., Gaffney T. 1986; Catabolic potential of Pseudomonas cepacia . In The Bacteria: a Treatise on Structure and Function vol 10 The Biology of Pseudomonads pp. 439–481 Edited by Ornston L. N., Sokatch J. R. Orlando, FL: Academic Press;
     [Google Scholar]
  48. MacDonald K. L., Speert D. P. 2008; Differential modulation of innate immune cell functions by the Burkholderia cepacia complex: Burkholderia cenocepacia but not Burkholderia multivorans disrupts maturation and induces necrosis in human dendritic cells. Cell Microbiol 10:2138–2149 [View Article][PubMed]
     [Google Scholar]
  49. Mahenthiralingam E., Vandamme P. 2005; Taxonomy and pathogenesis of the Burkholderia cepacia complex. Chron Respir Dis 2:209–217 [View Article][PubMed]
     [Google Scholar]
  50. Mahenthiralingam E., Vandamme P., Campbell M. E., Henry D. A., Gravelle A. M., Wong L. T., Davidson A. G., Wilcox P. G., Nakielna B., Speert D. P. 2001; Infection with Burkholderia cepacia complex genomovars in patients with cystic fibrosis: virulent transmissible strains of genomovar III can replace Burkholderia multivorans . Clin Infect Dis 33:1469–1475 [View Article][PubMed]
     [Google Scholar]
  51. Maier T. M., Casey M. S., Becker R. H., Dorsey C. W., Glass E. M., Maltsev N., Zahrt T. C., Frank D. W. 2007; Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 75:5376–5389 [View Article][PubMed]
     [Google Scholar]
  52. Manno G., Dalmastri C., Tabacchioni S., Vandamme P., Lorini R., Minicucci L., Romano L., Giannattasio A., Chiarini L., Bevivino A. 2004; Epidemiology and clinical course of Burkholderia cepacia complex infections, particularly those caused by different Burkholderia cenocepacia strains, among patients attending an Italian cystic fibrosis center. J Clin Microbiol 42:1491–1497 [View Article][PubMed]
     [Google Scholar]
  53. Marolda C. L., Welsh J., Dafoe L., Valvano M. A. 1990; Genetic analysis of the O7-polysaccharide biosynthesis region from the Escherichia coli O7 : K1 strain VW187. J Bacteriol 172:3590–3599[PubMed]
     [Google Scholar]
  54. Marolda C. L., Hauröder B., John M. A., Michel R., Valvano M. A. 1999; Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145:1509–1517 [View Article][PubMed]
     [Google Scholar]
  55. Miyata S., Casey M., Frank D. W., Ausubel F. M., Drenkard E. 2003; Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71:2404–2413 [View Article][PubMed]
     [Google Scholar]
  56. Moura J. A., Cristina de Assis M., Ventura G. C., Saliba A. M., Gonzaga L. Jr, Si-Tahar M., Marques E. A., Plotkowski M. C. 2008; Differential interaction of bacterial species from the Burkholderia cepacia complex with human airway epithelial cells. Microbes Infect 10:52–59 [View Article][PubMed]
     [Google Scholar]
  57. Nzula S., Vandamme P., Govan J. R. W. 2002; Influence of taxonomic status on the in vitro antimicrobial susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 50:265–269 [View Article][PubMed]
     [Google Scholar]
  58. Papini E., de Bernard M., Milia E., Bugnoli M., Zerial M., Rappuoli R., Montecucco C. 1994; Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Natl Acad Sci U S A 91:9720–9724 [View Article][PubMed]
     [Google Scholar]
  59. Porte F., Naroeni A., Ouahrani-Bettache S., Liautard J. P. 2003; Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome–lysosome fusion in murine macrophages. Infect Immun 71:1481–1490 [View Article][PubMed]
     [Google Scholar]
  60. Rabinowitz S., Horstmann H., Gordon S., Griffiths G. 1992; Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J Cell Biol 116:95–112 [View Article][PubMed]
     [Google Scholar]
  61. Racoosin E. L., Swanson J. A. 1993; Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 121:1011–1020 [View Article][PubMed]
     [Google Scholar]
  62. Raetz C. R. H., Whitfield C. 2002; Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700 [View Article][PubMed]
     [Google Scholar]
  63. Rajashekara G., Covert J., Petersen E., Eskra L., Splitter G. 2008; Genomic island 2 of Brucella melitensis is a major virulence determinant: functional analyses of genomic islands. J Bacteriol 190:6243–6252 [View Article][PubMed]
     [Google Scholar]
  64. Ramette A., LiPuma J. J., Tiedje J. M. 2005; Species abundance and diversity of Burkholderia cepacia complex in the environment. Appl Environ Microbiol 71:1193–1201 [View Article][PubMed]
     [Google Scholar]
  65. Riordan J. R., Rommens J. M., Kerem B. S., Alon N., Rozmahel R., Grzelczak Z., Zielenski J., Lok S., Plavsic N. other authors 1989; Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066–1073 [View Article][PubMed]
     [Google Scholar]
  66. Saldías M. S., Ortega X., Valvano M. A. 2009; Burkholderia cenocepacia O antigen lipopolysaccharide prevents phagocytosis by macrophages and adhesion to epithelial cells. J Med Microbiol 58:1542–1548 [View Article][PubMed]
     [Google Scholar]
  67. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  68. Santos A. V., Dillon R. J., Dillon V. M., Reynolds S. E., Samuels R. I. 2004; Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa . FEMS Microbiol Lett 239:319–323 [View Article][PubMed]
     [Google Scholar]
  69. Satin B., Norais N., Telford J., Rappuoli R., Murgia M., Montecucco C., Papini E. 1997; Effect of Helicobacter pylori vacuolating toxin on maturation and extracellular release of procathepsin D and on epidermal growth factor degradation. J Biol Chem 272:25022–25028 [View Article][PubMed]
     [Google Scholar]
  70. Schägger H., von Jagow G. 1987; Tricine–sodium dodecyl sulphate–polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [View Article][PubMed]
     [Google Scholar]
  71. Schell M. A., Lipscomb L., DeShazer D. 2008; Comparative genomics and an insect model rapidly identify novel virulence genes of Burkholderia mallei . J Bacteriol 190:2306–2313 [View Article][PubMed]
     [Google Scholar]
  72. Schmerk C. L., Bernards M. A., Valvano M. A. 2011; Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia . J Bacteriol 193:6712–6723 [View Article][PubMed]
     [Google Scholar]
  73. Scott C. C., Botelho R. J., Grinstein S. 2003; Phagosome maturation: a few bugs in the system. J Membr Biol 193:137–152 [View Article][PubMed]
     [Google Scholar]
  74. Seed K. D., Dennis J. J. 2008; Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76:1267–1275 [View Article][PubMed]
     [Google Scholar]
  75. Seed K. D., Dennis J. J. 2009; Experimental bacteriophage therapy increases survival of Galleria mellonella larvae infected with clinically relevant strains of the Burkholderia cepacia complex. Antimicrob Agents Chemother 53:2205–2208 [View Article][PubMed]
     [Google Scholar]
  76. Strasser J. E., Newman S. L., Ciraolo G. M., Morris R. E., Howell M. L., Dean G. E. 1999; Regulation of the macrophage vacuolar ATPase and phagosome–lysosome fusion by Histoplasma capsulatum . J Immunol 162:6148–6154[PubMed]
     [Google Scholar]
  77. Tolman J. S., Valvano M. A. 2012; Global changes in gene expression by the opportunistic pathogen Burkholderia cenocepacia in response to internalization by murine macrophages. BMC Genomics 13:63 [View Article][PubMed]
     [Google Scholar]
  78. Vergunst A. C., Meijer A. H., Renshaw S. A., O’Callaghan D. 2010; Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect Immun 78:1495–1508 [View Article][PubMed]
     [Google Scholar]
  79. Via L. E., Fratti R. A., McFalone M., Pagan-Ramos E., Deretic D., Deretic V. 1998; Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111:897–905[PubMed]
     [Google Scholar]
  80. Wand M. E., Müller C. M., Titball R. W., Michell S. L. 2011; Macrophage and Galleria mellonella infection models reflect the virulence of naturally occurring isolates of B. pseudomallei, B. thailandensis and B. oklahomensis . BMC Microbiol 11:11 [View Article][PubMed]
     [Google Scholar]
  81. Whitlock G. C., Estes D. M., Torres A. G. 2007; Glanders: off to the races with Burkholderia mallei . FEMS Microbiol Lett 277:115–122 [View Article][PubMed]
     [Google Scholar]
  82. Zelazny A. M., Ding L., Elloumi H. Z., Brinster L. R., Benedetti F., Czapiga M., Ulrich R. L., Ballentine S. J., Goldberg J. B. other authors 2009; Virulence and cellular interactions of Burkholderia multivorans in chronic granulomatous disease. Infect Immun 77:4337–4344 [View Article][PubMed]
     [Google Scholar]
  83. Zheng P. Y., Jones N. L. 2003; Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell Microbiol 5:25–40 [View Article][PubMed]
     [Google Scholar]
  84. Zloznik J. E., Henry D. A., Speert D. P. 2011; Burkholderia cepacia complex infections in Vancouver and British Columbia from 1981 to 2010. In: 15th Meeting of the International Burkholderia cepacia Working Group, 13–16 April, Prague, Czech Republic, Abstract A1
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.051243-0
Loading
Burkholderia multivorans survival and trafficking within macrophages
J. Med. Microbiol. 62, 173 (2013); https://doi.org/10.1099/jmm.0.051243-0
/content/journal/jmm/10.1099/jmm.0.051243-0
/content/journal/jmm/10.1099/jmm.0.051243-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error