Oropharyngeal aspiration of burkholderia mallei and Burkholderia pseudomallei in BALB/c mice

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Schully, Kevin L ^a   Bell, Matthew G ^a   Ward, Jerrold M ^b   Keane Myers, Andrea M ^a  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b Global VetPathology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIAL STRAIN; BAGG ALBINO MOUSE; BURKHOLDERIA MALLEI; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; EXPOSURE; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; INHALATION TEST; LUNG LAVAGE; MELIOIDOSIS; MOUSE; NONHUMAN; OROPHARYNGEAL ASPIRATION; OROPHARYNX; ACUTE DISEASE; ANIMAL; BACTERIAL INFECTION; DISEASE MODEL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; PATHOGENICITY; PATHOLOGY; POST EXPOSURE PROPHYLAXIS; TRANSMISSION;

BURKHOLDERIA MALLEI; BURKHOLDERIA PSEUDOMALLEI; MURINAE; MUS;

ACUTE DISEASE; ANIMALS; BACTERIAL INFECTIONS; BURKHOLDERIA MALLEI; BURKHOLDERIA PSEUDOMALLEI; DISEASE MODELS, ANIMAL; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MICE; MICE, INBRED BALB C; POST-EXPOSURE PROPHYLAXIS;

EID: 84916888241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115066     Document Type: Article

References (78)

1. Whitmore A (1913) An Account of a Glanders-like Disease occurring in Rangoon. J Hyg (Lond) 13: 1-34, 31.
2. Stanton AT, Fletcher W (1921) Melioidosis, a new disease of the tropics. Trans Fourth Congr Far East Assoc Trop Med Hyg. Batavia 2: 196-198.
3. Currie BJ, Dance DA, Cheng AC (2008) The global distribution of Burkholderia pseudomallei and melioidosis: an update. Trans R Soc Trop Med Hyg 102 Suppl 1: S1-4.
4. Chaowagul W, White NJ, Dance DA, Wattanagoon Y, Naigowit P, et al. (1989) Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J Infect Dis 159: 890-899.
5. Boonsawat W, Boonma P, Tangdajahiran T, Paupermpoonsiri S, Wongpratoom W, et al. (1990) Community-acquired pneumonia in adults at Srinagarind Hospital. J Med Assoc Thai 73: 345-352.
6. Currie BJ, Fisher DA, Howard DM, Burrow JN, Selvanayagam S, et al. (2000) The epidemiology of melioidosis in Australia and Papua New Guinea. Acta Trop 74: 121-127.
7. Currie BJ (2003) Melioidosis: an important cause of pneumonia in residents of and travellers returned from endemic regions. Eur Respir J 22: 542-550.
8. Barnes JL, Ketheesan N (2005) Route of infection in melioidosis. Emerg Infect Dis 11: 638-639.
9. Woods DE, DeShazer D, Moore RA, Brett PJ, Burtnick MN, et al. (1999) Current studies on the pathogenesis of melioidosis. Microbes Infect 1: 157-162.
10. Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, et al. (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci U S A 101: 14246-14251.
11. Howe C (1950) Glanders. In: Christian HA editor. The Oxford Medicine: Oxford University Press. pp. 185-202.
12. Benenson AS, editor (1995) Control of Communicable Diseases Mannual.Washington, D.C.: American Public Health Association.
13. Mandell GL, Bennett JA, Dolin R (1995) Pseudomonas species (including melioidosis and glanders) In: Mandell G L BJA, Dolin R, editor. Principles and practice of infectious diseases. 4th ed. New York, N.Y: Churchill Livingstone. pp. 2003-2009.
14. Srinivasan A, Kraus CN, DeShazer D, Becker PM, Dick JD, et al. (2001) Glanders in a military research microbiologist. N Engl J Med 345: 256-258.
15. Waag D, DeShazer D (2005) Glanders. In: Lindler L, Lebeda F, Korch G editors. Biological Weapons Defense: Humana Press. pp. 209-237.
16. National Select Agent Registry (2013) HHS AND USDA Select Agents and Toxins. In: APHIS/CDC, 7 CFR Part 331, 9 CFR Part 121, and 42 CFR Part 73.
17. Yeager JJ, Facemire P, Dabisch PA, Robinson CG, Nyakiti D, et al. (2012) Natural history of inhalation melioidosis in rhesus macaques (Macaca mulatta) and African green monkeys (Chlorocebus aethiops). Infect Immun 80: 3332-3340.
18. Soffler C, Bosco-Lauth AM, Aboellail TA, Marolf AJ, Bowen RA (2012) Development and characterization of a caprine aerosol infection model of melioidosis. PLoS One 7: e43207.
19. Lee YH, Chen Y, Ouyang X, Gan YH (2010) Identification of tomato plant as a novel host model for Burkholderia pseudomallei. BMC Microbiol 10: 28.
20. O'Quinn AL, Wiegand EM, Jeddeloh JA (2001) Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell Microbiol 3: 381-393.
21. Gan YH, Chua KL, Chua HH, Liu B, Hii CS, et al. (2002) Characterization of Burkholderia pseudomallei infection and identification of novel virulence factors using a Caenorhabditis elegans host system. Mol Microbiol 44: 1185-1197.
22. Schell MA, Lipscomb L, DeShazer D (2008) Comparative genomics and an insect model rapidly identify novel virulence genes of Burkholderia mallei. J Bacteriol 190: 2306-2313.
23. Wand ME, Muller CM, Titball RW, Michell SL (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.
24. Fisher NA, Ribot WJ, Applefeld W, DeShazer D (2012) The Madagascar hissing cockroach as a novel surrogate host for Burkholderia pseudomallei, B. mallei and B. thailandensis. BMC Microbiol 12: 117.
25. Liu B, Koo GC, Yap EH, Chua KL, Gan YH (2002) Model of differential susceptibility to mucosal Burkholderia pseudomallei infection. Infect Immun 70: 504-511.
26. Tan GY, Liu Y, Sivalingam SP, Sim SH, Wang D, et al. (2008) Burkholderia pseudomallei aerosol infection results in differential inflammatory responses in BALB/c and C57Bl/6 mice. J Med Microbiol 57: 508-515.
27. Lauw FN, Simpson AJ, Prins JM, Smith MD, Kurimoto M, et al. (1999) Elevated plasma concentrations of interferon (IFN)-gamma and the IFN-gamma-inducing cytokines interleukin (IL)-18, IL-12, and IL-15 in severe melioidosis. J Infect Dis 180: 1878-1885.
28. Simpson AJ, Smith MD, Weverling GJ, Suputtamongkol Y, Angus BJ, et al. (2000) Prognostic value of cytokine concentrations (tumor necrosis factor-alpha, interleukin-6, and interleukin-10) and clinical parameters in severe melioidosis. J Infect Dis 181: 621-625.
29. Warawa JM (2010) Evaluation of surrogate animal models of melioidosis. Front Microbiol 1: 141.
30. Hoppe I, Brenneke B, Rohde M, Kreft A, Haussler S, et al. (1999) Characterization of a murine model of melioidosis: comparison of different strains of mice. Infect Immun 67: 2891-2900.
31. Leakey AK, Ulett GC, Hirst RG (1998) BALB/c and C57Bl/6 mice infected with virulent Burkholderia pseudomallei provide contrasting animal models for the acute and chronic forms of human melioidosis. Microb Pathog 24: 269-275.
32. Ulett GC, Ketheesan N, Hirst RG (2000) Cytokine gene expression in innately susceptible BALB/c mice and relatively resistant C57BL/6 mice during infection with virulent Burkholderia pseudomallei. Infect Immun 68: 2034-2042.
33. Jeddeloh JA, Fritz DL, Waag DM, Hartings JM, Andrews GP (2003) Biodefense-driven murine model of pneumonic melioidosis. Infect Immun 71: 584-587.
34. Conejero L, Patel N, de Reynal M, Oberdorf S, Prior J, et al. (2011) Low-dose exposure of C57BL/6 mice to burkholderia pseudomallei mimics chronic human melioidosis. Am J Pathol 179: 270-280.
35. Lever MS, Nelson M, Ireland PI, Stagg AJ, Beedham RJ, et al. (2003) Experimental aerogenic Burkholderia mallei (glanders) infection in the BALB/c mouse. J Med Microbiol 52: 1109-1115.
36. Fritz DL, Vogel P, Brown DR, Deshazer D, Waag DM (2000) Mouse model of sublethal and lethal intraperitoneal glanders (Burkholderia mallei). Vet Pathol 37: 626-636.
37. West TE, Myers ND, Limmathurotsakul D, Liggitt HD, Chantratita N, et al. (2010) Pathogenicity of high-dose enteral inoculation of Burkholderia pseudomallei to mice. Am J Trop Med Hyg 83: 1066-1069.
38. Team RDC (2011) R: A Language and Environment for Statistical Computing.
39. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, et al. (2010) Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci U S A 107: 5652-5657.
40. Norris HH, Peterson ME, Stebbins CC, McConchie BW, Bundoc VG, et al. (2007) Inhibitory receptor gp49B regulates eosinophil infiltration during allergic inflammation. J Leukoc Biol 82: 1531-1541.
41. Meylan F, Davidson TS, Kahle E, Kinder M, Acharya K, et al. (2008) The TNF-family receptor DR3 is essential for diverse T cell-mediated inflammatory diseases. Immunity 29: 79-89.
42. McConchie BW, Norris HH, Bundoc VG, Trivedi S, Boesen A, et al. (2006) Ascaris suum-derived products suppress mucosal allergic inflammation in an interleukin-10-independent manner via interference with dendritic cell function. Infect Immun 74: 6632-6641.
43. Schully KL, Sharma S, Peine KJ, Pesce J, Elberson MA, et al. (2013) Rapid Vaccination Using an Acetalated Dextran Microparticulate Subunit Vaccine Confers Protection Against Triplicate Challenge by Bacillus Anthracis. Pharm Res.
44. Albrecht MT, Livingston BD, Pesce JT, Bell MG, Hannaman D, et al. (2012) Electroporation of a multivalent DNA vaccine cocktail elicits a protective immune response against anthrax and plague. Vaccine 30: 4872-4883.
45. Sarkar-Tyson M, Smither SJ, Harding SV, Atkins TP, Titball RW (2009) Protective efficacy of heat-inactivated B. thailandensis, B. mallei or B. pseudomallei against experimental melioidosis and glanders. Vaccine 27: 4447-4451.
46. Titball RW, Russell P, Cuccui J, Easton A, Haque A, et al. (2008) Burkholderia pseudomallei: animal models of infection. Trans R Soc Trop Med Hyg 102 Suppl 1: S111-116.
47. Massey S, Yeager LA, Blumentritt CA, Vijayakumar S, Sbrana E, et al. (2014) Comparative Burkholderia pseudomallei natural history virulence studies using an aerosol murine model of infection. Sci Rep 4: 4305.
48. Lafontaine ER, Zimmerman SM, Shaffer TL, Michel F, Gao X, et al. (2013) Use of a safe, reproducible, and rapid aerosol delivery method to study infection by Burkholderia pseudomallei and Burkholderia mallei in mice. PLoS One 8: e76804.
49. Revelli DA, Boylan JA, Gherardini FC (2012) A non-invasive intratracheal inoculation method for the study of pulmonary melioidosis. Front Cell Infect Microbiol 2: 164.
50. Gauthier YP, Hagen RM, Brochier GS, Neubauer H, Splettstoesser WD, et al. (2001) Study on the pathophysiology of experimental Burkholderia pseudomallei infection in mice. FEMS Immunol Med Microbiol 30: 53-63.
51. Ordway D, Henao-Tamayo M, Orme IM, Gonzalez-Juarrero M (2005) Foamy macrophages within lung granulomas of mice infected with Mycobacterium tuberculosis express molecules characteristic of dendritic cells and antiapoptotic markers of the TNF receptor-associated factor family. J Immunol 175: 3873-3881.
52. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, et al. (2011) Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186: 1666-1674.
53. Shevchenko MA, Bolkhovitina EL, Servuli EA, Sapozhnikov AM (2013) Elimination of Aspergillus fumigatus conidia from the airways of mice with allergic airway inflammation. Respir Res 14: 78.
54. Pratt TS, Pincus SH, Hale ML, Moreira AL, Roy CJ, et al. (2007) Oropharyngeal aspiration of ricin as a lung challenge model for evaluation of the therapeutic index of antibodies against ricin A-chain for post-exposure treatment. Exp Lung Res 33: 459-481.
55. Egger C, Cannet C, Gerard C, Jarman E, Jarai G, et al. (2013) Administration of bleomycin via the oropharyngeal aspiration route leads to sustained lung fibrosis in mice and rats as quantified by UTE-MRI and histology. PLoS One 8: e63432.
56. De Vooght V, Vanoirbeek JA, Haenen S, Verbeken E, Nemery B, et al. (2009) Oropharyngeal aspiration: an alternative route for challenging in a mouse model of chemical-induced asthma. Toxicology 259: 84-89.
57. Keane-Myers AM, Gause WC, Finkelman FD, Xhou XD, Wills-Karp M (1998) Development of murine allergic asthma is dependent upon B7-2 costimulation. J Immunol 160: 1036-1043.
58. Voynow JA, Fischer BM, Malarkey DE, Burch LH, Wong T, et al. (2004) Neutrophil elastase induces mucus cell metaplasia in mouse lung. Am J Physiol Lung Cell Mol Physiol 287: L1293-1302.
59. Rao GVS, Tinkle S, Weissman DN, Antonini JM, Kashon ML, et al. (2003) Efficacy of a technique for exposing the mouse lung to particles aspirated from the pharynx. Journal of Toxicology and Environmental Health-Part A 66: 1441-1452.
60. Foster WM, Walters DM, Longphre M, Macri K, Miller LM (2001) Methodology for the measurement of mucociliary function in the mouse by scintigraphy. J Appl Physiol (1985) 90: 1111-1117.
61. West TE, Myers ND, Liggitt HD, Skerrett SJ (2012) Murine pulmonary infection and inflammation induced by inhalation of Burkholderia pseudomallei. Int J Exp Pathol 93: 421-428.
62. Santanirand P, Harley VS, Dance DA, Drasar BS, Bancroft GJ (1999) Obligatory role of gamma interferon for host survival in a murine model of infection with Burkholderia pseudomallei. Infect Immun 67: 3593-3600.
63. Easton A, Haque A, Chu K, Lukaszewski R, Bancroft GJ (2007) A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J Infect Dis 195: 99-107.
64. Silva EB, Dow SW (2013) Development of Burkholderia mallei and pseudomallei vaccines. Front Cell Infect Microbiol 3: 10.
65. Miyagi K, Kawakami K, Saito A (1997) Role of reactive nitrogen and oxygen intermediates in gamma interferon-stimulated murine macrophage bactericidal activity against Burkholderia pseudomallei. Infect Immun 65: 4108-4113.
66. Utaisincharoen P, Tangthawornchaikul N, Kespichayawattana W, Chaisuriya P, Sirisinha S (2001) Burkholderia pseudomallei interferes with inducible nitric oxide synthase (iNOS) production: a possible mechanism of evading macrophage killing. Microbiol Immunol 45: 307-313.
67. Utaisincharoen P, Anuntagool N, Arjcharoen S, Limposuwan K, Chaisuriya P, et al. (2004) Induction of iNOS expression and antimicrobial activity by interferon (IFN)-beta is distinct from IFN-gamma in Burkholderia pseudomallei-infected mouse macrophages. Clin Exp Immunol 136: 277-283.
68. Shields AM, Panayi GS, Corrigall VM (2011) Resolution-associated molecular patterns (RAMP): RAMParts defending immunological homeostasis? Clin Exp Immunol 165: 292-300.
69. Bogdan C, Vodovotz Y, Nathan C (1991) Macrophage deactivation by interleukin 10. J Exp Med 174: 1549-1555.
70. Shields AM, Thompson SJ, Panayi GS, Corrigall VM (2012) Pro-resolution immunological networks: binding immunoglobulin protein and other resolution-associated molecular patterns. Rheumatology (Oxford) 51: 780-788.
71. Strieter RM, Belperio JA, Keane MP (2002) Cytokines in innate host defense in the lung. J Clin Invest 109: 699-705.
72. Ceballos-Olvera I, Sahoo M, Miller MA, Del Barrio L, Re F (2011) Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1beta is deleterious. PLoS Pathog 7: e1002452.
73. Cheng AC, Obrien M, Jacups SP, Anstey NM, Currie BJ (2004) C-reactive protein in the diagnosis of melioidosis. Am J Trop Med Hyg 70: 580-582.
74. Ashdown LR (1992) Serial serum C-reactive protein levels as an aid to the management of melioidosis. Am J Trop Med Hyg 46: 151-157.
75. Cheng AC, Currie BJ (2007) Serum C-reactive protein and liver disease in patients with melioidosis. Intensive Care Med 33: 562; author reply 563-564.
76. Spittler A, Razenberger M, Kupper H, Kaul M, Hackl W, et al. (2000) Relationship between interleukin-6 plasma concentration in patients with sepsis, monocyte phenotype, monocyte phagocytic properties, and cytokine production. Clin Infect Dis 31: 1338-1342.
77. Koo GC, Gan YH (2006) The innate interferon gamma response of BALB/c and C57BL/6 mice to in vitro Burkholderia pseudomallei infection. BMC Immunol 7: 19.
78. Rowland CA, Lertmemongkolchai G, Bancroft A, Haque A, Lever MS, et al. (2006) Critical role of type 1 cytokines in controlling initial infection with Burkholderia mallei. Infect Immun 74: 5333-5340.