Comparison of the early host immune response to two widely diverse virulent strains of Burkholderia pseudomallei that cause acute or chronic infections in BALB/c mice

Microbial Pathogenesis

Volumn 86, Issue , 2015, Pages 53-63

  Amemiya, Kei ^a   Dankmeyer, Jennifer L ^a   Fetterer, David P ^a   Worsham, Patricia L ^a   Welkos, Susan L ^a   Cote, Christopher K ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

Acute infection; Burkholderia pseudomallei; Chronic infection; Immune response; Melioidosis

Indexed keywords

CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BURKHOLDERIA PSEUDOMALLEI; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GRANULOCYTE; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MELIOIDOSIS; MONOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SPLEEN CELL; SURVIVAL RATE; ANIMAL; AUSTRALIA; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; CHRONIC DISEASE; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; MICROBIOLOGY; MONONUCLEAR CELL; PATHOLOGY; SERUM; SOUTHEAST ASIA; SPLEEN; VIRULENCE; YOUNG ADULT;

BACTERIA (MICROORGANISMS); BURKHOLDERIA PSEUDOMALLEI; MUS;

ANIMALS; ASIA, SOUTHEASTERN; AUSTRALIA; BACTERIAL LOAD; BURKHOLDERIA PSEUDOMALLEI; CHRONIC DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; MELIOIDOSIS; MICE, INBRED BALB C; SERUM; SPLEEN; VIRULENCE; YOUNG ADULT;

EID: 84938066888     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2015.07.004     Document Type: Article

References (65)

1. Allwood E.M., Devenish R.J., Prescott M., Adler B., Boyce J.D. Strategies for intracellular survival of Burkholderia pseudomallei. Front. Microbiol. 2011, 2:170.
2. Vietri N.J., DeShazer D. Melioidosis. Textbook of Military Medicine: Medical Aspect of Biological Warfare 2007, 147-166. Borden Institute Walter Reed Army Medical Center, Washington, D.C. Z. Dembek (Ed.).
3. Wiersinga W.J., Currie B.J., Peacock S.J. Melioidosis. N.Engl. J. Med. 2012, 367:1035-1044.
4. Cheng A.C., Currie B.J. Melioidosis: epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 2005, 18:383-416.
5. Dance D.A. Melioidosis: the tip of the iceberg?. Clin. Microbiol. Rev. 1991, 4:52-60.
6. Dance D.A. Melioidosis as an emerging global problem. Acta Trop. 2000, 74:115-119.
7. Lo T.J., Ang L.W., James L., Goh K.T. Melioidosis in a tropical city state, Singapore. Emerg. Infect. Dis. 2009, 15:1645-1647.
8. Rammaert B., Beaute J., Borand L., Hem S., Buchy P., et al. Pulmonary melioidosis in Cambodia: a prospective study. BMC Infect. Dis. 2011, 11:126.
9. Yabuuchi E., Arakawa M. Burkholderia pseudomallei and melioidosis: be aware in temperate area. Microbiol. Immunol. 1993, 37:823-836.
10. O'Sullivan B.P., Torres B., Conidi G., Smole S., Gauthier C., et al. Burkholderia pseudomallei infection in a child with cystic fibrosis: acquisition in the western hemisphere. Chest 2011, 140:239-242.
11. Aardema H., Luijnenburg E.M., Salm E.F., Bijlmer H.A., Visser C.E., et al. Changing epidemiology of melioidosis? A case of acute pulmonary melioidosis with fatal outcome imported from Brazil. Epidemiol. Infect. 2005, 133:871-875.
12. Doker T.J., Sharp T.M., Rivera-Garcia B., Perez-Padilla J., Benoit T.J., et al. Contact investigation of melioidosis cases reveals regional endemicity in Puerto Rico. Clin. Infect. Dis. 2015, 60:243-250.
13. Gee J.E., Allender C.J., Tuanyok A., Elrod M.G., Hoffmaster A.R. Burkholderia pseudomallei type G in western hemisphere. Emerg. Infect. Dis. 2014, 20:682-684.
14. Currie B.J., Jacups S.P. Intensity of rainfall and severity of melioidosis, Australia. Emerg. Infect. Dis. 2003, 9:1538-1542.
15. Hassan M.R., Pani S.P., Peng N.P., Voralu K., Vijayalakshmi N., et al. Incidence, risk factors and clinical epidemiology of melioidosis: a complex socio-ecological emerging infectious disease in the Alor Setar region of Kedah, Malaysia. BMC Infect. Dis. 2010, 10:302.
16. Currie B.J., Fisher D.A., Anstey N.M., Jacups S.P. Melioidosis: acute and chronic disease, relapse and re-activation. Trans. R. Soc. Trop. Med. Hyg. 2000, 94:301-304.
17. Kronmann K.C., Truett A.A., Hale B.R., Crum-Cianflone N.F. Melioidosis after brief exposure: a serologic survey in US Marines. Am. J. Trop. Med. Hyg. 2009, 80:182-184.
18. Ngauy V., Lemeshev Y., Sadkowski L., Crawford G. Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during World War II. J.Clin. Microbiol. 2005, 43:970-972.
19. Zhang B., Wear D.J., Kim H.S., Weina P., Stojadinovic A., et al. Development of hydrolysis probe-based real-time PCR for identification of virulent gene targets of Burkholderia pseudomallei and B.mallei - a retrospective study on archival cases of service members with melioidosis and glanders. Mil. Med. 2012, 177:216-221.
20. Dance D. Treatment and prophylaxis of melioidosis. Int. J. Antimicrob. Agents 2014, 43:310-318.
21. Challacombe J.F., Stubben C.J., Klimko C.P., Welkos S.L., Kern S.J., et al. Interrogation of the Burkholderia pseudomallei genome to address differential virulence among isolates. PLoS One 2014, 9:e115951.
22. Welkos S.L., Klimko C.P., Kern S.J., Bearss J.J., Bozue J., et al. Characterization of Burkholderia pseudomallei strains using a murine intraperitoneal infection model and invitro macrophage assays. PLoS One 2015, 10:e0124667.
23. Amemiya K., Meyers J.L., Trevino S.R., Chanh T.C., Norris S.L., et al. Interleukin-12 induces a Th1-like response to Burkholderia mallei and limited protection in BALB/c mice. Vaccine 2006, 24:1413-1420.
24. Nandi T., Ong C., Singh A.P., Boddey A., Atkins T., Sarkar-Tyson M., et al. Agenomic survey of positive selection in Burkholderia pseudomallei provides insights into the evolution of accidental virulence. PLoS Pathog. 2010, 6:e1000845.
25. van Zandt K.E., Tuanyok A., Keim P.S., Warren R.L., Gelhaus H.C. An objective approach for Burkholderia pseudomallei strain selection as challenge material for medical countermeasures efficacy testing. Front. Cell Infect. Microbiol. 2012, 2. 10.3389/fcimb.2012.00120.
26. Medzhitov R., Janeway C.A. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 1997, 9:4-9.
27. Corti A., Fassina G., Marcucci F., Barbanti E., Cassani G. Oligomeric tumour necrosis factor alpha slowly converts into inactive forms at bioactive levels. Biochem. J. 1992, 284(Pt 3):905-910.
28. Krippner-Heidenreich A., Grunwald I., Zimmermann G., Kuhnle M., Gerspach J., et al. Single-chain TNF, a TNF derivative with enhanced stability and antitumoral activity. J.Immunol. 2008, 180:8176-8183.
29. Remick D.G., Strieter R.M., Lynch J.P., Nguyen D., Eskandari M., et al. Invivo dynamics of murine tumor necrosis factor-alpha gene expression. Kinetics of dexamethasone-induced suppression. Lab. Invest. 1989, 60:766-771.
30. Friedland J.S., Suputtamongkol Y., Remick D.G., Chaowagul W., Strieter R.M., et al. Prolonged elevation of interleukin-8 and interleukin-6 concentrations in plasma and of leukocyte interleukin-8 mRNA levels during septicemic and localized Pseudomonas pseudomallei infection. Infect. Immun. 1992, 60:2402-2408.
31. Easton A., Haque A., Chu K., Lukaszewski R., Bancroft G.J. Acritical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J.Infect. Dis. 2007, 195:99-107.
32. Haque A., Easton A., Smith D., O'Garra A., Van Rooijen N., et al. Role of T cells in innate and adaptive immunity against murine Burkholderia pseudomallei infection. J.Infect. Dis. 2006, 193:370-379.
33. Koo G.C., Gan Y.H. The innate interferon gamma response of BALB/c and C57BL/6 mice to invitro Burkholderia pseudomallei infection. BMC Immunol. 2006, 7:19.
34. Liu B., Koo G.C., Yap E.H., Chua K.L., Gan Y.H. Model of differential susceptibility to mucosal Burkholderia pseudomallei infection. Infect. Immun. 2002, 70:504-511.
35. Rowland C.A., Lertmemongkolchai G., Bancroft A., Haque A., Lever M.S., et al. Critical role of type 1 cytokines in controlling initial infection with Burkholderia mallei. Infect. Immun. 2006, 74:5333-5340.
36. Santanirand P., Harley V.S., Dance D.A., Drasar B.S., Bancroft G.J. Obligatory role of gamma interferon for host survival in a murine model of infection with Burkholderia pseudomallei. Infect. Immun. 1999, 67:3593-3600.
37. Tan G.Y., Liu Y., Sivalingam S.P., Sim S.H., Wang D., et al. Burkholderia pseudomallei aerosol infection results in differential inflammatory responses in BALB/c and C57Bl/6 mice. J.Med. Microbiol. 2008, 57:508-515.
38. West T.E., Myers N.D., Liggitt H.D., Skerrett S.J. Murine pulmonary infection and inflammation induced by inhalation of Burkholderia pseudomallei. Int. J. Exp. Pathol. 2012, 93:421-428.
39. Andoh M., Zhang G., Russell-Lodrigue K.E., Shive H.R., Weeks B.R., et al. Tcells are essential for bacterial clearance, and gamma interferon, tumor necrosis factor alpha, and B cells are crucial for disease development in Coxiella burnetii infection in mice. Infect. Immun. 2007, 75:3245-3255.
40. Cavalcanti Y.V., Brelaz M.C., Neves J.K., Ferraz J.C., Pereira V.R. Role of TNF-alpha, IFN-gamma, and IL-10 in the development of pulmonary tuberculosis. Pulm. Med. 2012, 2012:745483.
41. Gazzinelli R.T., Wysocka M., Hieny S., Scharton-Kersten T., Cheever A., et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J.Immunol. 1996, 157:798-805.
42. Goodyear A., Jones A., Troyer R., Bielefeldt-Ohmann H., Dow S. Critical protective role for MCP-1 in pneumonic Burkholderia mallei infection. J.Immunol. 2010, 184:1445-1454.
43. Kummer L.W., Szaba F.M., Parent M.A., Adamovicz J.J., Hill J., et al. Antibodies and cytokines independently protect against pneumonic plague. Vaccine 2008, 26:6901-6907.
44. Lin J.S., Park S., Adamovicz J.J., Hill J., Bliska J.B., et al. TNFalpha and IFNgamma contribute to F1/LcrV-targeted immune defense in mouse models of fully virulent pneumonic plague. Vaccine 2010, 29:357-362.
45. Lin P.L., Flynn J.L. Understanding latent tuberculosis: a moving target. J.Immunol. 2010, 185:15-22.
46. Parent M.A., Wilhelm L.B., Kummer L.W., Szaba F.M., Mullarky I.K., et al. Gamma interferon, tumor necrosis factor alpha, and nitric oxide synthase 2, key elements of cellular immunity, perform critical protective functions during humoral defense against lethal pulmonary Yersinia pestis infection. Infect. Immun. 2006, 74:3381-3386.
47. Cyktor J.C., Turner J. Interleukin-10 and immunity against prokaryotic and eukaryotic intracellular pathogens. Infect. Immun. 2011, 79:2964-2973.
48. Saraiva M., O'Garra A. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 2010, 10:170-181.
49. Taylor A., Verhagen J., Blaser K., Akdis M., Akdis C.A. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 2006, 117:433-442.
50. Farber J.M. Mig and IP-10: CXC chemokines that target lymphocytes. J.Leukoc. Biol. 1997, 61:246-257.
51. Dvorak H.F. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J.Clin. Oncol. 2002, 20:4368-4380.
52. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999, 13:9-22.
53. Angelo L.S., Kurzrock R. Vascular endothelial growth factor and its relationship to inflammatory mediators. Clin. Cancer Res. 2007, 13:2825-2830.
54. Yu W.C., Chan R.W., Wang J., Travanty E.A., Nicholls J.M., et al. Viral replication and innate host responses in primary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J.Virol. 2011, 85:6844-6855.
55. Cousins S.W., Espinosa-Heidmann D.G., Miller D.M., Pereira-Simon S., Hernandez E.P., et al. Macrophage activation associated with chronic murine cytomegalovirus infection results in more severe experimental choroidal neovascularization. PLoS Pathog. 2012, 8:e1002671.
56. van der Flier M., Coenjaerts F., Kimpen J.L., Hoepelman A.M., Geelen S.P. Streptococcus pneumoniae induces secretion of vascular endothelial growth factor by human neutrophils. Infect. Immun. 2000, 68:4792-4794.
57. Kempf V.A., Volkmann B., Schaller M., Sander C.A., Alitalo K., et al. Evidence of a leading role for VEGF in Bartonella henselae-induced endothelial cell proliferations. Cell. Microbiol. 2001, 3:623-632.
58. van der Flier M., Stockhammer G., Vonk G.J., Nikkels P.G., van Diemen-Steenvoorde R.A., et al. Vascular endothelial growth factor in bacterial meningitis: detection in cerebrospinal fluid and localization in postmortem brain. J.Infect. Dis. 2001, 183:149-153.
59. Barnes J.L., Williams N.L., Ketheesan N. Susceptibility to Burkholderia pseudomallei is associated with host immune responses involving tumor necrosis factor receptor-1 (TNFR1) and TNF receptor-2 (TNFR2). FEMS Immunol. Med. Microbiol. 2008, 52:379-388.
60. Wiersinga W.J., Calandra T., Kager L.M., van der Windt G.J., Roger T., et al. Expression and function of macrophage migration inhibitory factor (MIF) in melioidosis. PLoS Negl. Trop. Dis. 2010, 4:e605.
61. Barnes J.L., Ulett G.C., Ketheesan N., Clair T., Summers P.M., et al. Induction of multiple chemokine and colony-stimulating factor genes in experimental Burkholderia pseudomallei infection. Immunol. Cell Biol. 2001, 79:490-501.
62. Massey S., Yeager L.A., Blumentritt C.A., Vijayakumar S., Sbrana E., et al. Comparative Burkholderia pseudomallei natural history virulence studies using an aerosol murine model of infection. Sci. Rep. 2014, 4:4305.
63. Lauw F.N., Simpson A.J., Prins J.M., Smith M.D., Kurimoto M., et al. 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. 1999, 180:1878-1885.
64. Breitbach K., Klocke S., Tschernig T., van Rooijen N., Baumann U., et al. Role of inducible nitric oxide synthase and NADPH oxidase in early control of Burkholderia pseudomallei infection in mice. Infect. Immun. 2006, 74:6300-6309.
65. Ulett G.C., Ketheesan N., Hirst R.G. Cytokine gene expression in innately susceptible BALB/c mice and relatively resistant C57BL/6 mice during infection with virulent Burkholderia pseudomallei. Infect. Immun. 2000, 68:2034-2042.