Survey of innate immune responses to Burkholderia pseudomallei in human blood identifies a central role for lipopolysaccharide

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Chantratita, Narisara ^a   Tandhavanant, Sarunporn ^a   Myers, Nicolle D ^b   Seal, Sudeshna ^b   Arayawichanont, Arkhom ^c   Kliangsa ad, Aroonsri ^c   Hittle, Lauren E ^d   Ernst, Robert K ^d   Emond, Mary J ^b   Wurfel, Mark M ^b   Day, Nicholas P J ^a,e   Peacock, Sharon J ^a,f   West, T Eoin ^b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Sappasitthiprasong Hospital   (Thailand)

^d UNIVERSITY OF MARYLAND   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; PATTERN RECOGNITION RECEPTOR; POLYMYXIN B; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ADOLESCENT; ADULT; ARTICLE; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; CYTOKINE RELEASE; ESCHERICHIA COLI; ETHNIC GROUP; EX VIVO STUDY; FEMALE; GRAM NEGATIVE BACTERIUM; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; MELIOIDOSIS; MORTALITY; SALMONELLA MINNESOTA; THAI; THAILAND; UPREGULATION;

ADOLESCENT; ADULT; BURKHOLDERIA PSEUDOMALLEI; CYTOKINES; FEMALE; HUMANS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; MALE; MELIOIDOSIS; MIDDLE AGED; MONOCYTES; TOLL-LIKE RECEPTOR 4; YOUNG ADULT;

EID: 84896721076     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081617     Document Type: Article

References (47)

1. Wiersinga WJ, Currie BJ, Peacock SJ (2012) Melioidosis. N Engl J Med 367: 1035-1044. doi:10.1056/NEJMra1204699. PubMed: 22970946.
2. Butler D (2012) Viral research faces clampdown. Nature 490: 456. doi:10.1038/490456a. PubMed: 23099377.
3. Limmathurotsakul D, Wongratanacheewin S, Teerawattanasook N, Wongsuvan G, Chaisuksant S et al. (2010) Increasing incidence of human melioidosis in Northeast Thailand. Am J Trop Med Hyg 82: 1113-1117. doi:10.4269/ajtmh.2010.10- 0038. PubMed: 20519609.
4. Currie BJ, Ward L, Cheng AC (2010) The epidemiology and clinical spectrum of melioidosis: 540 cases from the 20 year Darwin prospective study. PLoS Negl Trop. Drosophila Inf Service 4: e900.
5. Limmathurotsakul D, Wuthiekanun V, Chierakul W, Cheng AC, Maharjan B et al. (2005) Role and significance of quantitative urine cultures in diagnosis of melioidosis. J Clin Microbiol 43: 2274-2276. doi:10.1128/JCM.43.5.2274-2276. 2005. PubMed: 15872255. (Pubitemid 40656240)
6. Abbas AK, Lichtman AH, Pillai S (2012) Cellular and molecular immunology. Philadelphia: Elsevier, Saunders. 560pp.
7. Kumar H, Kawai T, Akira S (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30: 16-34. doi:10.3109/08830185.2010.529976. PubMed: 21235323.
8. Wiersinga WJ, Wieland CW, Dessing MC, Chantratita N, Cheng AC et al. (2007) Toll-like receptor 2 impairs host defense in gram-negative sepsis caused by Burkholderia pseudomallei (Melioidosis). PLoS Med 4: e248. doi:10.1371/journal.pmed.0040248. PubMed: 17676990.
9. Friedland JS, Suputtamongkol Y, Remick DG, Chaowagul W, Strieter RM et al. (1992) 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 60: 2402-2408. PubMed: 1375198.
10. Karima R, Matsumoto S, Higashi H, Matsushima K (1999) The molecular pathogenesis of endotoxic shock and organ failure. Mol Med Today 5: 123-132. doi:10.1016/S1357-4310(98)01430-0. PubMed: 10203736. (Pubitemid 29282266)
11. Matsuura M, Kawahara K, Ezaki T, Nakano M (1996) Biological activities of lipopolysaccharide of Burkholderia (Pseudomonas) pseudomallei. FEMS Microbiol Lett 137: 79-83. doi:10.1111/j.1574-6968.1996.tb08086.x. PubMed: 8935661. (Pubitemid 26120873)
12. Utaisincharoen P, Tangthawornchaikul N, Kespichayawattana W, Anuntagool N, Chaisuriya P et al. (2000) Kinetic studies of the production of nitric oxide (NO) and tumour necrosis factor-alpha (TNF-alpha) in macrophages stimulated with Burkholderia pseudomallei endotoxin. Clin Exp Immunol 122: 324-329. doi:10.1046/j.1365-2249.2000.01386.x. PubMed: 11122236. (Pubitemid 32002188)
13. West TE, Ernst RK, Jansson-Hutson MJ, Skerrett SJ (2008) Activation of Toll-like receptors by Burkholderia pseudomallei. BMC Immunol 9: 46. doi:10.1186/1471-2172-9-46. PubMed: 18691413.
14. Novem V, Shui G, Wang D, Bendt AK, Sim SH et al. (2009) Structural and biological diversity of lipopolysaccharides from Burkholderia pseudomallei and Burkholderia thailandensis. Clin Vaccine Immunol 16: 1420-1428. doi:10.1128/CVI.00472-08. PubMed: 19692625.
15. West TE, Hawn TR, Skerrett SJ (2009) Toll-like receptor signaling in airborne Burkholderia thailandensis infection. Infect Immun 77: 5612-5622. doi:10.1128/IAI.00618-09. PubMed: 19797072.
16. West TE, Chierakul W, Chantratita N, Limmathurotsakul D, Wuthiekanun V et al. (2012) Toll-like receptor 4 region genetic variants are associated with susceptibility to melioidosis. Genes Immun 13: 38-46. doi:10.1038/gene.2011.49. PubMed: 21776015.
17. Westphat O, Jann JK (1965) Bacterial lipopolysaccharide extractio with water-phenol and further applications of the procedure. In: RL WhistlerML Wolfrom. Methods in carbohydrate chemistry. New York: Academic Press. pp. 83-91.
18. Fischer W, Koch HU, Haas R (1983) Improved preparation of lipoteichoic acids. Eur J Biochem 133: 523-530. doi:10.1111/j. 1432-1033.1983.tb07495.x. PubMed: 6190649.
19. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509. PubMed: 13428781.
20. Hirschfeld M, Ma Y, Weis JH, Vogel SN, Weis JJ (2000) Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J Immunol 165: 618-622. PubMed: 10878331. (Pubitemid 30484724)
21. Darveau RP, Cunningham MD, Bailey T, Seachord C, Ratcliffe K et al. (1995) Ability of bacteria associated with chronic inflammatory disease to stimulate E-selectin expression and promote neutrophil adhesion. Infect Immun 63: 1311-1317. PubMed: 7534275.
22. Somerville JE Jr., Cassiano L, Bainbridge B, Cunningham MD, Darveau RP (1996) A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J Clin Invest 97: 359-365. doi:10.1172/JCI118423. PubMed: 8567955. (Pubitemid 26039398)
23. Wurfel MM, Gordon AC, Holden TD, Radella F, Strout J et al. (2008) Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis. Am J Respir Crit Care Med 178: 710-720. doi:10.1164/rccm.200803- 462OC. PubMed: 18635889.
24. Lynn WA, Golenbock DT (1992) Lipopolysaccharide antagonists. Immunol Today 13: 271-276. doi:10.1016/0167-5699(92)90009-V. PubMed: 1388655.
25. Anuntagool N, Wuthiekanun V, White NJ, Currie BJ, Sermswan RW et al. (2006) Lipopolysaccharide heterogeneity among Burkholderia pseudomallei from different geographic and clinical origins. Am J Trop Med Hyg 74: 348-352. PubMed: 16525090. (Pubitemid 46774353)
26. Wiersinga WJ, van der Poll T (2009) Immunity to Burkholderia pseudomallei. Curr Opin Infect Dis 22: 102-108. doi:10.1097/QCO. 0b013e328322e727. PubMed: 19276877.
27. Limmathurotsakul D, Peacock SJ (2011) Melioidosis: a clinical overview. Br Med Bull 99: 125-139. doi:10.1093/bmb/ldr007. PubMed: 21558159.
28. Simpson AJ, Opal SM, Angus BJ, Prins JM, Palardy JE et al. (2000) Differential antibiotic-induced endotoxin release in severe melioidosis. J Infect Dis 181: 1014-1019. doi:10.1086/315306. PubMed: 10720525. (Pubitemid 30194486)
29. Chin CY, Monack DM, Nathan S (2010) Genome wide transcriptome profiling of a murine acute melioidosis model reveals new insights into how Burkholderia pseudomallei overcomes host innate immunity. BMC Genomics 11: 672. doi:10.1186/1471-2164-11-672. PubMed: 21110886.
30. Wuthiekanun V, Chierakul W, Langa S, Chaowagul W, Panpitpat C et al. (2006) Development of antibodies to Burkholderia pseudomallei during childhood in melioidosis-endemic northeast Thailand. Am J Trop Med Hyg 74: 1074-1075. PubMed: 16760522. (Pubitemid 351627418)
31. Ulett GC, Currie BJ, Clair TW, Mayo M, Ketheesan N et al. (2001) Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3: 621-631. doi:10.1016/S1286-4579(01)01417-4. PubMed: 11445448. (Pubitemid 32607757)
32. Holden MT, Titball RW, Peacock SJ, Cerdeño-Tárraga AM, Atkins T et al. (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101: 14240-14245. doi:10.1073/pnas.0403302101. PubMed: 15377794. (Pubitemid 39305059)
33. Wurfel MM, Goss CH, Black RA, Radella F, Plant B et al. (2008) Characterization of TLR-Mediated Innate Immune Responses in Whole Blood of CF Patients and Relation to Pulmonary Phenotype. Pediatric Pulmonology 43.
34. Wurfel MM, Park WY, Radella F, Ruzinski J, Sandstrom A et al. (2005) Identification of high and low responders to lipopolysaccharide in normal subjects: an unbiased approach to identify modulators of innate immunity. J Immunol 175: 2570-2578. PubMed: 16081831. (Pubitemid 41113870)
35. Moxley G, Posthuma D, Carlson P, Estrada E, Han J et al. (2002) Sexual dimorphism in innate immunity. Arthritis Rheum 46: 250-258. doi:10.1002/1529- 0131(200201)46:1. PubMed: 11817599. (Pubitemid 34121672)
36. Imahara SD, Jelacic S, Junker CE, O'Keefe GE (2005) The influence of gender on human innate immunity. Surgery 138: 275-282. doi:10.1016/j.surg.2005. 03.020. PubMed: 16153437. (Pubitemid 41253811)
37. Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348: 1546-1554. doi:10.1056/NEJMoa022139. PubMed: 12700374. (Pubitemid 36437931)
38. Kollmann TR, Levy O, Montgomery RR, Goriely S (2012) Innate Immune Function by Toll-like Receptors: Distinct Responses in Newborns and the Elderly. Immunity 37: 771-783. doi:10.1016/j.immuni.2012.10.014. PubMed: 23159225.
39. Wiersinga WJ, Wieland CW, van der Windt GJ, de Boer A, Florquin S et al. (2007) Endogenous interleukin-18 improves the early antimicrobial host response in severe melioidosis. Infect Immun 75: 3739-3746. doi:10.1128/IAI.00080-07. PubMed: 17517876. (Pubitemid 47206271)
40. Wiersinga WJ, Dessing MC, Kager PA, Cheng AC, Limmathurotsakul D et al. (2007) High-throughput mRNA profiling characterizes the expression of inflammatory molecules in sepsis caused by Burkholderia pseudomallei. Infect Immun 75: 3074-3079. doi:10.1128/IAI.01733-06. PubMed: 17371859. (Pubitemid 46870193)
41. 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. doi:10.1086/315155. PubMed: 10558944.
42. Lauw FN, Simpson AJ, Hack CE, Prins JM, Wolbink AM et al. (2000) Soluble granzymes are released during human endotoxemia and in patients with severe infection due to gram-negative bacteria. J Infect Dis 182: 206-213. doi:10.1086/315642. PubMed: 10882599. (Pubitemid 30497806)
43. Lauw FN, Simpson AJ, Prins JM, van Deventer SJ, Chaowagul W et al. (2000) The CXC chemokines gamma interferon (IFN-gamma)-inducible protein 10 and monokine induced by IFN-gamma are released during severe melioidosis. Infect Immun 68: 3888-3893. doi:10.1128/IAI.68.7.3888-3893.2000. PubMed: 10858199. (Pubitemid 30434537)
44. 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. doi:10.1086/315271. PubMed: 10669346. (Pubitemid 30131830)
45. Doi K, Leelahavanichkul A, Yuen PS, Star RA (2009) Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest 119: 2868-2878. doi:10.1172/JCI39421. PubMed: 19805915.
46. Zanotti-Cavazzoni SL, Goldfarb RD (2009) Animal models of sepsis. Crit Care Clin 25: 703-719. doi:10.1016/j.ccc.2009.08.005. PubMed: 19892248.
47. Warren HS (2009) Editorial: Mouse models to study sepsis syndrome in humans. J Leukoc Biol 86: 199-201. doi:10.1189/jlb.0309210. PubMed: 19643738.