- INTRODUCTION
- MATERIALS AND METHODS
- Ethics statement.
- Organisms and animals.
- Caenorhabditis elegans survival assay.
- Resistance to predation by D. discoideum.
- In vitro association and invasion assay.
- Construction of a Tn5 transposon-mutant library.
- Survival rates of mice with melioidosis and bacterial loads in organs.
- Histological examination.
- Statistical analysis.
- Accession numbers.
- RESULTS
- DISCUSSION
- Supplemental tables and figures
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Cheng AC, Currie BJ, 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416.
-
2.
Dance DA, 2000. Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Trop 74: 159–168.
-
3.
Chen PS, Chen YS, Lin HH, Liu PJ, Ni WF, Hsueh PT, Liang SH, Chen C, Chen YL, 2015. Airborne transmission of melioidosis to humans from environmental aerosols contaminated with B. pseudomallei. PLoS Negl Trop Dis 9: e0003834.
-
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 Dis 4: e900.
-
5.
Ulett GC et al. 2001. Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3: 621–631.
-
6.
Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ, 2006. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272–282.
-
7.
Chen YS, Shieh WJ, Goldsmith CS, Metcalfe MG, Greer PW, Zaki SR, Chang HH, Chan H, Chen YL, 2014. Alteration of the phenotypic and pathogenic patterns of Burkholderia pseudomallei that persist in a soil environment. Am J Trop Med Hyg 90: 469–479.
-
8.
Vora SK, 2002. Sherlock Holmes and a biological weapon. J R Soc Med 95: 101–103.
-
9.
Lee SH, Ooi SK, Mahadi NM, Tan MW, Nathan S, 2011. Complete killing of Caenorhabditis elegans by Burkholderia pseudomallei is dependent on prolonged direct association with the viable pathogen. PLoS One 6: e16707.
-
10.
Hasselbring BM, Patel MK, Schell MA, 2011. Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors. Infect Immun 79: 2079–2088.
-
11.
Stone JK, DeShazer D, Brett PJ, Burtnick MN, 2014. Melioidosis: molecular aspects of pathogenesis. Expert Rev Anti Infect Ther 12: 1487–1499.
-
12.
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.
-
13.
Ooi SK, Lim TY, Lee SH, Nathan S, 2012. Burkholderia pseudomallei kills Caenorhabditis elegans through virulence mechanisms distinct from intestinal lumen colonization. Virulence 3: 485–496.
-
14.
Chen YS, Lin HH, Hsueh PT, Ni WF, Liu PJ, Chen PS, Chang HH, Sun DS, Chen YL, 2016. Involvement of L-selectin expression in Burkholderia pseudomallei-infected monocytes invading the brain during murine melioidosis. Virulence 8: 751–766.
-
15.
Hsueh PT, Lin HH, Liu CL, Ni WF, Chen YL, Chen YS, 2018. Burkholderia pseudomallei-loaded cells act as a Trojan horse to invade the brain during endotoxemia. Sci Rep 8: 13632.
-
16.
Jones AL, Beveridge TJ, Woods DE, 1996. Intracellular survival of Burkholderia pseudomallei. Infect Immun 64: 782–790.
-
17.
Chen YS, Lin HH, Hsueh PT, Liu PJ, Ni WF, Chung WC, Lin CP, Chen YL, 2015. Whole-genome sequence of an epidemic strain of Burkholderia pseudomallei vgh07 in Taiwan. Genome Announc 3: e00345-15.
-
18.
Hsueh PT, Liu JK, Chen YL, Liu PJ, Ni WF, Chen YS, Wu KM, Lin HH, 2015. Genomic sequence of Burkholderia multivorans NKI379, a soil bacterium that inhibits the growth of Burkholderia pseudomallei. Genome Announc 3: e01294-15.
-
19.
Hsueh PT, Liu CL, Wang HH, Ni WF, Chen YL, Liu JK, 2016. A comparison of the immunological potency of Burkholderia lipopolysaccharides in endotoxemic BALB/c mice. Microbiol Immunol 60: 725–739.
-
20.
Yu Y et al. 2006. Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 6: 46.
-
21.
Chen YS, Lin HH, Liu PJ, Tsai HY, Hsueh PT, Liu HY, Chen YL, 2011. Use of 3-hydroxy fatty acid concentrations in a murine air pouch infection model as a surrogate marker for LPS activity: a feasibility study using environmental Burkholderia cenocepacia isolates. J Microbiol Methods 87: 368–374.
-
22.
Pande A, Veale TC, Grove A, 2018. Gene regulation by redox-sensitive Burkholderia thailandensis OhrR and its role in bacterial killing of Caenorhabditis elegans. Infect Immun 86: e00322-18.
-
23.
Wong YC, Abd El Ghany M, Ghazzali RNM, Yap SJ, Hoh CC, Pain A, Nathan S, 2018. Genetic determinants associated with in vivo survival of Burkholderia cenocepacia in the Caenorhabditis elegans model. Front Microbiol 9: 1118.
-
24.
Cooper VS, Carlson WA, Lipuma JJ, 2009. Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS One 4: e7961.
-
25.
Eng SA, Nathan S, 2015. Curcumin rescues Caenorhabditis elegans from a Burkholderia pseudomallei infection. Front Microbiol 6: 290.
-
26.
Aubert DF, Flannagan RS, Valvano MA, 2008. A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76: 1979–1991.
-
27.
Chen PL, Chen YW, Ou CC, Lee TM, Wu CJ, Ko WC, Chen CS, 2016. A disease model of muscle necrosis caused by Aeromonas dhakensis infection in Caenorhabditis elegans. Front Microbiol 7: 2058.
-
28.
Fey P, Kowal AS, Gaudet P, Pilcher KE, Chisholm RL, 2007. Protocols for growth and development of Dictyostelium discoideum. Nat Protoc 2: 1307–1316.
-
29.
Novem V et al. 2009. Structural and biological diversity of lipopolysaccharides from Burkholderia pseudomallei and Burkholderia thailandensis. Clin Vaccin Immunol 16: 1420–1428.
-
30.
Lin HH, Chen YS, Li YC, Tseng IL, Hsieh TH, Buu LM, Chen YL, 2011. Burkholderia multivorans acts as an antagonist against the growth of Burkholderia pseudomallei in soil. Microbiol Immunol 55: 616–624.
-
31.
Hsueh PT, Chen YS, Lin HH, Liu PJ, Ni WF, Liu MC, Chen YL, 2015. Comparison of whole-genome sequences from two colony morphovars of Burkholderia pseudomallei. Genome Announc 3: e01194-15.
-
32.
Chen YS, Lin HH, Hung CC, Mu JJ, Hsiao YS, Chen YL, 2009. Phenotypic characteristics and pathogenic ability across distinct morphotypes of Burkholderia pseudomallei DT. Microbiol Immunol 53: 184–189.
-
33.
Wiersinga WJ, Virk HS, Torres AG, Currie BJ, Peacock SJ, Dance DAB, Limmathurotsakul D, 2018. Melioidosis. Nat Rev Dis Primers 4: 17107.
-
34.
Loutet SA, Valvano MA, 2010. A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78: 4088–1400.
-
35.
Glass MB, Gee JE, Steigerwalt AG, Cavuoti D, Barton T, Hardy RD, Godoy D, Spratt BG, Clark TA, Wilkins PP, 2006. Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. J Clin Microbiol 44: 4601–4604.
-
36.
Rozsa L, Apari P, Sulyok M, Tappe D, Bodo I, Hardi R, Müller V, 2017. The evolutionary logic of sepsis. Infect Genet Evol 55: 135–141.
-
37.
Eberl L, 2006. Quorum sensing in the genus Burkholderia. Int J Med Microbiol 296: 103–110.
-
38.
Buroni S, Scoffone VC, Fumagalli M, Makarov V, Cagnone M, Trespidi G, De Rossi E, Forneris F, Riccardi G, Chiarelli LR, 2018. Investigating the mechanism of action of diketopiperazines inhibitors of the Burkholderia cenocepacia quorum sensing synthase CepI: a site-directed mutagenesis study. Front Pharmacol 9: 836.
-
39.
Klaus JR et al. 2018. Malleilactone is a Burkholderia pseudomallei virulence factor regulated by antibiotics and quorum sensing. J Bacteriol 200: e00008-18.
-
40.
Chua KL, Chan YY, Gan YH, 2003. Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71: 1622–1629.
-
41.
Valvano MA, 2015. Intracellular survival of Burkholderia cepacia complex in phagocytic cells. Can J Microbiol 61: 607–615.
-
42.
Whiteley L, Haug M, Klein K, Willmann M, Bohn E, Chiantia S, Schwarz S, 2017. Cholesterol and host cell surface proteins contribute to cell-cell fusion induced by the Burkholderia type VI secretion system 5. PLoS One 12: e0185715.
-
43.
Whiteley L et al. 2017. Entry, intracellular survival, and multinucleated-giant-cell-forming activity of Burkholderia pseudomallei in human primary phagocytic and nonphagocytic cells. Infect Immun 85: e00468-17.
-
44.
Liu PJ, Chen YS, Lin HH, Ni WF, Hsieh TH, Chen HT, Chen YL, 2013. Induction of mouse melioidosis with meningitis by CD11b+ phagocytic cells harboring intracellular B. pseudomallei as a Trojan horse. PLoS Negl Trop Dis 7: e2363.
-
45.
Pukatzki S, Kessin RH, Mekalanos JJ, 2002. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 99: 3159–3164.
-
46.
Willcocks SJ, Denman CC, Atkins HS, Wren BW, 2016. Intracellular replication of the well-armed pathogen Burkholderia pseudomallei. Curr Opin Microbiol 29: 94–103.
-
47.
Hsueh PT, Huang WT, Hsueh HK, Chen YL, Chen YS, 2018. Transmission modes of melioidosis in Taiwan. Trop Med Infect Dis 3: E26.
-
48.
Zueter AR, Rahman ZA, Abumarzouq M, Harun A, 2018. Multilocus sequence types of clinical Burkholderia pseudomallei isolates from peninsular Malaysia and their associations with disease outcomes. BMC Infect Dis 18: 5.
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49.
Vesaratchavest M et al. 2006. Nonrandom distribution of Burkholderia pseudomallei clones in relation to geographical location and virulence. J Clin Microbiol 44: 2553–2557.
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50.
Shea AA et al. 2017. Two stable variants of Burkholderia pseudomallei strain MSHR5848 express broadly divergent in vitro phenotypes associated with their virulence differences. PLoS One 12: e0171363.
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Distinct Pathogenic Patterns of Burkholderia pseudomallei Isolates Selected from Caenorhabditis elegans and Dictyostelium discoideum Models
Ya-Lei Chen
Ya-Lei Chen
Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan;
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Duen-Wei Hsu
Duen-Wei Hsu
Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan;
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Pei-Tan Hsueh
Pei-Tan Hsueh
Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan;
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Jou-An Chen
Jou-An Chen
Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan;
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Pei-Jyun Shih
Pei-Jyun Shih
Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan;
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Susan Lee
Susan Lee
Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan;
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Hsi-Hsun Lin
Hsi-Hsun Lin
Medical Research Department, General Clinical Research Center, Taipei Veterans General Hospital, Taipei, Taiwan;
School of Medicine, Institute of Public Health, National Yang-Ming University, Taipei, Taiwan;
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School of Medicine, Institute of Public Health, National Yang-Ming University, Taipei, Taiwan;
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Yao-Shen Chen
Yao-Shen Chen
Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan;
Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan
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Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan
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Burkholderia pseudomallei is a selective agent that causes septic melioidosis and exhibits a broad range of lethal doses in animals. Host cellular virulence and phagocytic resistance are pathologic keys of B. pseudomallei. We first proposed Caenorhabditis elegans as the host cellular virulence model to mimic bacterial virulence against mammals and second established the resistance of B. pseudomallei to predation by Dictyostelium discoideum as the phagocytosis model. The saprophytic sepsis–causing Burkholderia sp. (B. pseudomallei, Burkholderia thailandensis, Burkholderia cenocepacia, and Burkholderia multivorans) exhibited different virulence patterns in both simple models, but B. pseudomallei was the most toxic. Using both models, attenuated isolates of B. pseudomallei were selected from a transposon-mutant library and a panel of environmental isolates and reconfirmed by in vitro mouse peritoneal exudate cell association and invasion assays. The distinct pathological patterns of melioidosis were inducted by different selected B. pseudomallei isolates. Fatal melioidosis was induced by the isolates with high virulence in both simple models within 4–5 day, whereas the low-virulence isolates resulted in prolonged survival greater than 30 day. Infection with the isolates having high resistance to D. discoideum predation but a low C. elegans killing effect led to 83% of mice with neurologic melioidosis. By contrast, infection with the isolates having low resistance to D. discoideum predation but high C. elegans killing effect led to 20% cases with inflammation in the salivary glands. Our results indicated that individual B. pseudomallei isolates selected from simple biological models contribute differently to disease progression and/or tissue tropism.
Author Notes
Authors’ addresses: Ya-Lei Chen, Duen-Wei Hsu, Jou-An Chen, and Pei-Jyun Shih, Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan, E-mails: dan1001@ms31.hinet.net, duenwei.hsu@gmail.com, kaiko1101@gmail.com, and spg831105@gmail.com. Pei-Tan Hsueh, Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan, E-mail: mulberrymonster@gmail.com. Susan Lee, Section of Infectious Disease, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan, E-mail: ssjlee@vghks.gov.tw. Hsi-Hsun Lin, Institute of Public Health, National Yang-Ming University, Taipei, Taiwan, E-mail: ed100233@yahoo.com.tw. Yao-Shen Chen, Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan, E-mail: yschen@vghks.gov.tw.
These authors contributed equally to this work.
- INTRODUCTION
- MATERIALS AND METHODS
- Ethics statement.
- Organisms and animals.
- Caenorhabditis elegans survival assay.
- Resistance to predation by D. discoideum.
- In vitro association and invasion assay.
- Construction of a Tn5 transposon-mutant library.
- Survival rates of mice with melioidosis and bacterial loads in organs.
- Histological examination.
- Statistical analysis.
- Accession numbers.
- RESULTS
- DISCUSSION
- Supplemental tables and figures
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Cheng AC, Currie BJ, 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416.
-
2.
Dance DA, 2000. Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Trop 74: 159–168.
-
3.
Chen PS, Chen YS, Lin HH, Liu PJ, Ni WF, Hsueh PT, Liang SH, Chen C, Chen YL, 2015. Airborne transmission of melioidosis to humans from environmental aerosols contaminated with B. pseudomallei. PLoS Negl Trop Dis 9: e0003834.
-
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 Dis 4: e900.
-
5.
Ulett GC et al. 2001. Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3: 621–631.
-
6.
Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ, 2006. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272–282.
-
7.
Chen YS, Shieh WJ, Goldsmith CS, Metcalfe MG, Greer PW, Zaki SR, Chang HH, Chan H, Chen YL, 2014. Alteration of the phenotypic and pathogenic patterns of Burkholderia pseudomallei that persist in a soil environment. Am J Trop Med Hyg 90: 469–479.
-
8.
Vora SK, 2002. Sherlock Holmes and a biological weapon. J R Soc Med 95: 101–103.
-
9.
Lee SH, Ooi SK, Mahadi NM, Tan MW, Nathan S, 2011. Complete killing of Caenorhabditis elegans by Burkholderia pseudomallei is dependent on prolonged direct association with the viable pathogen. PLoS One 6: e16707.
-
10.
Hasselbring BM, Patel MK, Schell MA, 2011. Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors. Infect Immun 79: 2079–2088.
-
11.
Stone JK, DeShazer D, Brett PJ, Burtnick MN, 2014. Melioidosis: molecular aspects of pathogenesis. Expert Rev Anti Infect Ther 12: 1487–1499.
-
12.
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.
-
13.
Ooi SK, Lim TY, Lee SH, Nathan S, 2012. Burkholderia pseudomallei kills Caenorhabditis elegans through virulence mechanisms distinct from intestinal lumen colonization. Virulence 3: 485–496.
-
14.
Chen YS, Lin HH, Hsueh PT, Ni WF, Liu PJ, Chen PS, Chang HH, Sun DS, Chen YL, 2016. Involvement of L-selectin expression in Burkholderia pseudomallei-infected monocytes invading the brain during murine melioidosis. Virulence 8: 751–766.
-
15.
Hsueh PT, Lin HH, Liu CL, Ni WF, Chen YL, Chen YS, 2018. Burkholderia pseudomallei-loaded cells act as a Trojan horse to invade the brain during endotoxemia. Sci Rep 8: 13632.
-
16.
Jones AL, Beveridge TJ, Woods DE, 1996. Intracellular survival of Burkholderia pseudomallei. Infect Immun 64: 782–790.
-
17.
Chen YS, Lin HH, Hsueh PT, Liu PJ, Ni WF, Chung WC, Lin CP, Chen YL, 2015. Whole-genome sequence of an epidemic strain of Burkholderia pseudomallei vgh07 in Taiwan. Genome Announc 3: e00345-15.
-
18.
Hsueh PT, Liu JK, Chen YL, Liu PJ, Ni WF, Chen YS, Wu KM, Lin HH, 2015. Genomic sequence of Burkholderia multivorans NKI379, a soil bacterium that inhibits the growth of Burkholderia pseudomallei. Genome Announc 3: e01294-15.
-
19.
Hsueh PT, Liu CL, Wang HH, Ni WF, Chen YL, Liu JK, 2016. A comparison of the immunological potency of Burkholderia lipopolysaccharides in endotoxemic BALB/c mice. Microbiol Immunol 60: 725–739.
-
20.
Yu Y et al. 2006. Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol 6: 46.
-
21.
Chen YS, Lin HH, Liu PJ, Tsai HY, Hsueh PT, Liu HY, Chen YL, 2011. Use of 3-hydroxy fatty acid concentrations in a murine air pouch infection model as a surrogate marker for LPS activity: a feasibility study using environmental Burkholderia cenocepacia isolates. J Microbiol Methods 87: 368–374.
-
22.
Pande A, Veale TC, Grove A, 2018. Gene regulation by redox-sensitive Burkholderia thailandensis OhrR and its role in bacterial killing of Caenorhabditis elegans. Infect Immun 86: e00322-18.
-
23.
Wong YC, Abd El Ghany M, Ghazzali RNM, Yap SJ, Hoh CC, Pain A, Nathan S, 2018. Genetic determinants associated with in vivo survival of Burkholderia cenocepacia in the Caenorhabditis elegans model. Front Microbiol 9: 1118.
-
24.
Cooper VS, Carlson WA, Lipuma JJ, 2009. Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS One 4: e7961.
-
25.
Eng SA, Nathan S, 2015. Curcumin rescues Caenorhabditis elegans from a Burkholderia pseudomallei infection. Front Microbiol 6: 290.
-
26.
Aubert DF, Flannagan RS, Valvano MA, 2008. A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76: 1979–1991.
-
27.
Chen PL, Chen YW, Ou CC, Lee TM, Wu CJ, Ko WC, Chen CS, 2016. A disease model of muscle necrosis caused by Aeromonas dhakensis infection in Caenorhabditis elegans. Front Microbiol 7: 2058.
-
28.
Fey P, Kowal AS, Gaudet P, Pilcher KE, Chisholm RL, 2007. Protocols for growth and development of Dictyostelium discoideum. Nat Protoc 2: 1307–1316.
-
29.
Novem V et al. 2009. Structural and biological diversity of lipopolysaccharides from Burkholderia pseudomallei and Burkholderia thailandensis. Clin Vaccin Immunol 16: 1420–1428.
-
30.
Lin HH, Chen YS, Li YC, Tseng IL, Hsieh TH, Buu LM, Chen YL, 2011. Burkholderia multivorans acts as an antagonist against the growth of Burkholderia pseudomallei in soil. Microbiol Immunol 55: 616–624.
-
31.
Hsueh PT, Chen YS, Lin HH, Liu PJ, Ni WF, Liu MC, Chen YL, 2015. Comparison of whole-genome sequences from two colony morphovars of Burkholderia pseudomallei. Genome Announc 3: e01194-15.
-
32.
Chen YS, Lin HH, Hung CC, Mu JJ, Hsiao YS, Chen YL, 2009. Phenotypic characteristics and pathogenic ability across distinct morphotypes of Burkholderia pseudomallei DT. Microbiol Immunol 53: 184–189.
-
33.
Wiersinga WJ, Virk HS, Torres AG, Currie BJ, Peacock SJ, Dance DAB, Limmathurotsakul D, 2018. Melioidosis. Nat Rev Dis Primers 4: 17107.
-
34.
Loutet SA, Valvano MA, 2010. A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78: 4088–1400.
-
35.
Glass MB, Gee JE, Steigerwalt AG, Cavuoti D, Barton T, Hardy RD, Godoy D, Spratt BG, Clark TA, Wilkins PP, 2006. Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. J Clin Microbiol 44: 4601–4604.
-
36.
Rozsa L, Apari P, Sulyok M, Tappe D, Bodo I, Hardi R, Müller V, 2017. The evolutionary logic of sepsis. Infect Genet Evol 55: 135–141.
-
37.
Eberl L, 2006. Quorum sensing in the genus Burkholderia. Int J Med Microbiol 296: 103–110.
-
38.
Buroni S, Scoffone VC, Fumagalli M, Makarov V, Cagnone M, Trespidi G, De Rossi E, Forneris F, Riccardi G, Chiarelli LR, 2018. Investigating the mechanism of action of diketopiperazines inhibitors of the Burkholderia cenocepacia quorum sensing synthase CepI: a site-directed mutagenesis study. Front Pharmacol 9: 836.
-
39.
Klaus JR et al. 2018. Malleilactone is a Burkholderia pseudomallei virulence factor regulated by antibiotics and quorum sensing. J Bacteriol 200: e00008-18.
-
40.
Chua KL, Chan YY, Gan YH, 2003. Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71: 1622–1629.
-
41.
Valvano MA, 2015. Intracellular survival of Burkholderia cepacia complex in phagocytic cells. Can J Microbiol 61: 607–615.
-
42.
Whiteley L, Haug M, Klein K, Willmann M, Bohn E, Chiantia S, Schwarz S, 2017. Cholesterol and host cell surface proteins contribute to cell-cell fusion induced by the Burkholderia type VI secretion system 5. PLoS One 12: e0185715.
-
43.
Whiteley L et al. 2017. Entry, intracellular survival, and multinucleated-giant-cell-forming activity of Burkholderia pseudomallei in human primary phagocytic and nonphagocytic cells. Infect Immun 85: e00468-17.
-
44.
Liu PJ, Chen YS, Lin HH, Ni WF, Hsieh TH, Chen HT, Chen YL, 2013. Induction of mouse melioidosis with meningitis by CD11b+ phagocytic cells harboring intracellular B. pseudomallei as a Trojan horse. PLoS Negl Trop Dis 7: e2363.
-
45.
Pukatzki S, Kessin RH, Mekalanos JJ, 2002. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 99: 3159–3164.
-
46.
Willcocks SJ, Denman CC, Atkins HS, Wren BW, 2016. Intracellular replication of the well-armed pathogen Burkholderia pseudomallei. Curr Opin Microbiol 29: 94–103.
-
47.
Hsueh PT, Huang WT, Hsueh HK, Chen YL, Chen YS, 2018. Transmission modes of melioidosis in Taiwan. Trop Med Infect Dis 3: E26.
-
48.
Zueter AR, Rahman ZA, Abumarzouq M, Harun A, 2018. Multilocus sequence types of clinical Burkholderia pseudomallei isolates from peninsular Malaysia and their associations with disease outcomes. BMC Infect Dis 18: 5.
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