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Distinct Pathogenic Patterns of Burkholderia pseudomallei Isolates Selected from Caenorhabditis elegans and Dictyostelium discoideum Models.
Am J Trop Med Hyg. 2019 10; 101(4):736-745.AJ

Abstract

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.

Authors+Show Affiliations

Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan.Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan.Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan.Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan.Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan.Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan.School of Medicine, Institute of Public Health, National Yang-Ming University, Taipei, Taiwan. Medical Research Department, General Clinical Research Center, Taipei Veterans General Hospital, Taipei, Taiwan.Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan. Department of Internal Medicine, National Yang-Ming University, Taipei, Taiwan.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31392941

Citation

Chen, Ya-Lei, et al. "Distinct Pathogenic Patterns of Burkholderia Pseudomallei Isolates Selected From Caenorhabditis Elegans and Dictyostelium Discoideum Models." The American Journal of Tropical Medicine and Hygiene, vol. 101, no. 4, 2019, pp. 736-745.
Chen YL, Hsu DW, Hsueh PT, et al. Distinct Pathogenic Patterns of Burkholderia pseudomallei Isolates Selected from Caenorhabditis elegans and Dictyostelium discoideum Models. Am J Trop Med Hyg. 2019;101(4):736-745.
Chen, Y. L., Hsu, D. W., Hsueh, P. T., Chen, J. A., Shih, P. J., Lee, S., Lin, H. H., & Chen, Y. S. (2019). Distinct Pathogenic Patterns of Burkholderia pseudomallei Isolates Selected from Caenorhabditis elegans and Dictyostelium discoideum Models. The American Journal of Tropical Medicine and Hygiene, 101(4), 736-745. https://doi.org/10.4269/ajtmh.19-0052
Chen YL, et al. Distinct Pathogenic Patterns of Burkholderia Pseudomallei Isolates Selected From Caenorhabditis Elegans and Dictyostelium Discoideum Models. Am J Trop Med Hyg. 2019;101(4):736-745. PubMed PMID: 31392941.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Distinct Pathogenic Patterns of Burkholderia pseudomallei Isolates Selected from Caenorhabditis elegans and Dictyostelium discoideum Models. AU - Chen,Ya-Lei, AU - Hsu,Duen-Wei, AU - Hsueh,Pei-Tan, AU - Chen,Jou-An, AU - Shih,Pei-Jyun, AU - Lee,Susan, AU - Lin,Hsi-Hsun, AU - Chen,Yao-Shen, PY - 2019/8/9/pubmed PY - 2020/3/31/medline PY - 2019/8/9/entrez SP - 736 EP - 745 JF - The American journal of tropical medicine and hygiene JO - Am J Trop Med Hyg VL - 101 IS - 4 N2 - 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. SN - 1476-1645 UR - https://www.unboundmedicine.com/medline/citation/31392941/Distinct_Pathogenic_Patterns_of_Burkholderia_pseudomallei_Isolates_Selected_from_Caenorhabditis_elegans_and_Dictyostelium_discoideum_Models_ L2 - https://ajtmh.org/doi/10.4269/ajtmh.19-0052 DB - PRIME DP - Unbound Medicine ER -