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Burkholderia pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells.
Infect Immun. 2016 07; 84(7):1941-1956.II

Abstract

Melioidosis, caused by the bacterium Burkholderia pseudomallei, is an often severe infection that regularly involves respiratory disease following inhalation exposure. Intranasal (i.n.) inoculation of mice represents an experimental approach used to study the contributions of bacterial capsular polysaccharide I (CPS I) to virulence during acute disease. We used aerosol delivery of B. pseudomallei to establish respiratory infection in mice and studied CPS I in the context of innate immune responses. CPS I improved B. pseudomallei survival in vivo and triggered multiple cytokine responses, neutrophil infiltration, and acute inflammatory histopathology in the spleen, liver, nasal-associated lymphoid tissue, and olfactory mucosa (OM). To further explore the role of the OM response to B. pseudomallei infection, we infected human olfactory ensheathing cells (OECs) in vitro and measured bacterial invasion and the cytokine responses induced following infection. Human OECs killed >90% of the B. pseudomallei in a CPS I-independent manner and exhibited an antibacterial cytokine response comprising granulocyte colony-stimulating factor, tumor necrosis factor alpha, and several regulatory cytokines. In-depth genome-wide transcriptomic profiling of the OEC response by RNA-Seq revealed a network of signaling pathways activated in OECs following infection involving a novel group of 378 genes that encode biological pathways controlling cellular movement, inflammation, immunological disease, and molecular transport. This represents the first antimicrobial program to be described in human OECs and establishes the extensive transcriptional defense network accessible in these cells. Collectively, these findings show a role for CPS I in B. pseudomallei survival in vivo following inhalation infection and the antibacterial signaling network that exists in human OM and OECs.

Authors+Show Affiliations

Institute for Glycomics, Griffith University, Gold Coast, Australia.Institute for Glycomics, Griffith University, Gold Coast, Australia. School of Medical Science, and Menzies Health Institute Queensland, Griffith University, Gold Coast, Australia.Institute for Glycomics, Griffith University, Gold Coast, Australia.School of Medical Science, and Menzies Health Institute Queensland, Griffith University, Gold Coast, Australia.Heflin Center for Human Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA.Heflin Center for Human Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA.Institute for Glycomics, Griffith University, Gold Coast, Australia.Institute for Glycomics, Griffith University, Gold Coast, Australia.School of Medical Science, and Menzies Health Institute Queensland, Griffith University, Gold Coast, Australia. Research and Development Center, Ezequiel Dias Foundation (FUNED), Belo Horizonte, MG, Brazil.School of Biomedical Sciences, Queensland University of Technology, Brisbane, Queensland, Australia. Eskitis Institute for Drug Discovery, Griffith University, Brisbane, Australia.Eskitis Institute for Drug Discovery, Griffith University, Brisbane, Australia.Institute for Glycomics, Griffith University, Gold Coast, Australia i.beacham@griffith.edu.au g.ulett@griffith.edu.au.Institute for Glycomics, Griffith University, Gold Coast, Australia i.beacham@griffith.edu.au g.ulett@griffith.edu.au. School of Medical Science, and Menzies Health Institute Queensland, Griffith University, Gold Coast, Australia. School of Medicine, Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, Alabama, USA.

Pub Type(s)

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

Language

eng

PubMed ID

27091931

Citation

Dando, Samantha J., et al. "Burkholderia Pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection Against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells." Infection and Immunity, vol. 84, no. 7, 2016, pp. 1941-1956.
Dando SJ, Ipe DS, Batzloff M, et al. Burkholderia pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells. Infect Immun. 2016;84(7):1941-1956.
Dando, S. J., Ipe, D. S., Batzloff, M., Sullivan, M. J., Crossman, D. K., Crowley, M., Strong, E., Kyan, S., Leclercq, S. Y., Ekberg, J. A. K., St John, J., Beacham, I. R., & Ulett, G. C. (2016). Burkholderia pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells. Infection and Immunity, 84(7), 1941-1956. https://doi.org/10.1128/IAI.01546-15
Dando SJ, et al. Burkholderia Pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection Against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells. Infect Immun. 2016;84(7):1941-1956. PubMed PMID: 27091931.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Burkholderia pseudomallei Capsule Exacerbates Respiratory Melioidosis but Does Not Afford Protection against Antimicrobial Signaling or Bacterial Killing in Human Olfactory Ensheathing Cells. AU - Dando,Samantha J, AU - Ipe,Deepak S, AU - Batzloff,Michael, AU - Sullivan,Matthew J, AU - Crossman,David K, AU - Crowley,Michael, AU - Strong,Emily, AU - Kyan,Stephanie, AU - Leclercq,Sophie Y, AU - Ekberg,Jenny A K, AU - St John,James, AU - Beacham,Ifor R, AU - Ulett,Glen C, Y1 - 2016/06/23/ PY - 2015/12/21/received PY - 2016/04/03/accepted PY - 2016/4/20/entrez PY - 2016/4/20/pubmed PY - 2017/5/19/medline SP - 1941 EP - 1956 JF - Infection and immunity JO - Infect Immun VL - 84 IS - 7 N2 - Melioidosis, caused by the bacterium Burkholderia pseudomallei, is an often severe infection that regularly involves respiratory disease following inhalation exposure. Intranasal (i.n.) inoculation of mice represents an experimental approach used to study the contributions of bacterial capsular polysaccharide I (CPS I) to virulence during acute disease. We used aerosol delivery of B. pseudomallei to establish respiratory infection in mice and studied CPS I in the context of innate immune responses. CPS I improved B. pseudomallei survival in vivo and triggered multiple cytokine responses, neutrophil infiltration, and acute inflammatory histopathology in the spleen, liver, nasal-associated lymphoid tissue, and olfactory mucosa (OM). To further explore the role of the OM response to B. pseudomallei infection, we infected human olfactory ensheathing cells (OECs) in vitro and measured bacterial invasion and the cytokine responses induced following infection. Human OECs killed >90% of the B. pseudomallei in a CPS I-independent manner and exhibited an antibacterial cytokine response comprising granulocyte colony-stimulating factor, tumor necrosis factor alpha, and several regulatory cytokines. In-depth genome-wide transcriptomic profiling of the OEC response by RNA-Seq revealed a network of signaling pathways activated in OECs following infection involving a novel group of 378 genes that encode biological pathways controlling cellular movement, inflammation, immunological disease, and molecular transport. This represents the first antimicrobial program to be described in human OECs and establishes the extensive transcriptional defense network accessible in these cells. Collectively, these findings show a role for CPS I in B. pseudomallei survival in vivo following inhalation infection and the antibacterial signaling network that exists in human OM and OECs. SN - 1098-5522 UR - https://www.unboundmedicine.com/medline/citation/27091931/Burkholderia_pseudomallei_Capsule_Exacerbates_Respiratory_Melioidosis_but_Does_Not_Afford_Protection_against_Antimicrobial_Signaling_or_Bacterial_Killing_in_Human_Olfactory_Ensheathing_Cells_ L2 - http://iai.asm.org/cgi/pmidlookup?view=long&pmid=27091931 DB - PRIME DP - Unbound Medicine ER -