Burkholderia pseudomallei capsule exacerbates respiratory melioidosis but does not afford protection against antimicrobial signaling or bacterial killing in human olfactory ensheathing cells

Samantha J. Dando, Deepak S. Ipe, Michael Batzloff, Matthew J. Sullivan, David K. Crossman, Michael Crowley, Emily Strong, Stephanie Kyan, Sophie Y. Leclercq, Jenny A.K. Ekberg, James St. John, Ifor R. Beacham, Glen C. Ulett

Research output: Contribution to journalArticle

1 Citation (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1941-1956
Number of pages16
JournalInfection and immunity
Volume84
Issue number7
DOIs
StatePublished - Jan 1 2016
Externally publishedYes

Fingerprint

Melioidosis
Burkholderia pseudomallei
Capsules
Olfactory Mucosa
Polysaccharides
Cytokines
Infection
Burkholderia Infections
Bacterial Polysaccharides
Inhalation Exposure
Survival
Neutrophil Infiltration
Gene Regulatory Networks
Immune System Diseases
Lymphoid Tissue
Acute Disease
Granulocyte Colony-Stimulating Factor
Aerosols
Nose
Innate Immunity

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

Burkholderia pseudomallei capsule exacerbates respiratory melioidosis but does not afford protection against antimicrobial signaling or bacterial killing in human olfactory ensheathing cells. / Dando, Samantha J.; Ipe, Deepak S.; Batzloff, Michael; Sullivan, Matthew J.; Crossman, David K.; Crowley, Michael; Strong, Emily; Kyan, Stephanie; Leclercq, Sophie Y.; Ekberg, Jenny A.K.; St. John, James; Beacham, Ifor R.; Ulett, Glen C.

In: Infection and immunity, Vol. 84, No. 7, 01.01.2016, p. 1941-1956.

Research output: Contribution to journalArticle

Dando, SJ, Ipe, DS, Batzloff, M, Sullivan, MJ, Crossman, DK, Crowley, M, Strong, E, Kyan, S, Leclercq, SY, Ekberg, JAK, St. John, J, Beacham, IR & Ulett, GC 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, vol. 84, no. 7, pp. 1941-1956. https://doi.org/10.1128/IAI.01546-15
Dando, Samantha J. ; Ipe, Deepak S. ; Batzloff, Michael ; Sullivan, Matthew J. ; Crossman, David K. ; Crowley, Michael ; Strong, Emily ; Kyan, Stephanie ; Leclercq, Sophie Y. ; Ekberg, Jenny A.K. ; St. John, James ; Beacham, Ifor R. ; Ulett, Glen C. / Burkholderia pseudomallei capsule exacerbates respiratory melioidosis but does not afford protection against antimicrobial signaling or bacterial killing in human olfactory ensheathing cells. In: Infection and immunity. 2016 ; Vol. 84, No. 7. pp. 1941-1956.
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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.",
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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.

AB - 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.

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