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Chapter 13 : Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation

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Abstract:

Many bacterial species colonize mucosal surfaces, but relatively few are capable of evading the numerous host defenses to gain access to epithelial cells and cause disease. The clinical signs and symptoms of infection are attributed to the local accumulation of polymorphonuclear leukocytes (PMNs) and subsequent destruction of host tissue. The clinical signs and symptoms of airway infection in cystic fibrosis (CF) are mediated primarily by the influx of PMNs from the circulation to the site of infection in the airway. Bacteria in the airway lumen provide a potent stimulus for the epithelial expression of the proinflammatory cytokines, TNF-α, interleukin-1 (IL-1) β, and IL-8. The epithelial cells lining mucosal surfaces act as a peripheral component of the immune system, serving to both signal and respond to the threat of microbial pathogens. One of the major tenets of bacterial pathogenesis is the requirement for a specific ligand receptor interaction between the host and pathogen to initiate infection. The biological relevance of pilin- or flagellin-induced IL-8 expression in the pathogenesis of airway inflammation was further established in an animal model of respiratory tract infection. Pilin-mediated adherence to asialylated receptors, in addition to stimulating IL-8 expression, may also be a prerequisite for other types of virulence. The organisms that elude mucociliary clearance, are resistant to antimicrobial peptide activity in the airways, and are not cleared by encounters with phagocytes, may reach the epithelial surface.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13

Key Concept Ranking

Bacterial Pathogenesis
0.51452744
Outer Membrane Proteins
0.48251376
Type IV Pili
0.44904235
Type 1 Fimbriae
0.44213402
Enzyme-Linked Immunosorbent Assay
0.4155783
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Figures

Image of FIGURE 1
FIGURE 1

Bacterial induction of IL-8 expression. IL-8 was assayed by enzyme-linked immunosorbent assay 18 h after a 1-h exposure of 1HAEo– airway epithelial cells to the strains listed, followed by sterilization of the monolayer with gentamicin and overnight incubation in tissue culture media. PAO1, which elicits 35 pg of IL-8 per g of protein, was considered 100%. The strains included H309 (strain Rd), H311 (ChoP variant), H394 (strain Eagan, ChoP), and H395 (strain Eagan, ChoP variant). strains tested included wild-type RN6390, RN6911 (), ALC 135 (), and ALC 136 ().

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 2
FIGURE 2

Binding competition studies. The percentage of the S-PAO1 inoculum that bound in the presence of each of the competing strains in five- to eightfold excess is shown.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 3
FIGURE 3

Ca fluxes in 1HAEo– cells. Changes in Ca following the addition of bacteria to fura-2 loaded cells (arrows) are shown. Composite images of single cell Ca transients are depicted.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 4
FIGURE 4

Nuclear localization of NF-AT3 in 16HBe- respiratory epithelial cells. NF-AT3 immunofluorescence is detected using polyclonal antibody tagged with fluorescein isothiocyanate-labeled goat anti-rabbit antibody. (A) Control conditions. (B) Fifteen minutes after addition of PAO1 to the epithelial cells showing nuclear localization of NF-AT3.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 5
FIGURE 5

IL-8 expression in 1HAEo– cells. IL-8 production stimulated by PAO1 (5 × 10CFU/ml) in the presence of the several selective kinase inhibitors and compounds expected to block MAPK signaling was measured by ELISA. Solid bars, with PAO; white bar, without PAO.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 6
FIGURE 6

IL-8 expression induced by antibody to asialoGM1. IL-8 expression was inhibited in 1HAEo– cells pretreated with the p38 MAPK inhibitor SB202190 or with the ERK1/1 inhibitor PD98059 but was not altered by NiCl. Solid bars, with antibody to asialoGM1; white bars, without antibody to asialoGM1.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 7
FIGURE 7

Phosphorylated ERK1/2 in response to . A Western hybridization using antibody to phospho-ERK1/2 is shown. Lane A, 0– unstimulated 9HTEo– cells; lanes B, C, and D, 15, 30, and 60 min after stimulation with thapsigargin (100 nM); lanes E, F, and G, 15, 30, and 60 min after stimulation with PAO1; lane H, negative control; lane I, positive control.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 8
FIGURE 8

Colocalization of caveolin, IP3-R, and asialoGM1 in triton-insoluble fraction of 9HTEo– cells. Proteins in the triton insoluble fraction of 9HTEo– cell lysates were immunoprecipitated with anti-caveolin polyclonal antibody. Aliquots of the IP are shown stained with silver on a sodium dodecyl sulfate-polyacrylamide gel (left) or hybridized with anti-caveolin, anti-asialoGM1, or anti-IP3-R1.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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Image of FIGURE 9
FIGURE 9

A model of epithelial activation. Adherent bacteria stimulate asialoGM1 receptors contained within caveolae and signal IL-8 expression through a Ca-dependent MAPK cascade, resulting in translocation of AP-1 and NF-B and gene transcription.

Citation: Prince A. 2000. Bacterial Induction of Cytokine Secretion in Pathogenesis of Airway Inflammation, p 189-202. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch13
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