Acanthamoeba castellanii (Genotype T4) Stimulates the Production of Interleukin-10 as well as Pro-inflammatory Cytokines in THP-1 Cells, Human Peripheral Blood Mononuclear Cells and Human Monocyte-Derived Macrophages

Antonella Mattana, Manuela Sanna, Antonella Cano, Giuseppe Delogu, Giuseppe Erre, Craig W. Roberts, Fiona Henriquez, Pier Luigi Fiori, Piero Cappuccinelli

Research output: Contribution to journalArticle

Abstract

Free-living amoebae of the genus Acanthamoeba can cause severe and chronic infections in humans, mainly localized in immune privileged sites, as the brain and the eye. Monocytes/macrophages are thought to be involved in Acanthamoeba infections, but little is known about how these facultative parasites influence their functions. The aim of this work was to investigate the effects of Acanthamoeba on human monocytes/macrophages, during the early phase of infection. Herein, THP-1 cells, primary human monocytes isolated from peripheral blood and human monocyte-derived macrophages were either co-incubated with trophozoites of a clinical isolate of Acanthamoeba (genotype T4) or stimulated with amoeba-derived cell free conditioned medium. Production of pro-inflammatory cytokines (TNF-α, IL-6, IL-12), anti-inflammatory cytokine (IL-10) and chemokine (IL-8) was evaluated at specific hours post-stimulation (ranging from 1.30 h to 23 h). We showed that both Acanthamoeba trophozoites and soluble amoebic products induce an early anti-inflammatory monocyte-macrophage phenotype, characterized by a significant production of IL-10; furthermore, challenge with either trophozoites or their soluble metabolites stimulate both pro-inflammatory cytokines and chemokine production, suggesting that this protozoan infection may result from the early induction of coexisting, opposed immune responses. Results reported in this paper confirm that the production of pro-inflammatory cytokines and chemokines by monocytes and macrophages can play a role in the development of the inflammatory response during Acanthamoeba infections. Furthermore, we demonstrate for the first time that Acanthamoeba stimulates IL-10 production in human innate immune cells, which might both promote the immune evasion of Acanthamoeba and limit the induced inflammatory response.

Original languageEnglish
Pages (from-to)2953-2962
JournalInfection and immunity
Volume84
Issue number10
Early online date1 Aug 2016
DOIs
Publication statusPublished - Oct 2016

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Acanthamoeba castellanii
Acanthamoeba
Interleukin-10
Blood Cells
Macrophages
Genotype
Cytokines
Monocytes
Trophozoites
Chemokines
Amoeba
Infection
Anti-Inflammatory Agents
Protozoan Infections
Immune Evasion
Interleukin-12
Conditioned Culture Medium
Interleukin-8
Interleukin-6
Parasites

Cite this

Mattana, Antonella ; Sanna, Manuela ; Cano, Antonella ; Delogu, Giuseppe ; Erre, Giuseppe ; Roberts, Craig W. ; Henriquez, Fiona ; Fiori, Pier Luigi ; Cappuccinelli, Piero. / Acanthamoeba castellanii (Genotype T4) Stimulates the Production of Interleukin-10 as well as Pro-inflammatory Cytokines in THP-1 Cells, Human Peripheral Blood Mononuclear Cells and Human Monocyte-Derived Macrophages. In: Infection and immunity. 2016 ; Vol. 84, No. 10. pp. 2953-2962.
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abstract = "Free-living amoebae of the genus Acanthamoeba can cause severe and chronic infections in humans, mainly localized in immune privileged sites, as the brain and the eye. Monocytes/macrophages are thought to be involved in Acanthamoeba infections, but little is known about how these facultative parasites influence their functions. The aim of this work was to investigate the effects of Acanthamoeba on human monocytes/macrophages, during the early phase of infection. Herein, THP-1 cells, primary human monocytes isolated from peripheral blood and human monocyte-derived macrophages were either co-incubated with trophozoites of a clinical isolate of Acanthamoeba (genotype T4) or stimulated with amoeba-derived cell free conditioned medium. Production of pro-inflammatory cytokines (TNF-α, IL-6, IL-12), anti-inflammatory cytokine (IL-10) and chemokine (IL-8) was evaluated at specific hours post-stimulation (ranging from 1.30 h to 23 h). We showed that both Acanthamoeba trophozoites and soluble amoebic products induce an early anti-inflammatory monocyte-macrophage phenotype, characterized by a significant production of IL-10; furthermore, challenge with either trophozoites or their soluble metabolites stimulate both pro-inflammatory cytokines and chemokine production, suggesting that this protozoan infection may result from the early induction of coexisting, opposed immune responses. Results reported in this paper confirm that the production of pro-inflammatory cytokines and chemokines by monocytes and macrophages can play a role in the development of the inflammatory response during Acanthamoeba infections. Furthermore, we demonstrate for the first time that Acanthamoeba stimulates IL-10 production in human innate immune cells, which might both promote the immune evasion of Acanthamoeba and limit the induced inflammatory response.",
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Acanthamoeba castellanii (Genotype T4) Stimulates the Production of Interleukin-10 as well as Pro-inflammatory Cytokines in THP-1 Cells, Human Peripheral Blood Mononuclear Cells and Human Monocyte-Derived Macrophages. / Mattana, Antonella; Sanna, Manuela; Cano, Antonella; Delogu, Giuseppe; Erre, Giuseppe; Roberts, Craig W.; Henriquez, Fiona ; Fiori, Pier Luigi; Cappuccinelli, Piero.

In: Infection and immunity, Vol. 84, No. 10, 10.2016, p. 2953-2962.

Research output: Contribution to journalArticle

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AU - Mattana, Antonella

AU - Sanna, Manuela

AU - Cano, Antonella

AU - Delogu, Giuseppe

AU - Erre, Giuseppe

AU - Roberts, Craig W.

AU - Henriquez, Fiona

AU - Fiori, Pier Luigi

AU - Cappuccinelli, Piero

N1 - Copyright © 2016 Mattana et al.

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DO - 10.1128/IAI.00345-16

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JO - Infection and immunity

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