Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice

Geraldyne A. Salazar, Hernán F. Peñaloza, Catalina Pardo-Roa, Bárbara M. Schultz, Natalia Muñoz-Durango, Roberto S. Gómez, Francisco J. Salazar, Daniela P. Pizarro, Claudia A. Riedel, Pablo A. González, Manuel Alvarez-Lobos, Alexis M. Kalergis, Susan M. Bueno

Resultado de la investigación: Article

8 Citas (Scopus)

Resumen

Salmonella enterica serovar Typhimurium (S. Typhimurium) is a Gram-negative bacterium that produces disease in numerous hosts. In mice, oral inoculation is followed by intestinal colonization and subsequent systemic dissemination, which leads to severe pathogenesis without the activation of an efficient anti-Salmonella immune response. This feature suggests that the infection caused by S. Typhimurium may promote the production of anti-inflammatory molecules by the host that prevent efficient T cell activation and bacterial clearance. In this study, we describe the contribution of immune cells producing the anti-inflammatory cytokine interleukin-10 (IL-10) to the systemic infection caused by S. Typhimurium in mice. We observed that the production of IL-10 was required by S. Typhimurium to cause a systemic disease, since mice lacking IL-10 (IL-10-/-) were significantly more resistant to die after an infection as compared to wild-type (WT) mice. IL-10-/- mice had reduced bacterial loads in internal organs and increased levels of pro-inflammatory cytokines in serum at 5 days of infection. Importantly, WT mice showed high bacterial loads in tissues and no increase of cytokines in serum after 5 days of S. Typhimurium infection, except for IL-10. In WT mice, we observed a peak of il-10 messenger RNA production in ileum, spleen, and liver after 5 days of infection. Importantly, the adoptive transfer of T or B cells from WT mice restored the susceptibility of IL-10-/- mice to systemic S. Typhimurium infection, suggesting that the generation of regulatory cells in vivo is required to sustain a systemic infection by S. Typhimurium. These findings support the notion that IL-10 production from lymphoid cells is a key process in the infective cycle of S. Typhimurium in mice due to generation of a tolerogenic immune response that prevents bacterial clearance and supports systemic dissemination.

Idioma originalEnglish
Número de artículo889
PublicaciónFrontiers in Immunology
Volumen8
N.ºAUG
DOI
EstadoPublished - 2 ago 2017

Huella dactilar

Salmonella enterica
Interleukin-10
B-Lymphocytes
T-Lymphocytes
Infection
Bacterial Load
Cytokines
Anti-Inflammatory Agents
Serogroup
Adoptive Transfer
Gram-Negative Bacteria
Serum
Ileum
Salmonella
Spleen
Lymphocytes
Messenger RNA

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Citar esto

Salazar, G. A., Peñaloza, H. F., Pardo-Roa, C., Schultz, B. M., Muñoz-Durango, N., Gómez, R. S., ... Bueno, S. M. (2017). Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice. Frontiers in Immunology, 8(AUG), [889]. https://doi.org/10.3389/fimmu.2017.00889
Salazar, Geraldyne A. ; Peñaloza, Hernán F. ; Pardo-Roa, Catalina ; Schultz, Bárbara M. ; Muñoz-Durango, Natalia ; Gómez, Roberto S. ; Salazar, Francisco J. ; Pizarro, Daniela P. ; Riedel, Claudia A. ; González, Pablo A. ; Alvarez-Lobos, Manuel ; Kalergis, Alexis M. ; Bueno, Susan M. / Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice. En: Frontiers in Immunology. 2017 ; Vol. 8, N.º AUG.
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title = "Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice",
abstract = "Salmonella enterica serovar Typhimurium (S. Typhimurium) is a Gram-negative bacterium that produces disease in numerous hosts. In mice, oral inoculation is followed by intestinal colonization and subsequent systemic dissemination, which leads to severe pathogenesis without the activation of an efficient anti-Salmonella immune response. This feature suggests that the infection caused by S. Typhimurium may promote the production of anti-inflammatory molecules by the host that prevent efficient T cell activation and bacterial clearance. In this study, we describe the contribution of immune cells producing the anti-inflammatory cytokine interleukin-10 (IL-10) to the systemic infection caused by S. Typhimurium in mice. We observed that the production of IL-10 was required by S. Typhimurium to cause a systemic disease, since mice lacking IL-10 (IL-10-/-) were significantly more resistant to die after an infection as compared to wild-type (WT) mice. IL-10-/- mice had reduced bacterial loads in internal organs and increased levels of pro-inflammatory cytokines in serum at 5 days of infection. Importantly, WT mice showed high bacterial loads in tissues and no increase of cytokines in serum after 5 days of S. Typhimurium infection, except for IL-10. In WT mice, we observed a peak of il-10 messenger RNA production in ileum, spleen, and liver after 5 days of infection. Importantly, the adoptive transfer of T or B cells from WT mice restored the susceptibility of IL-10-/- mice to systemic S. Typhimurium infection, suggesting that the generation of regulatory cells in vivo is required to sustain a systemic infection by S. Typhimurium. These findings support the notion that IL-10 production from lymphoid cells is a key process in the infective cycle of S. Typhimurium in mice due to generation of a tolerogenic immune response that prevents bacterial clearance and supports systemic dissemination.",
keywords = "B cells, Dendritic cells, Interleukin-10, Macrophages, Regulatory T cells, Salmonella enterica serovar Typhimurium, Systemic infection, T cells",
author = "Salazar, {Geraldyne A.} and Pe{\~n}aloza, {Hern{\'a}n F.} and Catalina Pardo-Roa and Schultz, {B{\'a}rbara M.} and Natalia Mu{\~n}oz-Durango and G{\'o}mez, {Roberto S.} and Salazar, {Francisco J.} and Pizarro, {Daniela P.} and Riedel, {Claudia A.} and Gonz{\'a}lez, {Pablo A.} and Manuel Alvarez-Lobos and Kalergis, {Alexis M.} and Bueno, {Susan M.}",
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Salazar, GA, Peñaloza, HF, Pardo-Roa, C, Schultz, BM, Muñoz-Durango, N, Gómez, RS, Salazar, FJ, Pizarro, DP, Riedel, CA, González, PA, Alvarez-Lobos, M, Kalergis, AM & Bueno, SM 2017, 'Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice', Frontiers in Immunology, vol. 8, n.º AUG, 889. https://doi.org/10.3389/fimmu.2017.00889

Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice. / Salazar, Geraldyne A.; Peñaloza, Hernán F.; Pardo-Roa, Catalina; Schultz, Bárbara M.; Muñoz-Durango, Natalia; Gómez, Roberto S.; Salazar, Francisco J.; Pizarro, Daniela P.; Riedel, Claudia A.; González, Pablo A.; Alvarez-Lobos, Manuel; Kalergis, Alexis M.; Bueno, Susan M.

En: Frontiers in Immunology, Vol. 8, N.º AUG, 889, 02.08.2017.

Resultado de la investigación: Article

TY - JOUR

T1 - Interleukin-10 production by T and B cells is a key factor to promote systemic Salmonella enterica serovar typhimurium infection in mice

AU - Salazar, Geraldyne A.

AU - Peñaloza, Hernán F.

AU - Pardo-Roa, Catalina

AU - Schultz, Bárbara M.

AU - Muñoz-Durango, Natalia

AU - Gómez, Roberto S.

AU - Salazar, Francisco J.

AU - Pizarro, Daniela P.

AU - Riedel, Claudia A.

AU - González, Pablo A.

AU - Alvarez-Lobos, Manuel

AU - Kalergis, Alexis M.

AU - Bueno, Susan M.

PY - 2017/8/2

Y1 - 2017/8/2

N2 - Salmonella enterica serovar Typhimurium (S. Typhimurium) is a Gram-negative bacterium that produces disease in numerous hosts. In mice, oral inoculation is followed by intestinal colonization and subsequent systemic dissemination, which leads to severe pathogenesis without the activation of an efficient anti-Salmonella immune response. This feature suggests that the infection caused by S. Typhimurium may promote the production of anti-inflammatory molecules by the host that prevent efficient T cell activation and bacterial clearance. In this study, we describe the contribution of immune cells producing the anti-inflammatory cytokine interleukin-10 (IL-10) to the systemic infection caused by S. Typhimurium in mice. We observed that the production of IL-10 was required by S. Typhimurium to cause a systemic disease, since mice lacking IL-10 (IL-10-/-) were significantly more resistant to die after an infection as compared to wild-type (WT) mice. IL-10-/- mice had reduced bacterial loads in internal organs and increased levels of pro-inflammatory cytokines in serum at 5 days of infection. Importantly, WT mice showed high bacterial loads in tissues and no increase of cytokines in serum after 5 days of S. Typhimurium infection, except for IL-10. In WT mice, we observed a peak of il-10 messenger RNA production in ileum, spleen, and liver after 5 days of infection. Importantly, the adoptive transfer of T or B cells from WT mice restored the susceptibility of IL-10-/- mice to systemic S. Typhimurium infection, suggesting that the generation of regulatory cells in vivo is required to sustain a systemic infection by S. Typhimurium. These findings support the notion that IL-10 production from lymphoid cells is a key process in the infective cycle of S. Typhimurium in mice due to generation of a tolerogenic immune response that prevents bacterial clearance and supports systemic dissemination.

AB - Salmonella enterica serovar Typhimurium (S. Typhimurium) is a Gram-negative bacterium that produces disease in numerous hosts. In mice, oral inoculation is followed by intestinal colonization and subsequent systemic dissemination, which leads to severe pathogenesis without the activation of an efficient anti-Salmonella immune response. This feature suggests that the infection caused by S. Typhimurium may promote the production of anti-inflammatory molecules by the host that prevent efficient T cell activation and bacterial clearance. In this study, we describe the contribution of immune cells producing the anti-inflammatory cytokine interleukin-10 (IL-10) to the systemic infection caused by S. Typhimurium in mice. We observed that the production of IL-10 was required by S. Typhimurium to cause a systemic disease, since mice lacking IL-10 (IL-10-/-) were significantly more resistant to die after an infection as compared to wild-type (WT) mice. IL-10-/- mice had reduced bacterial loads in internal organs and increased levels of pro-inflammatory cytokines in serum at 5 days of infection. Importantly, WT mice showed high bacterial loads in tissues and no increase of cytokines in serum after 5 days of S. Typhimurium infection, except for IL-10. In WT mice, we observed a peak of il-10 messenger RNA production in ileum, spleen, and liver after 5 days of infection. Importantly, the adoptive transfer of T or B cells from WT mice restored the susceptibility of IL-10-/- mice to systemic S. Typhimurium infection, suggesting that the generation of regulatory cells in vivo is required to sustain a systemic infection by S. Typhimurium. These findings support the notion that IL-10 production from lymphoid cells is a key process in the infective cycle of S. Typhimurium in mice due to generation of a tolerogenic immune response that prevents bacterial clearance and supports systemic dissemination.

KW - B cells

KW - Dendritic cells

KW - Interleukin-10

KW - Macrophages

KW - Regulatory T cells

KW - Salmonella enterica serovar Typhimurium

KW - Systemic infection

KW - T cells

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U2 - 10.3389/fimmu.2017.00889

DO - 10.3389/fimmu.2017.00889

M3 - Article

AN - SCOPUS:85026731050

VL - 8

JO - Frontiers in Immunology

JF - Frontiers in Immunology

SN - 1664-3224

IS - AUG

M1 - 889

ER -