Carp Il10 has anti-inflammatory activities on phagocytes, promotes proliferation of memory T-cells and regulates B-cell differentiation and antibody secretion

M.C. Piazzon de Haro, H.F.J. Savelkoul, D. Pietretti, G. Wiegertjes, M. Forlenza

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Abstract

In the current study, we investigated the effects of carp Il10 on phagocytes and lymphocytes. Carp Il10 shares several prototypical inhibitory activities on phagocytes with mammalian IL-10, including deactivation of neutrophils and macrophages, as shown by inhibition of oxygen and nitrogen radical production, as well as reduced expression of proinflammatory genes and mhc genes involved in Ag presentation. Similar to mammalian IL-10, carp Il10 acts through a signaling pathway involving phosphorylation of Stat3, ultimately leading to the early upregulation of socs3 expression. To our knowledge, this is the first study of the effects of Il10 on lymphocytes in fish. Although Il10 did not affect survival and proliferation of T cells from naive animals, it greatly promoted survival and proliferation of T cells in cultures from immunized animals, but only when used in combination with the immunizing Ag. Preliminary gene expression analysis suggests that, under these circumstances, carp Il10 stimulates a subset of CD8+ memory T cells while downregulating CD4+ memory Th1 and Th2 responses. In addition to the regulatory effect on T cells, carp Il10 stimulates proliferation, differentiation, and Ab secretion by IgM+ B cells. Overall, carp Il10 shares several prototypical activities with mammalian IL-10, including downregulation of the inflammatory response of phagocytes, stimulation of proliferation of subsets of memory T lymphocytes, and proliferation, differentiation, and Ab secretion by IgM+ B lymphocytes. To our knowledge, this is the first comprehensive analysis of biological activities of fish Il10 on both phagocytes and lymphocytes showing functional conservation of several properties of Il10.
Original languageEnglish
Pages (from-to)187-199
JournalThe Journal of Immunology
Volume194
Issue number1
DOIs
Publication statusPublished - 2015

Fingerprint

Carps
Phagocytes
Interleukin-10
Cell Differentiation
B-Lymphocytes
Anti-Inflammatory Agents
T-Lymphocytes
Antibodies
Lymphocytes
Immunoglobulin M
Fishes
Down-Regulation
Gene Expression
T-Lymphocyte Subsets
Reactive Oxygen Species
Neutrophils
Up-Regulation
Nitrogen
Cell Culture Techniques

Keywords

  • carassius-auratus l.
  • inhibits cytokine production
  • trout oncorhynchus-mykiss
  • zebrafish danio-rerio
  • necrosis-factor-alpha
  • mhc class-i
  • cyprinus-carpio
  • common carp
  • expression analysis
  • interleukin-10 receptor

Cite this

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title = "Carp Il10 has anti-inflammatory activities on phagocytes, promotes proliferation of memory T-cells and regulates B-cell differentiation and antibody secretion",
abstract = "In the current study, we investigated the effects of carp Il10 on phagocytes and lymphocytes. Carp Il10 shares several prototypical inhibitory activities on phagocytes with mammalian IL-10, including deactivation of neutrophils and macrophages, as shown by inhibition of oxygen and nitrogen radical production, as well as reduced expression of proinflammatory genes and mhc genes involved in Ag presentation. Similar to mammalian IL-10, carp Il10 acts through a signaling pathway involving phosphorylation of Stat3, ultimately leading to the early upregulation of socs3 expression. To our knowledge, this is the first study of the effects of Il10 on lymphocytes in fish. Although Il10 did not affect survival and proliferation of T cells from naive animals, it greatly promoted survival and proliferation of T cells in cultures from immunized animals, but only when used in combination with the immunizing Ag. Preliminary gene expression analysis suggests that, under these circumstances, carp Il10 stimulates a subset of CD8+ memory T cells while downregulating CD4+ memory Th1 and Th2 responses. In addition to the regulatory effect on T cells, carp Il10 stimulates proliferation, differentiation, and Ab secretion by IgM+ B cells. Overall, carp Il10 shares several prototypical activities with mammalian IL-10, including downregulation of the inflammatory response of phagocytes, stimulation of proliferation of subsets of memory T lymphocytes, and proliferation, differentiation, and Ab secretion by IgM+ B lymphocytes. To our knowledge, this is the first comprehensive analysis of biological activities of fish Il10 on both phagocytes and lymphocytes showing functional conservation of several properties of Il10.",
keywords = "carassius-auratus l., inhibits cytokine production, trout oncorhynchus-mykiss, zebrafish danio-rerio, necrosis-factor-alpha, mhc class-i, cyprinus-carpio, common carp, expression analysis, interleukin-10 receptor",
author = "{Piazzon de Haro}, M.C. and H.F.J. Savelkoul and D. Pietretti and G. Wiegertjes and M. Forlenza",
year = "2015",
doi = "10.4049/jimmunol.1402093",
language = "English",
volume = "194",
pages = "187--199",
journal = "The Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "1",

}

Carp Il10 has anti-inflammatory activities on phagocytes, promotes proliferation of memory T-cells and regulates B-cell differentiation and antibody secretion. / Piazzon de Haro, M.C.; Savelkoul, H.F.J.; Pietretti, D.; Wiegertjes, G.; Forlenza, M.

In: The Journal of Immunology, Vol. 194, No. 1, 2015, p. 187-199.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Carp Il10 has anti-inflammatory activities on phagocytes, promotes proliferation of memory T-cells and regulates B-cell differentiation and antibody secretion

AU - Piazzon de Haro, M.C.

AU - Savelkoul, H.F.J.

AU - Pietretti, D.

AU - Wiegertjes, G.

AU - Forlenza, M.

PY - 2015

Y1 - 2015

N2 - In the current study, we investigated the effects of carp Il10 on phagocytes and lymphocytes. Carp Il10 shares several prototypical inhibitory activities on phagocytes with mammalian IL-10, including deactivation of neutrophils and macrophages, as shown by inhibition of oxygen and nitrogen radical production, as well as reduced expression of proinflammatory genes and mhc genes involved in Ag presentation. Similar to mammalian IL-10, carp Il10 acts through a signaling pathway involving phosphorylation of Stat3, ultimately leading to the early upregulation of socs3 expression. To our knowledge, this is the first study of the effects of Il10 on lymphocytes in fish. Although Il10 did not affect survival and proliferation of T cells from naive animals, it greatly promoted survival and proliferation of T cells in cultures from immunized animals, but only when used in combination with the immunizing Ag. Preliminary gene expression analysis suggests that, under these circumstances, carp Il10 stimulates a subset of CD8+ memory T cells while downregulating CD4+ memory Th1 and Th2 responses. In addition to the regulatory effect on T cells, carp Il10 stimulates proliferation, differentiation, and Ab secretion by IgM+ B cells. Overall, carp Il10 shares several prototypical activities with mammalian IL-10, including downregulation of the inflammatory response of phagocytes, stimulation of proliferation of subsets of memory T lymphocytes, and proliferation, differentiation, and Ab secretion by IgM+ B lymphocytes. To our knowledge, this is the first comprehensive analysis of biological activities of fish Il10 on both phagocytes and lymphocytes showing functional conservation of several properties of Il10.

AB - In the current study, we investigated the effects of carp Il10 on phagocytes and lymphocytes. Carp Il10 shares several prototypical inhibitory activities on phagocytes with mammalian IL-10, including deactivation of neutrophils and macrophages, as shown by inhibition of oxygen and nitrogen radical production, as well as reduced expression of proinflammatory genes and mhc genes involved in Ag presentation. Similar to mammalian IL-10, carp Il10 acts through a signaling pathway involving phosphorylation of Stat3, ultimately leading to the early upregulation of socs3 expression. To our knowledge, this is the first study of the effects of Il10 on lymphocytes in fish. Although Il10 did not affect survival and proliferation of T cells from naive animals, it greatly promoted survival and proliferation of T cells in cultures from immunized animals, but only when used in combination with the immunizing Ag. Preliminary gene expression analysis suggests that, under these circumstances, carp Il10 stimulates a subset of CD8+ memory T cells while downregulating CD4+ memory Th1 and Th2 responses. In addition to the regulatory effect on T cells, carp Il10 stimulates proliferation, differentiation, and Ab secretion by IgM+ B cells. Overall, carp Il10 shares several prototypical activities with mammalian IL-10, including downregulation of the inflammatory response of phagocytes, stimulation of proliferation of subsets of memory T lymphocytes, and proliferation, differentiation, and Ab secretion by IgM+ B lymphocytes. To our knowledge, this is the first comprehensive analysis of biological activities of fish Il10 on both phagocytes and lymphocytes showing functional conservation of several properties of Il10.

KW - carassius-auratus l.

KW - inhibits cytokine production

KW - trout oncorhynchus-mykiss

KW - zebrafish danio-rerio

KW - necrosis-factor-alpha

KW - mhc class-i

KW - cyprinus-carpio

KW - common carp

KW - expression analysis

KW - interleukin-10 receptor

U2 - 10.4049/jimmunol.1402093

DO - 10.4049/jimmunol.1402093

M3 - Article

VL - 194

SP - 187

EP - 199

JO - The Journal of Immunology

JF - The Journal of Immunology

SN - 0022-1767

IS - 1

ER -