Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes

Sif Gudbrandsdottir; Hans C Hasselbalch; Claus H Nielsen

doi:10.4049/jimmunol.1201103

Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes

Sif Gudbrandsdottir, Hans C Hasselbalch, Claus H Nielsen

Section 01 - Prosthetics

66 Citations (Scopus)

Abstract

Activated platelets are known to modulate immune responses by secreting or shedding a range of immunomodulatory substances. We examined the influence of activated platelets on cytokine production by normal human mononuclear cells, induced by tetanus toxoid (TT), human thyroglobulin (TG),Escherichia coliLPS, or intactPorphyromonas gingivalis. Addition of platelets activated by thrombin-receptor-Activating peptide enhanced IL-10 production induced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis (p< 0.01), and reduced the production of TNF-αinduced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis(p< 0.001), and of IL-6 in LPS- andP. gingivalis-stimulated cultures (p< 0.001). Similar effects on IL-10 and TNF-αproduction were observed on addition of platelet supernatant to mononuclear cells, whereas addition of recombinant soluble CD40L mimicked the effects on IL-10 production. Moreover, Ab-mediated blockade of CD40L counteracted the effect of platelets and platelet supernatants on TNF-αproduction. Monocytes separated into two populations with respect to IL-10 production induced by TG; the high-secreting fraction increased from 0.8 to 2.1% (p< 0.001) on addition of activated platelets. Adherence of platelets increased TG- and TTinduced IL-10 secretion by monocytes (p< 0.05). In addition, activated platelets inhibited CD4 ⁺ T cell proliferation elicited by TT (p< 0.001) andP. gingivalis(p< 0.001). Our findings suggest that activated platelets have anti-inflammatory properties related to the interaction between CD40L and CD40, and exert a hitherto undescribed immunoregulatory action by enhancing IL-10 production and inhibiting TNF-αproduction by monocytes.

Original language	English
Journal	Journal of immunology (Baltimore, Md. : 1950)
Volume	191
Issue number	8
Pages (from-to)	4059-67
Number of pages	9
ISSN	0022-1767
DOIs	https://doi.org/10.4049/jimmunol.1201103
Publication status	Published - 15 Oct 2013

Keywords

Antigens, CD40
Blood Platelets
CD4-Positive T-Lymphocytes
CD40 Ligand
Cell Proliferation
Cells, Cultured
Humans
Inflammation
Interleukin-10
Lipopolysaccharides
Monocytes
Platelet Activation
Porphyromonas gingivalis
Tetanus Toxin
Thyroglobulin
Tumor Necrosis Factor-alpha

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10.4049/jimmunol.1201103

https://www.jimmunol.org/content/jimmunol/191/8/4059.full.pdf

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@article{448526f5ce0149519ade42ef2f33e6c8,

title = "Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes",

abstract = "Activated platelets are known to modulate immune responses by secreting or shedding a range of immunomodulatory substances. We examined the influence of activated platelets on cytokine production by normal human mononuclear cells, induced by tetanus toxoid (TT), human thyroglobulin (TG),Escherichia coliLPS, or intactPorphyromonas gingivalis. Addition of platelets activated by thrombin-receptor-Activating peptide enhanced IL-10 production induced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis (p< 0.01), and reduced the production of TNF-αinduced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis(p< 0.001), and of IL-6 in LPS- andP. gingivalis-stimulated cultures (p< 0.001). Similar effects on IL-10 and TNF-αproduction were observed on addition of platelet supernatant to mononuclear cells, whereas addition of recombinant soluble CD40L mimicked the effects on IL-10 production. Moreover, Ab-mediated blockade of CD40L counteracted the effect of platelets and platelet supernatants on TNF-αproduction. Monocytes separated into two populations with respect to IL-10 production induced by TG; the high-secreting fraction increased from 0.8 to 2.1% (p< 0.001) on addition of activated platelets. Adherence of platelets increased TG- and TTinduced IL-10 secretion by monocytes (p< 0.05). In addition, activated platelets inhibited CD4 + T cell proliferation elicited by TT (p< 0.001) andP. gingivalis(p< 0.001). Our findings suggest that activated platelets have anti-inflammatory properties related to the interaction between CD40L and CD40, and exert a hitherto undescribed immunoregulatory action by enhancing IL-10 production and inhibiting TNF-αproduction by monocytes.",

keywords = "Antigens, CD40, Blood Platelets, CD4-Positive T-Lymphocytes, CD40 Ligand, Cell Proliferation, Cells, Cultured, Humans, Inflammation, Interleukin-10, Lipopolysaccharides, Monocytes, Platelet Activation, Porphyromonas gingivalis, Tetanus Toxin, Thyroglobulin, Tumor Necrosis Factor-alpha",

author = "Sif Gudbrandsdottir and Hasselbalch, {Hans C} and Nielsen, {Claus H}",

year = "2013",

month = oct,

day = "15",

doi = "10.4049/jimmunol.1201103",

language = "English",

volume = "191",

pages = "4059--67",

journal = "Journal of immunology (Baltimore, Md. : 1950)",

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publisher = "American Association of Immunologists",

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TY - JOUR

T1 - Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes

AU - Gudbrandsdottir, Sif

AU - Hasselbalch, Hans C

AU - Nielsen, Claus H

PY - 2013/10/15

Y1 - 2013/10/15

N2 - Activated platelets are known to modulate immune responses by secreting or shedding a range of immunomodulatory substances. We examined the influence of activated platelets on cytokine production by normal human mononuclear cells, induced by tetanus toxoid (TT), human thyroglobulin (TG),Escherichia coliLPS, or intactPorphyromonas gingivalis. Addition of platelets activated by thrombin-receptor-Activating peptide enhanced IL-10 production induced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis (p< 0.01), and reduced the production of TNF-αinduced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis(p< 0.001), and of IL-6 in LPS- andP. gingivalis-stimulated cultures (p< 0.001). Similar effects on IL-10 and TNF-αproduction were observed on addition of platelet supernatant to mononuclear cells, whereas addition of recombinant soluble CD40L mimicked the effects on IL-10 production. Moreover, Ab-mediated blockade of CD40L counteracted the effect of platelets and platelet supernatants on TNF-αproduction. Monocytes separated into two populations with respect to IL-10 production induced by TG; the high-secreting fraction increased from 0.8 to 2.1% (p< 0.001) on addition of activated platelets. Adherence of platelets increased TG- and TTinduced IL-10 secretion by monocytes (p< 0.05). In addition, activated platelets inhibited CD4 + T cell proliferation elicited by TT (p< 0.001) andP. gingivalis(p< 0.001). Our findings suggest that activated platelets have anti-inflammatory properties related to the interaction between CD40L and CD40, and exert a hitherto undescribed immunoregulatory action by enhancing IL-10 production and inhibiting TNF-αproduction by monocytes.

AB - Activated platelets are known to modulate immune responses by secreting or shedding a range of immunomodulatory substances. We examined the influence of activated platelets on cytokine production by normal human mononuclear cells, induced by tetanus toxoid (TT), human thyroglobulin (TG),Escherichia coliLPS, or intactPorphyromonas gingivalis. Addition of platelets activated by thrombin-receptor-Activating peptide enhanced IL-10 production induced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis (p< 0.01), and reduced the production of TNF-αinduced by LPS (p< 0.001), TG (p< 0.05), andP. gingivalis(p< 0.001), and of IL-6 in LPS- andP. gingivalis-stimulated cultures (p< 0.001). Similar effects on IL-10 and TNF-αproduction were observed on addition of platelet supernatant to mononuclear cells, whereas addition of recombinant soluble CD40L mimicked the effects on IL-10 production. Moreover, Ab-mediated blockade of CD40L counteracted the effect of platelets and platelet supernatants on TNF-αproduction. Monocytes separated into two populations with respect to IL-10 production induced by TG; the high-secreting fraction increased from 0.8 to 2.1% (p< 0.001) on addition of activated platelets. Adherence of platelets increased TG- and TTinduced IL-10 secretion by monocytes (p< 0.05). In addition, activated platelets inhibited CD4 + T cell proliferation elicited by TT (p< 0.001) andP. gingivalis(p< 0.001). Our findings suggest that activated platelets have anti-inflammatory properties related to the interaction between CD40L and CD40, and exert a hitherto undescribed immunoregulatory action by enhancing IL-10 production and inhibiting TNF-αproduction by monocytes.

KW - Antigens, CD40

KW - Blood Platelets

KW - CD4-Positive T-Lymphocytes

KW - CD40 Ligand

KW - Cell Proliferation

KW - Cells, Cultured

KW - Humans

KW - Inflammation

KW - Interleukin-10

KW - Lipopolysaccharides

KW - Monocytes

KW - Platelet Activation

KW - Porphyromonas gingivalis

KW - Tetanus Toxin

KW - Thyroglobulin

KW - Tumor Necrosis Factor-alpha

U2 - 10.4049/jimmunol.1201103

DO - 10.4049/jimmunol.1201103

M3 - Journal article

C2 - 24048901

SN - 0022-1767

VL - 191

SP - 4059

EP - 4067

JO - Journal of immunology (Baltimore, Md. : 1950)

JF - Journal of immunology (Baltimore, Md. : 1950)

IS - 8

ER -

Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes

Abstract

Keywords

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