Ixodes ricinus tick salivary gland extract inhibits IL-10 secretion and CD69 expression by mitogen-stimulated murine splenocytes and induces hyporesponsiveness in B lymphocytes

Sigrid Hannier, Janet Mary Liversidge, Jeremy M Sternberg, Alan Stuart Bowman (Corresponding Author)

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42 Citations (Scopus)

Abstract

Tick saliva contains immunosuppressive factors allowing this blood-feeding ectoparasite to remain on hosts and enhancing pathogen transmission. In this study, we examined the modulation of mitogen-induced activation of naive murine splenocytes by the saliva and salivary gland extract (SGE) of I. ricinus ticks. We found that saliva-specific factors reduced IL-10 production by both concanavalin A (ConA) and lipopolysaccharide (LPS) stimulated splenocytes. The LPS-induced IL-10 production is 10 times more sensitive to SGE than the ConA-induced IL-10 production. Flow cytometric analysis determined that SGE particularly inhibited B (B220 (+) ) cell IL-10 production in mitogen-stimulated splenocyte preparations. Moreover, SGE reduced the early activation marker CD69 expression on ConA-activated T cells and also on B cells in presence of ConA or LPS. Annexin V and Via-probe staining demonstrated that SGE did not increase cell death in activated splenocytes and slightly decreased apoptosis in B lymphocytes. By employing assays with isolated B cells, we further showed that SGE had a direct effect on B cells and inhibited LPS-induced B cell proliferation. Taken together, our results indicate that salivary immunomodulators induce hyporesponsiveness to mitogen in both T and B cells, and that a direct B-cell inhibitory activity is present in tick saliva.

Original languageEnglish
Pages (from-to)27-37
Number of pages10
JournalParasite Immunology
Volume25
Issue number1
DOIs
Publication statusPublished - Jan 2003

Keywords

  • B lymphocytes
  • IL-10
  • immunosuppression
  • Ixodes ricinus
  • salivary glands
  • tick
  • LYME-DISEASE VECTOR
  • BORRELIA-BURGDORFERI
  • IN-VITRO
  • IFN-GAMMA
  • CYTOKINE PRODUCTION
  • CELL ACTIVATION
  • IMMUNE-RESPONSE
  • BALB/C MICE
  • SCAPULARIS
  • PROTEIN

Cite this

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title = "Ixodes ricinus tick salivary gland extract inhibits IL-10 secretion and CD69 expression by mitogen-stimulated murine splenocytes and induces hyporesponsiveness in B lymphocytes",
abstract = "Tick saliva contains immunosuppressive factors allowing this blood-feeding ectoparasite to remain on hosts and enhancing pathogen transmission. In this study, we examined the modulation of mitogen-induced activation of naive murine splenocytes by the saliva and salivary gland extract (SGE) of I. ricinus ticks. We found that saliva-specific factors reduced IL-10 production by both concanavalin A (ConA) and lipopolysaccharide (LPS) stimulated splenocytes. The LPS-induced IL-10 production is 10 times more sensitive to SGE than the ConA-induced IL-10 production. Flow cytometric analysis determined that SGE particularly inhibited B (B220 (+) ) cell IL-10 production in mitogen-stimulated splenocyte preparations. Moreover, SGE reduced the early activation marker CD69 expression on ConA-activated T cells and also on B cells in presence of ConA or LPS. Annexin V and Via-probe staining demonstrated that SGE did not increase cell death in activated splenocytes and slightly decreased apoptosis in B lymphocytes. By employing assays with isolated B cells, we further showed that SGE had a direct effect on B cells and inhibited LPS-induced B cell proliferation. Taken together, our results indicate that salivary immunomodulators induce hyporesponsiveness to mitogen in both T and B cells, and that a direct B-cell inhibitory activity is present in tick saliva.",
keywords = "B lymphocytes, IL-10, immunosuppression, Ixodes ricinus, salivary glands, tick, LYME-DISEASE VECTOR, BORRELIA-BURGDORFERI, IN-VITRO, IFN-GAMMA, CYTOKINE PRODUCTION, CELL ACTIVATION, IMMUNE-RESPONSE, BALB/C MICE, SCAPULARIS, PROTEIN",
author = "Sigrid Hannier and Liversidge, {Janet Mary} and Sternberg, {Jeremy M} and Bowman, {Alan Stuart}",
year = "2003",
month = "1",
doi = "10.1046/j.1365-3024.2003.00605.x",
language = "English",
volume = "25",
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journal = "Parasite Immunology",
issn = "0141-9838",
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TY - JOUR

T1 - Ixodes ricinus tick salivary gland extract inhibits IL-10 secretion and CD69 expression by mitogen-stimulated murine splenocytes and induces hyporesponsiveness in B lymphocytes

AU - Hannier, Sigrid

AU - Liversidge, Janet Mary

AU - Sternberg, Jeremy M

AU - Bowman, Alan Stuart

PY - 2003/1

Y1 - 2003/1

N2 - Tick saliva contains immunosuppressive factors allowing this blood-feeding ectoparasite to remain on hosts and enhancing pathogen transmission. In this study, we examined the modulation of mitogen-induced activation of naive murine splenocytes by the saliva and salivary gland extract (SGE) of I. ricinus ticks. We found that saliva-specific factors reduced IL-10 production by both concanavalin A (ConA) and lipopolysaccharide (LPS) stimulated splenocytes. The LPS-induced IL-10 production is 10 times more sensitive to SGE than the ConA-induced IL-10 production. Flow cytometric analysis determined that SGE particularly inhibited B (B220 (+) ) cell IL-10 production in mitogen-stimulated splenocyte preparations. Moreover, SGE reduced the early activation marker CD69 expression on ConA-activated T cells and also on B cells in presence of ConA or LPS. Annexin V and Via-probe staining demonstrated that SGE did not increase cell death in activated splenocytes and slightly decreased apoptosis in B lymphocytes. By employing assays with isolated B cells, we further showed that SGE had a direct effect on B cells and inhibited LPS-induced B cell proliferation. Taken together, our results indicate that salivary immunomodulators induce hyporesponsiveness to mitogen in both T and B cells, and that a direct B-cell inhibitory activity is present in tick saliva.

AB - Tick saliva contains immunosuppressive factors allowing this blood-feeding ectoparasite to remain on hosts and enhancing pathogen transmission. In this study, we examined the modulation of mitogen-induced activation of naive murine splenocytes by the saliva and salivary gland extract (SGE) of I. ricinus ticks. We found that saliva-specific factors reduced IL-10 production by both concanavalin A (ConA) and lipopolysaccharide (LPS) stimulated splenocytes. The LPS-induced IL-10 production is 10 times more sensitive to SGE than the ConA-induced IL-10 production. Flow cytometric analysis determined that SGE particularly inhibited B (B220 (+) ) cell IL-10 production in mitogen-stimulated splenocyte preparations. Moreover, SGE reduced the early activation marker CD69 expression on ConA-activated T cells and also on B cells in presence of ConA or LPS. Annexin V and Via-probe staining demonstrated that SGE did not increase cell death in activated splenocytes and slightly decreased apoptosis in B lymphocytes. By employing assays with isolated B cells, we further showed that SGE had a direct effect on B cells and inhibited LPS-induced B cell proliferation. Taken together, our results indicate that salivary immunomodulators induce hyporesponsiveness to mitogen in both T and B cells, and that a direct B-cell inhibitory activity is present in tick saliva.

KW - B lymphocytes

KW - IL-10

KW - immunosuppression

KW - Ixodes ricinus

KW - salivary glands

KW - tick

KW - LYME-DISEASE VECTOR

KW - BORRELIA-BURGDORFERI

KW - IN-VITRO

KW - IFN-GAMMA

KW - CYTOKINE PRODUCTION

KW - CELL ACTIVATION

KW - IMMUNE-RESPONSE

KW - BALB/C MICE

KW - SCAPULARIS

KW - PROTEIN

U2 - 10.1046/j.1365-3024.2003.00605.x

DO - 10.1046/j.1365-3024.2003.00605.x

M3 - Article

VL - 25

SP - 27

EP - 37

JO - Parasite Immunology

JF - Parasite Immunology

SN - 0141-9838

IS - 1

ER -