Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages

Abstract Background The horn fly Haematobia irritans is a blood-sucking ectoparasite responsible for substantial economic loss of livestock. Like other hematophagous arthropods species, the successful blood-feeding of H. irritans is highly dependent on the modulation of the host’s hemostasis and imm...

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Main Authors: Martin Breijo, Eliane Esteves, Bruna Bizzarro, Priscila G. Lara, Josiane B. Assis, Sergio Rocha, Lucía Pastro, Cecilia Fernández, Ana Meikle, Anderson Sá-Nunes
Format: Article
Language:English
Published: BMC 2018-07-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-018-3017-z
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author Martin Breijo
Eliane Esteves
Bruna Bizzarro
Priscila G. Lara
Josiane B. Assis
Sergio Rocha
Lucía Pastro
Cecilia Fernández
Ana Meikle
Anderson Sá-Nunes
author_facet Martin Breijo
Eliane Esteves
Bruna Bizzarro
Priscila G. Lara
Josiane B. Assis
Sergio Rocha
Lucía Pastro
Cecilia Fernández
Ana Meikle
Anderson Sá-Nunes
author_sort Martin Breijo
collection DOAJ
description Abstract Background The horn fly Haematobia irritans is a blood-sucking ectoparasite responsible for substantial economic loss of livestock. Like other hematophagous arthropods species, the successful blood-feeding of H. irritans is highly dependent on the modulation of the host’s hemostasis and immune system. Here, we evaluated the biological activity of hematobin (HTB), a protein recently identified in the H. irritans saliva, on macrophage biology. The goal was to understand the putative interactions between the components of H. irritans saliva and the early host immune responses. Results Thioglycolate-elicited peritoneal macrophages from BALB/c mice were stimulated by lipopolysaccharide (LPS) plus interferon-γ (IFN-γ) in the presence or absence of recombinant HTB. The presence of the salivary protein in the cultures inhibited nitric oxide production and decreased the inducible nitric oxide synthase (iNOS) expression induced by LPS plus IFN-γ. The tumor necrosis factor-α (TNF-α) and interleukin-12p40 (IL-12p40) levels were also reduced in the macrophages pre-incubated with HTB; these findings correlated to the decreased NF-κB expression. The biological activities described here were not associated with changes in annexin V binding to macrophages suggesting that HTB does not induce cell death. In addition, the activity of HTB seems to be specific to macrophages because no changes were observed in lymphocyte proliferation or cytokine production. Conclusions We describe here the first bioactive salivary protein of H. irritans. We characterized its ability to modulate macrophage inflammatory response, and the results can help explain how horn flies modulate the host immune system to feed on blood.
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spelling doaj.art-98f20741a8314aacaff4e1327d57c36d2022-12-21T23:42:25ZengBMCParasites & Vectors1756-33052018-07-0111111110.1186/s13071-018-3017-zHematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophagesMartin Breijo0Eliane Esteves1Bruna Bizzarro2Priscila G. Lara3Josiane B. Assis4Sergio Rocha5Lucía Pastro6Cecilia Fernández7Ana Meikle8Anderson Sá-Nunes9Unidad de Reactivos y Biomodelos de Experimentación, Facultad de Medicina, Universidad de la RepúblicaDepartment of Immunology, Laboratory of Experimental Immunology, Institute of Biomedical Sciences, University of Sao PauloDepartment of Immunology, Laboratory of Experimental Immunology, Institute of Biomedical Sciences, University of Sao PauloDepartment of Immunology, Laboratory of Experimental Immunology, Institute of Biomedical Sciences, University of Sao PauloDepartment of Immunology, Laboratory of Experimental Immunology, Institute of Biomedical Sciences, University of Sao PauloUnidad de Reactivos y Biomodelos de Experimentación, Facultad de Medicina, Universidad de la RepúblicaLaboratorio de Interacciones Moleculares, Facultad de Ciencias, Universidad de la RepúblicaCátedra de Inmunología, Facultad de Química, Universidad de la RepúblicaLaboratorio de Técnicas Nucleares, Facultad de Veterinaria, Universidad de la RepúblicaDepartment of Immunology, Laboratory of Experimental Immunology, Institute of Biomedical Sciences, University of Sao PauloAbstract Background The horn fly Haematobia irritans is a blood-sucking ectoparasite responsible for substantial economic loss of livestock. Like other hematophagous arthropods species, the successful blood-feeding of H. irritans is highly dependent on the modulation of the host’s hemostasis and immune system. Here, we evaluated the biological activity of hematobin (HTB), a protein recently identified in the H. irritans saliva, on macrophage biology. The goal was to understand the putative interactions between the components of H. irritans saliva and the early host immune responses. Results Thioglycolate-elicited peritoneal macrophages from BALB/c mice were stimulated by lipopolysaccharide (LPS) plus interferon-γ (IFN-γ) in the presence or absence of recombinant HTB. The presence of the salivary protein in the cultures inhibited nitric oxide production and decreased the inducible nitric oxide synthase (iNOS) expression induced by LPS plus IFN-γ. The tumor necrosis factor-α (TNF-α) and interleukin-12p40 (IL-12p40) levels were also reduced in the macrophages pre-incubated with HTB; these findings correlated to the decreased NF-κB expression. The biological activities described here were not associated with changes in annexin V binding to macrophages suggesting that HTB does not induce cell death. In addition, the activity of HTB seems to be specific to macrophages because no changes were observed in lymphocyte proliferation or cytokine production. Conclusions We describe here the first bioactive salivary protein of H. irritans. We characterized its ability to modulate macrophage inflammatory response, and the results can help explain how horn flies modulate the host immune system to feed on blood.http://link.springer.com/article/10.1186/s13071-018-3017-zHaematobia irritansSalivaHematobinMacrophagesInflammationImmunomodulatory activity
spellingShingle Martin Breijo
Eliane Esteves
Bruna Bizzarro
Priscila G. Lara
Josiane B. Assis
Sergio Rocha
Lucía Pastro
Cecilia Fernández
Ana Meikle
Anderson Sá-Nunes
Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
Parasites & Vectors
Haematobia irritans
Saliva
Hematobin
Macrophages
Inflammation
Immunomodulatory activity
title Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
title_full Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
title_fullStr Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
title_full_unstemmed Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
title_short Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages
title_sort hematobin is a novel immunomodulatory protein from the saliva of the horn fly haematobia irritans that inhibits the inflammatory response in murine macrophages
topic Haematobia irritans
Saliva
Hematobin
Macrophages
Inflammation
Immunomodulatory activity
url http://link.springer.com/article/10.1186/s13071-018-3017-z
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