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https://www.arca.fiocruz.br/handle/icict/44586
HEME OXYGENASE-1 INDUCTION BY BLOOD-FEEDING ARTHROPODS CONTROLS SKIN INFLAMMATION AND PROMOTES DISEASE TOLERANCE
Author
Vieira, Thiago de Souza
Iniguez, Eva
Castro, Waldione de
Karmakar, Subir
Disotuar, Maria M.
Cecilio, Pedro
Lacsina, Joshua R.
Meneses, Claudio
Nagata, Bianca M.
Cardoso, Silvia
Sonenshine, Daniel E.
Moore, Ian N.
Borges, Valeria de Matos
Dey, Ranadhir
Soares, Miguel P.
Nakhasi, Hira L.
Oliveira, Fabiano
Valenzuela, Jesus G.
Kamhawi, Shaden
Iniguez, Eva
Castro, Waldione de
Karmakar, Subir
Disotuar, Maria M.
Cecilio, Pedro
Lacsina, Joshua R.
Meneses, Claudio
Nagata, Bianca M.
Cardoso, Silvia
Sonenshine, Daniel E.
Moore, Ian N.
Borges, Valeria de Matos
Dey, Ranadhir
Soares, Miguel P.
Nakhasi, Hira L.
Oliveira, Fabiano
Valenzuela, Jesus G.
Kamhawi, Shaden
Affilliation
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Infectious Disease Pathogenesis Section, Comparative Medicine Branch. Rockville, MD, USA.
Instituto Gulbenkian de Ciência. Oeiras, Lisboa, Portugal.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Infectious Disease Pathogenesis Section. Comparative Medicine Branch. Rockville, MD, USA.
Fundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
Instituto Gulbenkian de Ciência. Oeiras, Lisboa, Portugal.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Infectious Disease Pathogenesis Section, Comparative Medicine Branch. Rockville, MD, USA.
Instituto Gulbenkian de Ciência. Oeiras, Lisboa, Portugal.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Infectious Disease Pathogenesis Section. Comparative Medicine Branch. Rockville, MD, USA.
Fundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
Instituto Gulbenkian de Ciência. Oeiras, Lisboa, Portugal.
Center for Biologics Evaluation and Research. Food and Drug Administration. Laboratory of Emerging Pathogens. Division of Emerging and Transfusion Transmitted Diseases. Silver Spring, MD, USA
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
National Institutes of Health. National Institute of Allergy and Infectious Diseases. Vector Molecular Biology Section, Laboratory of Malaria and Vector Research. Rockville, MD, USA.
Abstract
Hematophagous vectors lacerate host skin and capillaries to acquire a blood meal, resulting in leakage of red blood cells (RBCs) and inflammation. Here, we show that heme oxygenase-1 (HO-1), a pleiotropic cytoprotective isoenzyme that mitigates heme-mediated tissue damage, is induced after bites of sand flies, mosquitoes, and ticks. Further, we demonstrate that erythrophagocytosis by macrophages, including a skinresiding CD163+CD91+ professional iron-recycling subpopulation, produces HO-1 after bites. Importantly, we establish that global deletion or transient inhibition of HO-1 in mice increases inflammation and pathology following Leishmania-infected sand fly bites without affecting parasite number, whereas CO, an end product of the HO-1 enzymatic reaction, suppresses skin inflammation. This indicates that HO-1 induction by bloodfeeding sand flies promotes tolerance to Leishmania infection. Collectively, our data demonstrate that HO-1 induction through erythrophagocytosis is a universal mechanism that regulates skin inflammation following blood feeding by arthropods, thus promoting early-stage disease tolerance to vector-borne pathogens.
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