Frontiers in Immunology (Nov 2018)
Lutzomyia longipalpis Saliva Induces Heme Oxygenase-1 Expression at Bite Sites
- Nivea F. Luz,
- Thiago DeSouza-Vieira,
- Waldione De Castro,
- Aislan Carvalho Vivarini,
- Lais Pereira,
- Riam Rocha França,
- Riam Rocha França,
- Paulo S. Silveira-Mattos,
- Paulo S. Silveira-Mattos,
- Diego L. Costa,
- Clarissa Teixeira,
- Claudio Meneses,
- Viviane S. Boaventura,
- Viviane S. Boaventura,
- Camila I. de Oliveira,
- Camila I. de Oliveira,
- Ulisses Gazos Lopes,
- Naomi Aronson,
- Bruno B. Andrade,
- Bruno B. Andrade,
- Bruno B. Andrade,
- Claudia I. Brodskyn,
- Claudia I. Brodskyn,
- Jesus G. Valenzuela,
- Shaden Kamhawi,
- Valeria M. Borges,
- Valeria M. Borges
Affiliations
- Nivea F. Luz
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Thiago DeSouza-Vieira
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Waldione De Castro
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Aislan Carvalho Vivarini
- Laboratory of Molecular Parasitology, Center of Health Science, Carlos Chagas Filho Biophysics Institute, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
- Lais Pereira
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Riam Rocha França
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Riam Rocha França
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Paulo S. Silveira-Mattos
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Paulo S. Silveira-Mattos
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Diego L. Costa
- Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United States
- Clarissa Teixeira
- Oswaldo Cruz Foundation (Fiocruz-PI), Teresina, Brazil
- Claudio Meneses
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Viviane S. Boaventura
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Viviane S. Boaventura
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Camila I. de Oliveira
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Camila I. de Oliveira
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Ulisses Gazos Lopes
- Laboratory of Molecular Parasitology, Center of Health Science, Carlos Chagas Filho Biophysics Institute, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
- Naomi Aronson
- Infectious Diseases Division, Uniformed Services University of the Health Sciences, Bethesda, MD, United States
- Bruno B. Andrade
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Bruno B. Andrade
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Bruno B. Andrade
- Multinational Organization Network Sponsoring Translational and Epidemiological Research Initiative, Fundação José Silveira, Salvador, Brazil
- Claudia I. Brodskyn
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Claudia I. Brodskyn
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- Jesus G. Valenzuela
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Shaden Kamhawi
- Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Valeria M. Borges
- Gonçalo Moniz Institute, Oswaldo Cruz Foundation, Salvador, Brazil
- Valeria M. Borges
- Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, Brazil
- DOI
- https://doi.org/10.3389/fimmu.2018.02779
- Journal volume & issue
-
Vol. 9
Abstract
Sand flies bite mammalian hosts to obtain a blood meal, driving changes in the host inflammatory response that support the establishment of Leishmania infection. This effect is partially attributed to components of sand fly saliva, which are able to recruit and activate leukocytes. Our group has shown that heme oxygenase-1 (HO-1) favors Leishmania survival in infected cells by reducing inflammatory responses. Here, we show that exposure to sand fly bites is associated with induction of HO-1 in vivo. Histopathological analyses of skin specimens from human volunteers experimentally exposed to sand fly bites revealed that HO-1 and Nrf2 are produced at bite sites in the skin. These results were recapitulated in mice ears injected with a salivary gland sonicate (SGS) or exposed to sand fly bites, indicating that vector saliva may be a key factor in triggering HO-1 expression. Resident skin macrophages were the main source HO-1 at 24–48 h after bites. Additionally, assays in vivo after bites and in vitro after stimulation with saliva both demonstrated that HO-1 production by macrophages was Nrf2-dependent. Collectively, our data demonstrates that vector saliva induces early HO-1 production at the bite sites, representing a major event associated with establishment of naturally-transmitted Leishmania infections.
Keywords
