Nitric Oxide Resistance in Leishmania (Viannia) braziliensis Involves Regulation of Glucose Consumption, Glutathione Metabolism and Abundance of Pentose Phosphate Pathway Enzymes
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In American Tegumentary Leishmaniasis production of cytokines, reactive oxygen species and nitric oxide (NO) by host macrophages normally lead to parasite death. However, some Leishmania braziliensis strains exhibit natural NO resistance. NO-resistant strains cause more lesions and are frequently more resistant to antimonial treatment than NO-susceptible ones, suggesting that NO-resistant parasites are endowed with specific mechanisms of survival and persistence. To tests this, we analyzed the effect of pro- and antioxidant molecules on the infectivity in vitro of L. braziliensis strains exhibiting polar phenotypes of resistance or susceptibility to NO. In addition, we conducted a comprehensive quantitative mass spectrometry-based proteomics analysis of those parasites. NO-resistant parasites were more infective to peritoneal macrophages, even in the presence of high levels of reactive species. Principal component analysis of protein concentration values clearly differentiated NO-resistant from NO-susceptible parasites, suggesting that there are natural intrinsic differences at molecular level among those strains. Upon NO exposure, NO-resistant parasites rapidly modulated their proteome, increasing their total protein content and glutathione (GSH) metabolism. Furthermore, NO-resistant parasites showed increased glucose analogue uptake, and increased abundance of phosphotransferase and G6PDH after nitrosative challenge, which can contribute to NADPH pool maintenance and fuel the reducing conditions for the recovery of GSH upon NO exposure. Thus, increased glucose consumption and GSH-mediated redox capability may explain the natural resistance of L. braziliensis against NO.
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Leishmania is successfully destroyed by •NO.
“Leishmania is also successfully destroyed by •NO [138]”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [138]
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- Authors
- Pinho, N., Bombaça, A. C., Wiśniewski, J. R., Dias-Lopes, G., Saboia-Vahia, L., Cupolillo, E., de Jesus, J. B., de Almeida, R. P., Padrón, G., Menna-Barreto, R., & Cuervo, P.
- Affiliations
- Instituto Oswaldo Cruz (BR)
- Max Planck Institute of Biochemistry (DE)
- Laboratório de Pesquisa em Leishmanioses, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro 21040-360, RJ, Brazil
- Departamento de Medicina, Universidade Federal de São João Del Rei, São João del Rei 35501-296, MG, Brazil
- Department of Medicine, Hospital Universitário, EBSERH, Universidade Federal de Sergipe, Aracaju 49100-000, SE, Brazil
- Laboratório de Biologia Celular, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro 21040-360, RJ, Brazil
- ORCID
- Venue
- Antioxidants
- Publisher
- MDPI AG
- Published
- 2022-01-29
- Volume
- 11
- Issue
- 2
- Pages
- 277
- ISSN
- 2076-3921 (ISSN-L)
- PMC
- PMC8868067
- OpenAlex
- W4210407646
- Cited by
- 21
- References
- 81
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 9 · 2022: 3
- FWCI
- 4.64
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Antioxidants (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arca - Repositório Institucional da Fiocruz (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- National Council for Scientific and Technological Development (Universal grant No. 423300/2018-0, PQ-P.C. Process No. 305796/2017-8 and 312573/2020-0, R.P.A. – PQ Process No. 309776/2018-0)
- Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (P.C. - JCNE E-26/203.253/2017, N.P. - TCT No. E-26/202.464/2017)
- Coordenação de Aperfeicoamento de Pessoal de Nível Superior (Finance Code 001 - P.C. - Process No. 88887.374332/2019-00, G.P. Process No. 0344141)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Epidemiology › Trypanosoma species research and implications
- Keywords
- Leishmania braziliensis, nitric oxide resistance, American tegumentary leishmaniasis, glutathione metabolism, pentose phosphate pathway, glucose utilization, NADPH regeneration, peritoneal macrophages, parasite proteome, glucose-6-phosphate dehydrogenase, antimonial resistance, reactive oxygen species, host-parasite interactions
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