Auranofin is active against Histoplasma capsulatum and reduces the expression of virulence-related genes

PLoS Negl Trop Dis. 2024 Oct 7;18(10):e0012586. doi: 10.1371/journal.pntd.0012586. eCollection 2024 Oct.

Abstract

Background: Auranofin is an approved anti-rheumatic drug that has a broad-range inhibitory action against several microorganisms, including human pathogenic fungi. The auranofin activity against Histoplasma capsulatum, the dimorphic fungus that causes histoplasmosis, has not been properly addressed. Since there are few therapeutic options for this life-threatening systemic mycosis, this study evaluated the effects of auranofin on H. capsulatum growth and expression of virulence factors.

Methodology/principal findings: Minimal inhibitory and fungicidal concentrations (MIC and MFC, respectively) of auranofin against 15 H. capsulatum strains with distinct genetic backgrounds were determined using the yeast form of the fungus and a microdilution protocol. Auranofin activity was also assessed on a macrophage model of infection and on a Tenebrio molitor invertebrate animal model. Expression of virulence-related genes was compared between auranofin treated and untreated H. capsulatum yeast cells using a quantitative PCR assay. Auranofin affected the growth of different strains of H. capsulatum, with MIC and MFC values ranging from 1.25 to 5.0 μM and from 2.5 to >10 μM, respectively. Auranofin was able to kill intracellular H. capsulatum yeast cells and conferred protection against the fungus in the experimental animal model of infection. Moreover, the expression of catalase A, HSP70, superoxide dismutase, thioredoxin reductase, serine proteinase, cytochrome C peroxidase, histone 2B, formamidase, metallopeptidase, Y20 and YPS3 proteins were reduced after six hours of auranofin treatment. CONCLUSIONS/SIGNIFICANCE: Auranofin is fungicidal against H. capsulatum and reduces the expression of several virulence-related genes, which makes this anti-rheumatic drug a good candidate for new medicines against histoplasmosis.

MeSH terms

  • Animals
  • Antifungal Agents* / pharmacology
  • Auranofin* / pharmacology
  • Disease Models, Animal
  • Histoplasma* / drug effects
  • Histoplasma* / genetics
  • Histoplasma* / pathogenicity
  • Histoplasmosis / drug therapy
  • Histoplasmosis / microbiology
  • Humans
  • Macrophages / drug effects
  • Macrophages / microbiology
  • Mice
  • Microbial Sensitivity Tests*
  • Tenebrio / microbiology
  • Virulence / drug effects
  • Virulence Factors / genetics

Substances

  • Auranofin
  • Antifungal Agents
  • Virulence Factors

Grants and funding

This study was supported by a grant from an international Tripartite Fiocruz/USP/Pasteur initiative to R.A.-P., C.P.T., and A.A. The study has also received financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grant number 403627/2023-0 and Programa Jovens Pesquisadores (INI/Fiocruz), grant number INI-003-FIO-19-2-7 (both to R.A.-P.). R.M.Z-O is supported in part by CNPq, grant number 308315/2021-9 and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), grant number E-26/200.381/2023. R.A.-P. is supported in part by CNPq, grant number 307171/2023-0, and FAPERJ, grant number E-26/201.441/2021. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.