Heteroresistance to Itraconazole Alters the Morphology and Increases the Virulence of Cryptococcus gattii
Open accessAbstract
Cryptococcus gattii is the main etiological agent of cryptococcosis in immunocompetent individuals. The triazole drug itraconazole is one of the antifungals used to treat patients with cryptococcosis. Heteroresistance is an adaptive mechanism to counteract the stress of increasing drug concentrations, and it can enhance the ability of a microorganism to survive under antifungal pressure. In this study, we evaluated the ability of 11 C. gattii strains to develop itraconazole heteroresistance. Heteroresistant clones were analyzed for drug susceptibility, alterations in cell diameter, capsule properties, and virulence in a murine model. Heteroresistance to itraconazole was intrinsic in all of the strains analyzed, reduced both the capsule size and the cell diameter, induced molecular heterogeneity at the chromosomal level, changed the negatively charged cells, reduced ergosterol content, and improved the antioxidant system. A positive correlation between surface/volume ratio of original cells and the level of heteroresistance to itraconazole (LHI) was observed in addition to a negative correlation between capsule size of heteroresistant clones and LHI. Moreover, heteroresistance to itraconazole increased the engulfment of C. gattii by macrophages and augmented fungal proliferation inside these cells, which probably accounted for the reduced survival of the mice infected with the heteroresistant clones and the higher fungal burden in lungs and brain. Our results indicate that heteroresistance to itraconazole is intrinsic and increases the virulence of C. gattii . This phenomenon may represent an additional mechanism that contributes to relapses of cryptococcosis in patients during itraconazole therapy.
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Repeated culture in stress-free environments can abolish heteroresistance.
“Repeated culture in stress-free environments can abolish heteroresistance [48].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [48]
The Results report that highly resistant C. gattii subclones returned to their initial itraconazole susceptibility after 10 subcultures in drug-free medium. But the paper also says the original strains exhibited heteroresistance, so the experiment shows loss of the elevated resistance level, not abolition of heteroresistance altogether. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn a mouse model, heteroresistant C. cryptococcus isolates achieve higher fungal burden in different organs.
“For fungi, a mouse model showed that heteroresistant C. cryptococcus isolates suppress the host immune response to enhance evasion, achieve higher fungal burden in different organs, and increase virulence [48,102].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [48]
The Results report significantly higher lung fungal burden and brain colonization in mice infected with heteroresistant clones. However, the studied isolates were C. gattii, not C. cryptococcus, so the species named in the claim is not supported by this paper. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn a mouse model, heteroresistant C. cryptococcus isolates increase virulence.
“For fungi, a mouse model showed that heteroresistant C. cryptococcus isolates suppress the host immune response to enhance evasion, achieve higher fungal burden in different organs, and increase virulence [48,102].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [48]
The Discussion reports that heteroresistant clones were more virulent in mice, and the Results report higher fungal burden in their lungs. However, the studied isolates were C. gattii, not C. cryptococcus as the claim states. (LLM, conf=0.91)
Experimental — accuracy not yet measuredIn a mouse model, heteroresistant C. cryptococcus isolates suppress host immune response to enhance evasion.
“For fungi, a mouse model showed that heteroresistant C. cryptococcus isolates suppress the host immune response to enhance evasion, achieve higher fungal burden in different organs, and increase virulence [48,102].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [48]
The Results report lower inflammatory infiltrate in mice infected with heteroresistant clones, and the Discussion reports higher fungal burden and virulence. However, the study concerns C. gattii, not C. cryptococcus, and reduced inflammation does not establish that the isolates actively suppress host immunity to evade it. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThere are studies showing existence of intrinsic heteroresistance.
“However, there are also studies showing the existence of intrinsic heteroresistance [48,102]”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [48]
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Dornelas, J. C. M., Paixão, V. M., do Carmo, P. H. F., da Costa, M. C., Gomes, E. C. Q., de Resende, M. A., & Santos, D. A. (2024) · Brazilian Journal of Microbiology · doi:10.1007/s42770-024-01440-9
Self-citationColonization of the central nervous system as a key factor in the Cryptococcus gattii pathogenicity
de Freitas, G. J. C., Gouveia‐Eufrásio, L., Emídio, E. C. P., Peres, N. T. A., & Santos, D. A. (2025) · Virulence · doi:10.1080/21505594.2025.2594289
Self-citationde Oliveira, L., Melhem, M. D. S. C., Buccheri, R., Chagas, O. J., Vidal, J. E., & Díaz-Quijano, F. A. (2022) · Figshare · doi:10.6084/m9.figshare.19151184
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Khodashenas, S., Aboualigalehdari, E., Safdarian, M., Rezaei‐Matehkolaei, A., Didehdar, M., & Fatahinia, M. (2026) · Jundishapur Journal of Microbiology · doi:10.5812/jjm-168836
- Authors
- Ferreira, G. F., Santos, J. R. A., Costa, M. C. D., Holanda, R. A. D., Denadai, Â. M. L., Freitas, G. J. C. D., Santos, Á. R. C., Tavares, P. B., Paixão, T. A., & Santos, D. A.
- Affiliations
- Universidade Federal de Juiz de Fora (BR)
- Universidade Federal de Minas Gerais (BR)
- Universidade Vale do Rio Doce (BR)
- ORCID
- Venue
- Antimicrobial Agents and Chemotherapy
- Publisher
- American Society for Microbiology
- Published
- 2015-08
- Volume
- 59
- Issue
- 8
- Pages
- 4600-4609
- ISSN
- 0066-4804 (ISSN-L)
- 1098-6596
- PMC
- PMC4505268
- OpenAlex
- W1846795630
- Cited by
- 44
- References
- 36
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 4 · 2023: 2 · 2022: 4 · 2021: 1 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 9 · 2016: 4
- FWCI
- 4.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Antimicrobial Agents and Chemotherapy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
- Keywords
- Cryptococcus gattii, itraconazole, heteroresistance, intrinsic drug resistance, virulence, cryptococcosis, capsule size, cell diameter, ergosterol, antioxidant defense, macrophage engulfment, surface-to-volume ratio
- MeSH terms
- Animals, Antifungal Agents, Brain, Cryptococcosis, Lung, Macrophages, Male, Mice, Inbred C57BL, Microbial Sensitivity Tests, Virulence, Itraconazole, Drug Resistance, Fungal, Cell Proliferation, Mice, Cryptococcus gattii
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