Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans
Open accessAbstract
Summary: Cryptococcus neoformans is an environmental pathogen requiring atmospheric levels of oxygen for optimal growth. Upon inhalation, C. neoformans disseminates to the brain and causes meningoencephalitis, but the mechanisms by which the pathogen adapts to the low‐oxygen environment in the brain have not been investigated. We found that SRE1, a homologue of the mammalian sterol regulatory element‐binding protein (SREBP), functions in an oxygen‐sensing pathway. Low oxygen decreased sterol synthesis in C. neoformans and triggered activation of membrane‐bound Sre1p by the cleavage‐activating protein, Scp1p. Microarray and Northern blot analysis demonstrated that under low oxygen, Sre1p activates genes required for ergosterol biosynthesis and iron uptake. Consistent with these regulatory functions, sre1 Δ cells were hypersensitive to azole drugs and failed to grow under iron‐limiting conditions. Importantly, sre1 Δ cells failed to produce fulminating brain infection in mice. Our in vitro data support a model in which Sre1p is activated under low oxygen leading to the upregulation of genes required for sterol biosynthesis and growth in a nutrient‐limiting environment. Animal studies confirm the importance of SRE1 for C. neoformans to adapt to the host environment and to cause fatal meningoencephalitis, thereby identifying the SREBP pathway as a therapeutic target for cryptococcosis.
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In A. fumigatus and C. neoformans, expression of cyp51A/ERG11 in response to azole exposure is regulated by the SREBP SrbA and Sre1, respectively.
“In A. fumigatus and C. neoformans, expression of cyp51A /ERG11 in response to azole exposure is regulated by the sterol regulatory element-binding protein (SREBP), SrbA and Sre1, respectively28,29.”
From Molecular mechanisms governing antifungal drug resistance (2023) · cites this paper as [29]
C. neoformans Sre1/Scp1 mutants failed to proliferate in host tissue, failed to cause fatal meningoencephalitis, and displayed hypersensitivity to the azole class of antifungal drugs.
“these mutants also failed to proliferate in host tissue, failed to cause fatal meningoencephalitis, and displayed hypersensitivity to the azole class of antifungal drugs [32],[33]”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
The SREBP pathway mediated by Sre1 and Scp1 in Cryptococcus neoformans is crucial for adaptation to hypoxia and sterol biosynthesis.
“As in fission yeast, the SREBP pathway mediated by Sre1 and Scp1 in C. neoformans was crucial for adaptation to hypoxia and sterol biosynthesis.”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
There is an important link between sterol biosynthesis, hypoxia adaptation, azole drug resistance, and the virulence of pathogenic yeasts.
“Taken together, these observations demonstrate an important link between sterol biosynthesis, hypoxia adaptation, azole drug resistance, and the virulence of pathogenic yeasts.”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
In the yeasts S. pombe and C. neoformans, SREBP homologs are crucial for sterol biosynthesis, survival under hypoxic conditions, resistance to azole antifungal agents, and fungal virulence.
“In the yeasts S. pombe and C. neoformans, SREBP homologs are crucial for sterol biosynthesis, survival under hypoxic conditions, resistance to azole antifungal agents, and fungal virulence [25],[32],[33].”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
Unlike C. neoformans, we did not observe SrbA dependent genes involved in iron or copper uptake in A. fumigatus.
“Unlike C. neoformans, we did not observe SrbA dependent genes involved in iron or copper uptake in A. fumigatus [32].”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
C. neoformans lacks an apparent Insig homolog and the Insig homolog in S. pombe does not appear to be required for regulation of SREBP signalling.
“Interestingly, C. neoformans lacks an apparent Insig homolog and the Insig homolog in S. pombe does not appear to be required for regulation of SREBP signalling [25],[32].”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [32]
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- Authors
- Chang, Y. C., Bien, C. M., Lee, H., Espenshade, P. J., & Kwon‐Chung, K. J.
- Affiliations
- National Institutes of Health (US)
- Johns Hopkins University (US)
- Corresponding author
- Espenshade, Peter J.
- Venue
- Molecular Microbiology
- Publisher
- Wiley
- Published
- 2007-04-24
- Volume
- 64
- Issue
- 3
- Pages
- 614-629
- ISSN
- 0950-382X (ISSN-L)
- 1365-2958
- OpenAlex
- W2000282782
- Cited by
- 212
- References
- 40
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 10 · 2023: 12 · 2022: 6 · 2021: 10 · 2020: 7 · 2019: 12 · 2018: 6 · 2017: 14 · 2016: 12 · 2015: 5 · 2014: 15 · 2013: 8 · 2012: 19
- FWCI
- 10.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL077588, HL 077588)
- National Institute of Allergy and Infectious Diseases
- Topics
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Keywords
- SREBP, Cryptococcus neoformans, oxygen sensing, sterol homeostasis, ergosterol biosynthesis, iron absorption, meningoencephalitis, cryptococcosis, virulence, low oxygen adaptation, brain infection
- MeSH terms
- Animals, Antifungal Agents, Azoles, Brain, Cryptococcus neoformans, Electrophoresis, Polyacrylamide Gel, Ergosterol, Female, Fungal Proteins, Homeostasis, Iron, Mice, Inbred BALB C, Models, Biological, Oxygen, Sterols, Virulence, Blotting, Northern, Gene Expression Regulation, Fungal, Genome, Fungal, Itraconazole, Oligonucleotide Array Sequence Analysis, Mice, Sterol Regulatory Element Binding Proteins
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