Aspartyl proteases in Candida glabrata are required for suppression of the host innate immune response
Open accessAbstract
A family of 11 cell surface-associated aspartyl proteases (CgYps1–11), also referred as yapsins, is a key virulence factor in the pathogenic yeast Candida glabrata . However, the mechanism by which CgYapsins modulate immune response and facilitate survival in the mammalian host remains to be identified. Here, using RNA-Seq analysis, we report that genes involved in cell wall metabolism are differentially regulated in the Cgyps1–11 Δ mutant. Consistently, the mutant contained lower β-glucan and mannan levels and exhibited increased chitin content in the cell wall. As cell wall components are known to regulate the innate immune response, we next determined the macrophage transcriptional response to C. glabrata infection and observed differential expression of genes implicated in inflammation, chemotaxis, ion transport, and the tumor necrosis factor signaling cascade. Importantly, the Cgyps1–11 Δ mutant evoked a different immune response, resulting in an enhanced release of the pro-inflammatory cytokine IL-1β in THP-1 macrophages. Further, Cgyps1–11 Δ–induced IL-1β production adversely affected intracellular proliferation of co-infected WT cells and depended on activation of spleen tyrosine kinase (Syk) signaling in the host cells. Accordingly, the Syk inhibitor R406 augmented intracellular survival of the Cgyps1–11 Δ mutant. Finally, we demonstrate that C. glabrata infection triggers elevated IL-1β production in mouse organs and that the CgYPS genes are required for organ colonization and dissemination in the murine model of systemic infection. Altogether, our results uncover the basis for macrophage-mediated killing of Cgyps1–11 Δ cells and provide the first evidence that aspartyl proteases in C. glabrata are required for suppression of IL-1β production in macrophages.
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There is a close association between the capacity to form biofilms and colonize murine organs in the systemic candidiasis model.
“Moreover, recent studies have shown a close association between the capacity to form biofilms and colonize murine organs in the systemic candidiasis model [57,58], however, the precise mechanisms underlying this relationship are unknown.”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
CgYapsins are pivotal to the regulation of several cellular processes such as maintenance of the cell wall architecture, pH and vacuole homeostasis, biofilm formation and interaction with the host.
“Consistently, CgYapsins are pivotal to the regulation of several cellular processes such as maintenance of the cell wall architecture, pH and vacuole homeostasis, biofilm formation and interaction with the host [58,60,61,64].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
CgYapsins suppress production of pro-inflammatory cytokine IL-1β in human THP-1 macrophages, facilitate survival in macrophages and virulence in the models of murine systemic candidiasis and Drosophila melanogaster.
“The latter includes suppression of the production of pro-inflammatory cytokine IL-1β in human THP-1 macrophages, facilitating survival in macrophages and virulence in the models of murine systemic candidiasis and Drosophila melanogaster [58,60,65,66].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
The Cgyps1-11Δ mutant displays sunken cell walls containing higher chitin and reduced β-glucan and mannan levels.
“Lastly, the Cgyps1-11Δ mutant displayed sunken cell walls containing higher chitin and reduced β-glucan and mannan levels (Figure 1) [58,64].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
Syk is phosphorylated in response to C. glabrata infection, resulting in NLRP3 inflammasome-dependent production of IL-1β in human THP-1 macrophages.
“Additionally, the spleen tyrosine kinase, Syk, is known to be phosphorylated in response to C. glabrata infection which resulted in the NLRP3 inflammasome-dependent production of IL-1β in human THP-1 macrophages [58].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
The family of eleven cell surface-associated proteases (CgYapsins) is required to keep the Syk pathway activation in check.
“The family of eleven cell surface-associated proteases (CgYapsins) has been shown to be required to keep the Syk pathway activation in check, as lack of these proteases led to increased IL-1β release and killing of C. glabrata cells [58].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
Lack of CgYapsins led to increased IL-1β release and killing of C. glabrata cells.
“The family of eleven cell surface-associated proteases (CgYapsins) has been shown to be required to keep the Syk pathway activation in check, as lack of these proteases led to increased IL-1β release and killing of C. glabrata cells [58].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [58]
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“glabrata cells has previously been shown to result in prolonged activation of the Syk pathway while having no effect on the NF- B pathway (49).”
BackgroundDectin-1 plays an important role in host defense against systemicCandida glabratainfection
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- Authors
- Rasheed, M., Battu, A., & Kaur, R.
- Affiliations
- Manipal Academy of Higher Education (IN)
- Centre for DNA Fingerprinting and Diagnostics (IN)
- Corresponding author
- Kaur, Rupinder
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 293
- Issue
- 17
- Pages
- 6410-6433
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC5925793
- OpenAlex
- W2793266396
- Cited by
- 51
- References
- 60
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 11 · 2023: 11 · 2022: 9 · 2021: 5 · 2020: 1 · 2019: 4 · 2018: 2
- FWCI
- 2.27
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust/DBT India Alliance (IA/S/15/1/501831)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida glabrata, aspartic protease, macrophage response, IL-1β, R406, cell wall metabolism, β-glucan, mannan, chitin, fungal virulence, systemic fungal infection, organ colonization, THP-1 macrophages
- MeSH terms
- Syk Kinase, THP-1 Cells, Animals, Candidiasis, Cell Survival, Female, Fungal Proteins, Humans, Immunity, Innate, Macrophages, Mice, Inbred BALB C, Gene Deletion, Candida glabrata, Mice, Interleukin-1beta, Aspartic Acid Proteases
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