Transcriptional Regulation of Chitin Synthases by Calcineurin Controls Paradoxical Growth of Aspergillus fumigatus in Response to Caspofungin

Fortwendel, Jarrod R.; Juvvadi, Praveen R.; Perfect, B. Zachary; Rogg, Luise E.; Perfect, John R.; Steinbach, William J.

doi:10.1128/aac.00854-09

Cited by 153Fungal and yeast genetics researchAntifungal resistance and susceptibilityFungal Infections and Studies

Transcriptional Regulation of Chitin Synthases by Calcineurin Controls Paradoxical Growth of Aspergillus fumigatus in Response to Caspofungin

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Fortwendel, Jarrod R., Juvvadi, Praveen R., Perfect, B. Zachary, Rogg, Luise E., Perfect, John R., Steinbach, William J.·2010·Antimicrobial Agents and Chemotherapy

DOI 10.1128/aac.00854-09PMC PMC2849361

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Abstract

Attenuated activity of echinocandin antifungals at high concentrations, known as the “paradoxical effect,” is a well-established phenomenon in Candida albicans and Aspergillus fumigatus . In the yeast C. albicans , upregulation of chitin biosynthesis via the protein kinase C (PKC), high-osmolarity glycerol response (HOG), and Ca 2+ /calcineurin signaling pathways is an important cell wall stress response that permits growth in the presence of high concentrations of echinocandins. However, nothing is known of the molecular mechanisms regulating the mold A. fumigatus and its paradoxical response to echinocandins. Here, we show that the laboratory strain of A. fumigatus and five of seven clinical A. fumigatus isolates tested display various magnitudes of paradoxical growth in response to caspofungin. Interestingly, none of the eight strains showed paradoxical growth in the presence of micafungin or anidulafungin. Treatment of the Δ cnaA and Δ crzA strains, harboring gene deletions of the calcineurin A subunit and the calcineurin-dependent transcription factor, respectively, with high concentrations of caspofungin revealed that the A. fumigatus paradoxical effect is calcineurin pathway dependent. Exploring a molecular role for CnaA in the compensatory chitin biosynthetic response, we found that caspofungin treatment resulted in increased chitin synthase gene expression, leading to a calcineurin-dependent increase in chitin synthase activity. Taken together, our data suggest a mechanistic role for A. fumigatus calcineurin signaling in the chitin biosynthetic response observed during paradoxical growth in the presence of high-dose caspofungin treatment.

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Calcineurin also increases echinocandin tolerance in C. albicans and A. fumigatus.
“As calcineurin also increases echinocandin tolerance in C. albicans and A. fumigatus (45, 46)”
From Echinocandin tolerance and persistence in vitro are regulated by calcineurin signaling in Candida glabrata (2026) · cites this paper as [46]
For A. fumigatus, the chitin biosynthetic response is controlled, at least in part, by calcineurin-mediated transcriptional upregulation of chitin synthases.
“For A. fumigatus, the chitin biosynthetic response is controlled, at least in part, by calcineurin-mediated transcriptional upregulation of chitin synthases83.”
From Molecular mechanisms governing antifungal drug resistance (2023) · cites this paper as [83]
Genetic or pharmacologic repression of Hsp90 in A. fumigatus causes defective sporulation.
“Genetic or pharmacologic repression of Hsp90 resulted in various similar phenotypic consequences compared to calcineurin deletion, such as impaired hyphal elongation, decreased β-glucan content of the cell wall, defective sporulation, and increased susceptibility to caspofungin with abolition of the paradoxical effect of this drug”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010
Genetic or pharmacologic repression of Hsp90 in A. fumigatus decreases β-glucan content of the cell wall.
“Genetic or pharmacologic repression of Hsp90 resulted in various similar phenotypic consequences compared to calcineurin deletion, such as impaired hyphal elongation, decreased β-glucan content of the cell wall, defective sporulation, and increased susceptibility to caspofungin with abolition of the paradoxical effect of this drug”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010
Genetic or pharmacologic repression of Hsp90 in A. fumigatus impairs hyphal elongation.
“Genetic or pharmacologic repression of Hsp90 resulted in various similar phenotypic consequences compared to calcineurin deletion, such as impaired hyphal elongation, decreased β-glucan content of the cell wall, defective sporulation, and increased susceptibility to caspofungin with abolition of the paradoxical effect of this drug”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010

Genetic or pharmacologic repression of Hsp90 in A. fumigatus increases susceptibility to caspofungin and abolishes the paradoxical effect of caspofungin.
“Genetic or pharmacologic repression of Hsp90 resulted in various similar phenotypic consequences compared to calcineurin deletion, such as impaired hyphal elongation, decreased β-glucan content of the cell wall, defective sporulation, and increased susceptibility to caspofungin with abolition of the paradoxical effect of this drug”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010
In A. fumigatus, the ΔcrzA strain is hypersensitive to caspofungin.
“Akin to the Hsp90 repression strain, the A. fumigatus ΔcrzA strain exhibited the same sporulation and cell wall defects, and was also hypersensitive to caspofungin and incapable of generating a paradoxical response at high caspofungin concentrations (Cramer et al., 2008; Fortwendel et al., 2010; Fortwendel et al., 2009).”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010
In A. fumigatus, the ΔcrzA strain is incapable of generating a paradoxical response at high caspofungin concentrations.
“Akin to the Hsp90 repression strain, the A. fumigatus ΔcrzA strain exhibited the same sporulation and cell wall defects, and was also hypersensitive to caspofungin and incapable of generating a paradoxical response at high caspofungin concentrations (Cramer et al., 2008; Fortwendel et al., 2010; Fortwendel et al., 2009).”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010
In A. fumigatus, the ΔcrzA strain exhibits sporulation and cell wall defects.
“Akin to the Hsp90 repression strain, the A. fumigatus ΔcrzA strain exhibited the same sporulation and cell wall defects, and was also hypersensitive to caspofungin and incapable of generating a paradoxical response at high caspofungin concentrations (Cramer et al., 2008; Fortwendel et al., 2010; Fortwendel et al., 2009).”
From Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis (2014) · cites this paper as Fortwendel et al., 2010

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Caspofungin Treatment of Aspergillus fumigatus Results in ChsG-Dependent Upregulation of Chitin Synthesis and the Formation of Chitin-Rich Microcolonies
Walker, L. A., Lee, K. K., Munro, C. A., & Gow, N. A. R. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00862-15 · Cited by 90 · see citing works
The Aspergillus fumigatus CrzA Transcription Factor Activates Chitin Synthase Gene Expression during the Caspofungin Paradoxical Effect
Ries, L. N. A., Rocha, M. C., de Castro, P. A., Silva-Rocha, R., Silva, R. N., Freitas, F. Z., de Assis, L. J., Bertolini, M. C., Malavazi, I., & Goldman, G. H. (2017) · mBio · doi:10.1128/mbio.00705-17 · Cited by 76 · see citing works

Authors: Fortwendel, J. R., Juvvadi, P. R., Perfect, B. Z., Rogg, L. E., Perfect, J. R., & Steinbach, W. J.
Affiliations: Departments of Pediatrics
Duke Medical Center (US)
Corresponding author: Steinbach, William J.
ORCID: Fortwendel, Jarrod R.
Juvvadi, Praveen R.
Perfect, John R.
Steinbach, William J.
Venue: Antimicrobial Agents and Chemotherapy
Publisher: American Society for Microbiology
Published: 2010-04
Volume: 54
Issue: 4
Pages: 1555-1563
ISSN: 0066-4804 (ISSN-L)
1098-6596
DOI: 10.1128/aac.00854-09
PMC: PMC2849361
OpenAlex: W2126957470
Cited by: 153
References: 39
Citations by year: 2026: 7 · 2025: 6 · 2024: 8 · 2023: 9 · 2022: 9 · 2021: 8 · 2020: 18 · 2019: 12 · 2018: 4 · 2017: 13 · 2016: 11 · 2015: 10 · 2014: 13 · 2013: 6 · 2012: 7
FWCI: 3.25
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Antimicrobial Agents and Chemotherapy (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Children's Miracle Network Hospitals
Astellas Pharma
U.S. Public Health Service (A1061149)
National Institute of Allergy and Infectious Diseases (T32AI052080)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords: Aspergillus fumigatus, caspofungin, echinocandins, calcineurin signaling, chitin synthase, chitin synthesis, transcriptional regulation, antifungal resistance, cell wall stress response, micafungin, anidulafungin
MeSH terms: Caspofungin, Antifungal Agents, Aspergillus fumigatus, Base Sequence, Chitin Synthase, DNA, Fungal, Fungal Proteins, Genes, Fungal, Transcription Factors, Signal Transduction, Gene Expression Regulation, Fungal, Gene Deletion, DNA Primers, Calcineurin, Echinocandins, Lipopeptides

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Transcriptional Regulation of Chitin Synthases by Calcineurin Controls Paradoxical Growth of Aspergillus fumigatus in Response to Caspofungin

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