Autophagy supports Candida glabrata survival during phagocytosis
Open accessAbstract
The opportunistic human fungal pathogen Candida glabrata is confronted with phagocytic cells of the host defence system. Survival of internalized cells is thought to contribute to successful dissemination. We investigated the reaction of engulfed C. glabrata cells using fluorescent protein fusions of the transcription factors CgYap1 and CgMig1 and catalase CgCta1. The expression level and peroxisomal localization of catalase was used to monitor the metabolic and stress status of internalized C. glabrata cells. These reporters revealed that the phagocytosed C. glabrata cells were exposed to transient oxidative stress and starved for carbon source. Cells trapped within macrophages increased their peroxisome numbers indicating a metabolic switch. Prolonged phagocytosis caused a pexophagy-mediated decline in peroxisome numbers. Autophagy, and in particular pexophagy, contributed to survival of C. glabrata during engulfment. Mutants lacking CgATG11 or CgATG17, genes required for pexophagy and non-selective autophagy, respectively, displayed reduced survival rates. Furthermore, both CgAtg11 and CgAtg17 contribute to survival, since the double mutant was highly sensitive to engulfment. Inhibition of peroxisome formation by deletion of CgPEX3 partially restored viability of CgATG11 deletion mutants during engulfment. This suggests that peroxisome formation and maintenance might sequester resources required for optimal survival. Mobilization of intracellular resources via autophagy is an important virulence factor that supports the viability of C. glabrata in the phagosomal compartment of infected innate immune cells.
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C. glabrata lacks hyphal formation and phagosomal extrusions to escape phagocytic cell attack, contrary to C. albicans.
“Candida glabrata lacks hyphal formation and phagosomal extrusions to escape the phagocytic cells attack contrary to C. albicans [68,69].”
From Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival (2021) · cites this paper as [69]
Inside phagosomes, C. glabrata faces glucose-limited environments and must change its metabolism to utilize non-fermentable carbon sources.
“In such niches, for example inside phagosomes, it faces glucose-limited environments. To survive, it has to change its metabolism and utilize non-fermentable carbon sources (Kaur et al., 2007; Roetzer et al., 2010; Fukuda et al., 2013).”
From Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate (2015) · cites this paper as Roetzer et al., 2010
CgCTA1 expression is regulated by several stress response transcriptional regulators including CgYap1, CgMsn2, CgMsn4 and CgSkn7.
“CgCTA1 expression is regulated by several stress response transcriptional regulators including CgYap1, CgMsn2, CgMsn4 and CgSkn7 [80,84,85,86].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [84]
C. glabrata activates pexophagy and autophagy processes.
“C. glabrata activates pexophagy and autophagy processes, undergoes chromatin remodeling and evades immune responses to survive and replicate in macrophages [84,147,150].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [84]
C. glabrata evades immune responses to survive and replicate in macrophages.
“C. glabrata activates pexophagy and autophagy processes, undergoes chromatin remodeling and evades immune responses to survive and replicate in macrophages [84,147,150].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [84]
C. glabrata undergoes chromatin remodeling.
“C. glabrata activates pexophagy and autophagy processes, undergoes chromatin remodeling and evades immune responses to survive and replicate in macrophages [84,147,150].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [84]
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Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Guidelines for the use and interpretation of assays for monitoring autophagy
Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., et al. (2012) · Autophagy · doi:10.4161/auto.19496 · Cited by 3,996 · see citing works
Self-citationKlionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Self-citationPharmacological modulation of autophagy: therapeutic potential and persisting obstacles
Galluzzi, L., Bravo-San Pedro, J. M., Levine, B., Green, D. R., & Kroemer, G. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.22 · Cited by 842 · see citing works
Candida glabrata: A review of its features and resistance
Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
Brunke, S., & Hube, B. (2013) · Cellular Microbiology · doi:10.1111/cmi.12091 · Cited by 239 · see citing works
Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., Barz, D., Haas, A., Kuchler, K., Schaller, M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003730 · Cited by 220 · see citing works
Schwarzmüller, T., Ma, B., Hiller, E., Istel, F., Tscherner, M., Brunke, S., Ames, L., Firon, A., Green, B., Cabral, V., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004211 · Cited by 191 · see citing works
Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival
Hassan, Y., Chew, S. Y., & Than, L. T. L. (2021) · Journal of Fungi · doi:10.3390/jof7080667 · Cited by 170 · see citing works
Metabolism in fungal pathogenesis
Ene, I. V., Brunke, S., Brown, A. J. P., & Hube, B. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019695 · Cited by 169 · see citing works
Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape.
Seider, K., Heyken, A., Lüttich, A., Miramón, P., & Hube, B. (2010) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.05.001 · Cited by 167 · see citing works
Roetzer, A., Gabaldón, T., & Schüller, C. (2011) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02102.x · Cited by 154 · see citing works
Self-citationCandida glabrata: A Lot More Than Meets the Eye
Kumar, K., Askari, F., Sahu, M. S., & Kaur, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020039 · Cited by 128 · see citing works
Bourgeois, C., Majer, O., Frohner, I. E., Lesiak-Markowicz, I., Hildering, K.-S., Glaser, W., Stockinger, S., Decker, T., Akira, S., Müller, M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002599 · Cited by 116 · see citing works
Divergent Approaches to Virulence in C. albicans and C. glabrata: Two Sides of the Same Coin
Galocha, M., Pais, P., Cavalheiro, M., Pereira, D., Viana, R., & Teixeira, M. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092345 · Cited by 105 · see citing works
Gabaldón, T., & Carreté, L. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fov110 · Cited by 99 · see citing works
Regulation of <i>Candida glabrata</i> oxidative stress resistance is adapted to host environment
Roetzer, A., Klopf, E., Gratz, N., Marcet-Houben, M., Hiller, E., Rupp, S., Gabaldón, T., Kovarik, P., & Schüller, C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2010.12.006 · Cited by 90 · see citing works
Self-citationSeider, K., Gerwien, F., Kasper, L., Allert, S., Brunke, S., Jablonowski, N., Schwarzmüller, T., Barz, D., Rupp, S., Kuchler, K., et al. (2014) · Eukaryotic Cell · doi:10.1128/ec.00262-13 · Cited by 91 · see citing works
Vale-Silva, L., Ischer, F., Leibundgut-Landmann, S., & Sanglard, D. (2013) · Infection and Immunity · doi:10.1128/iai.00074-13 · Cited by 65 · see citing works
Orta‐Zavalza, E., Guerrero‐Serrano, G., Gutiérrez‐Escobedo, G., Cañas‐Villamar, I., Juárez‐Cepeda, J., Castaño, I., & De Las Peñas, A. (2013) · Molecular Microbiology · doi:10.1111/mmi.12247 · Cited by 61 · see citing works
Kasper, L., Seider, K., Gerwien, F., Allert, S., Brunke, S., Schwarzmüller, T., Ames, L., Zubiria-Barrera, C., Mansour, M. K., Becken, U., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096015 · Cited by 59 · see citing works
Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate
Mota, S., Alves, R., Carneiro, C., Silva, S., Brown, A. J., Istel, F., Kuchler, K., Sampaio, P., Casal, M., Henriques, M., et al. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00919 · Cited by 49 · see citing works
Rasheed, M., Battu, A., & Kaur, R. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.813741 · Cited by 51 · see citing works
Chew, S. Y., Ho, K. L., Cheah, Y. K., Ng, T. S., Sandai, D., Brown, A. J. P., & Than, L. T. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-39117-1 · Cited by 49 · see citing works
Role of glutathione in the oxidative stress response in the fungal pathogen Candida glabrata
Gutiérrez-Escobedo, G., Orta-Zavalza, E., Castaño, I., & De Las Peñas, A. (2013) · Current Genetics · doi:10.1007/s00294-013-0390-1 · Cited by 47 · see citing works
Chen, S. C.-A., Lewis, R. E., & Kontoyiannis, D. P. (2011) · Virulence · doi:10.4161/viru.2.4.16764 · Cited by 41 · see citing works
Fukuda, Y., Tsai, H.-F., Myers, T. G., & Bennett, J. E. (2013) · Infection and Immunity · doi:10.1128/iai.00851-12 · Cited by 41 · see citing works
Kuhn, D. M., & Vyas, V. K. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00785.x · Cited by 38 · see citing works
<i>Candida glabrata</i> : new tools and technologies—expanding the toolkit
Ho, H.-L., & Haynes, K. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov066 · Cited by 29 · see citing works
Ng, T. S., Chew, S. Y., Rangasamy, P., Mohd Desa, M. N., Sandai, D., Chong, P. P., & Than, L. T. L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01334 · Cited by 15 · see citing works
- Authors
- Roetzer, A., Gratz, N., Kovarik, P., & Schüller, C.
- Affiliations
- University of Vienna (AT)
- ORCID
- Kovarik, Pavel
- Venue
- Cellular Microbiology
- Publisher
- Hindawi Limited
- Published
- 2010-02
- Volume
- 12
- Issue
- 2
- Pages
- 199-216
- ISSN
- 1462-5814 (ISSN-L)
- 1462-5822
- PMC
- PMC2816358
- OpenAlex
- W1982281067
- Cited by
- 142
- References
- 91
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 5 · 2023: 7 · 2022: 6 · 2021: 7 · 2020: 7 · 2019: 12 · 2018: 8 · 2017: 6 · 2016: 7 · 2015: 16 · 2014: 11 · 2013: 14 · 2012: 10
- FWCI
- 5.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Austrian Science Fund (SFB‐F28)
- Universität Wien (I031-B)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- Candida glabrata, autophagy, pexophagy, phagocytosis, macrophages, peroxisomes, oxidative stress, carbon starvation, Atg11, Atg17, PEX3, YAP, Mig1, fungal virulence
- MeSH terms
- Animals, Autophagy, Cells, Cultured, Fungal Proteins, Mice, Inbred C57BL, Microscopy, Fluorescence, Phagocytosis, Blotting, Southern, Blotting, Northern, Candida glabrata, Mice
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