Candida albicans Hap43 Is a Repressor Induced under Low-Iron Conditions and Is Essential for Iron-Responsive Transcriptional Regulation and Virulence

Hsu, Po-Chen; Yang, Cheng-Yao; Lan, Chung-Yu

doi:10.1128/ec.00158-10

Cited by 157Fungal and yeast genetics researchAntifungal resistance and susceptibilityFungal Infections and Studies

Candida albicans Hap43 Is a Repressor Induced under Low-Iron Conditions and Is Essential for Iron-Responsive Transcriptional Regulation and Virulence

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Hsu, Po-Chen, Yang, Cheng-Yao, Lan, Chung-Yu·2011·Eukaryotic Cell

DOI 10.1128/ec.00158-10PMC PMC3067405

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Abstract

Candida albicans is an opportunistic fungal pathogen that exists as normal flora in healthy human bodies but causes life-threatening infections in immunocompromised patients. In addition to innate and adaptive immunities, hosts also resist microbial infections by developing a mechanism of “natural resistance” that maintains a low level of free iron to restrict the growth of invading pathogens. C. albicans must overcome this iron-deprived environment to cause infections. There are three types of iron-responsive transcriptional regulators in fungi; Aft1/Aft2 activators in yeast, GATA-type repressors in many fungi, and HapX/Php4 in Schizosaccharomyces pombe and Aspergillus species. In this study, we characterized the iron-responsive regulator Hap43, which is the C. albicans homolog of HapX/Php4 and is repressed by the GATA-type repressor Sfu1 under iron-sufficient conditions. We provide evidence that Hap43 is essential for the growth of C. albicans under low-iron conditions and for C. albicans virulence in a mouse model of infection. Hap43 was not required for iron acquisition under low-iron conditions. Instead, it was responsible for repression of genes that encode iron-dependent proteins involved in mitochondrial respiration and iron-sulfur cluster assembly. We also demonstrated that Hap43 executes its function by becoming a transcriptional repressor and accumulating in the nucleus in response to iron deprivation. Finally, we found a connection between Hap43 and the global corepressor Tup1 in low-iron-induced flavinogenesis. Taken together, our data suggest a complex interplay among Hap43, Sfu1, and Tup1 to coordinately regulate iron acquisition, iron utilization, and other iron-responsive metabolic activities.

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Hap43, Sfu1, and Tup1 act coordinately and regulate iron acquisition, iron utilization, and other iron-responsive metabolic activities in C. albicans.
“Finally, it has been recently reported that Hap43, Sfu1, and Tup1 act coordinately and regulate iron acquisition, iron utilization, and other iron-responsive metabolic activities in C. albicans [75].”
From Strategies of intracellular pathogens for obtaining iron from the environment (2015) · cites this paper as [75]

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The role of mitochondria in cellular iron–sulfur protein biogenesis and iron metabolism
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HapX-Mediated Iron Homeostasis Is Essential for Rhizosphere Competence and Virulence of the Soilborne Pathogen Fusarium oxysporum
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Sterol Biosynthesis and Azole Tolerance Is Governed by the Opposing Actions of SrbA and the CCAAT Binding Complex
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Cap2-HAP complex is a critical transcriptional regulator that has dual but contrasting roles in regulation of iron homeostasis in Candida albicans
Singh, R. P., Prasad, H. K., Sinha, I., Agarwal, N., & Natarajan, K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.233569 · Cited by 113 · see citing works
Divergent Targets of Candida albicans Biofilm Regulator Bcr1 In Vitro and In Vivo
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Candida albicans specializations for iron homeostasis: from commensalism to virulence
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Yeast AP-1 like transcription factors (Yap) and stress response: a current overview
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An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë festucae with Lolium perenne
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Conserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
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Sequence and Analysis of the Genome of the Pathogenic Yeast Candida orthopsilosis
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The Crz1/Sp1 Transcription Factor of Cryptococcus neoformans Is Activated by Calcineurin and Regulates Cell Wall Integrity
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Overview on the Bacterial Iron-Riboflavin Metabolic Axis
Cisternas, I. S., Salazar, J. C., & García-Angulo, V. A. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01478 · Cited by 83 · see citing works
Exploring and exploiting the connection between mitochondria and the virulence of human pathogenic fungi
Verma, S., Shakya, V. P. S., & Idnurm, A. (2018) · Virulence · doi:10.1080/21505594.2017.1414133 · Cited by 67 · see citing works
Iron–sulfur cluster signaling: The common thread in fungal iron regulation
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Dynamic Transcript Profiling of Candida albicans Infection in Zebrafish: A Pathogen-Host Interaction Study
Chen, Y. Y., Chao, C., Liu, F., Hsu, P., Chen, H.-F., Peng, S.-C., Chuang, Y., Lan, C., Hsieh, W., & Wong, D. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072483 · Cited by 64 · see citing works
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Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review
Lapière, A., & Richard, M. L. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2105610 · Cited by 61 · see citing works
SRE1 Regulates Iron-Dependent and -Independent Pathways in the Fungal Pathogen Histoplasma capsulatum
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Iron uptake and regulation in Schizosaccharomyces pombe
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The Monothiol Glutaredoxin Grx4 Regulates Iron Homeostasis and Virulence in Cryptococcus neoformans
Attarian, R., Hu, G., Caza, M., Sánchez‐León, E., Croll, D., Do, E., Bach, H., Missall, T. A., Lodge, J. K., Jung, W. H., et al. (2018) · mBio · doi:10.1128/mbio.02377-18 · Cited by 57 · see citing works
The Transcriptional Stress Response of Candida albicans to Weak Organic Acids
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The CCAAT-binding complex (CBC) in Aspergillus species
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The Hap Complex in Yeasts: Structure, Assembly Mode, and Gene Regulation
Mao, Y., & Chen, C. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01645 · Cited by 54 · see citing works
Examining the virulence of Candida albicans transcription factor mutants using Galleria mellonella and mouse infection models
Amorim-Vaz, S., Delarze, E., Ischer, F., Sanglard, D., & Coste, A. T. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00367 · Cited by 53 · see citing works
Study of Candida albicans and its interactions with the host: A mini review
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Transcriptional Circuits Regulating Developmental Processes in Candida albicans
Rodríguez, D. L., Quail, M. M., Hernday, A. D., & Nobile, C. J. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.605711 · Cited by 53 · see citing works
Strategies of intracellular pathogens for obtaining iron from the environment
Leon-Sicairos, N., Reyes-Cortes, R., Guadrón-Llanos, A. M., Madueña-Molina, J., Leon-Sicairos, C., & Canizalez-Román, A. (2015) · BioMed Research International · doi:10.1155/2015/476534 · Cited by 51 · see citing works
Identification and Functional Characterization of Rca1, a Transcription Factor Involved in both Antifungal Susceptibility and Host Response in Candida albicans
Vandeputte, P., Pradervand, S., Ischer, F., Coste, A. T., Ferrari, S., Harshman, K., & Sanglard, D. (2012) · Eukaryotic Cell · doi:10.1128/ec.00134-12 · Cited by 51 · see citing works
Dual transcriptome of the immediate neutrophil and Candida albicans interplay
Niemiec, M. J., Grumaz, C., Ermert, D., Desel, C., Shankar, M., Lopes, J. P., Mills, I. G., Stevens, P., Sohn, K., & Urban, C. F. (2017) · BMC Genomics · doi:10.1186/s12864-017-4097-4 · Cited by 49 · see citing works
A novel hybrid iron regulation network combines features from pathogenic and nonpathogenic yeasts
Gerwien, F., Safyan, A., Wisgott, S., Hille, F., Kaemmer, P., Linde, J., Brunke, S., Kasper, L., & Hube, B. (2016) · mBio · doi:10.1128/mbio.01782-16 · Cited by 47 · see citing works
Cellular iron homeostasis mediated by the Mrs4–Ccc1–Smf3 pathway is essential for mitochondrial function, morphogenesis and virulence in Candida albicans
Xu, N., Dong, Y., Cheng, X., Yu, Q., Qian, K., Mao, J., Jia, C., Ding, X., Zhang, B., Chen, Y., et al. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.12.009 · Cited by 47 · see citing works
Y ap7 is a transcriptional repressor of nitric oxide oxidase in yeasts, which arose from neofunctionalization after whole genome duplication
Merhej, J., Delaveau, T., Guitard, J., Palancade, B., Hennequin, C., Garcia, M., Lelandais, G., & Devaux, F. (2015) · Molecular Microbiology · doi:10.1111/mmi.12983 · Cited by 46 · see citing works
Novel role of the Candida albicans ferric reductase gene CFL1 in iron acquisition, oxidative stress tolerance, morphogenesis and virulence
Xu, N., Qian, K., Dong, Y., Chen, Y., Yu, Q., Zhang, B., Xing, L., & Li, M. (2014) · Research in Microbiology · doi:10.1016/j.resmic.2014.03.001 · Cited by 44 · see citing works
The Monothiol Glutaredoxin Grx4 Exerts an Iron-Dependent Inhibitory Effect on Php4 Function
Vachon, P., Mercier, A., Jbel, M., & Labbé, S. (2012) · Eukaryotic Cell · doi:10.1128/ec.00060-12 · Cited by 44 · see citing works
The Transcription Factor VdHapX Controls Iron Homeostasis and Is Crucial for Virulence in the Vascular Pathogen Verticillium dahliae
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Role of SFP1 in the Regulation of Candida albicans Biofilm Formation
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Novel insight into the expression and function of the multicopper oxidases in Candida albicans
Cheng, X., Xu, N., Yu, Q., Ding, X., Qian, K., Zhao, Q., Wang, Y., Zhang, B., Xing, L., & Li, M. (2013) · Microbiology · doi:10.1099/mic.0.065268-0 · Cited by 41 · see citing works
Candida albicans Sfp1 Is Involved in the Cell Wall and Endoplasmic Reticulum Stress Responses Induced by Human Antimicrobial Peptide LL-37
Hsu, C.-M., Liao, Y.-L., Chang, C.-K., & Lan, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910633 · Cited by 39 · see citing works
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The fungal CCAAT-binding complex and HapX display highly variable but evolutionary conserved synergetic promoter-specific DNA recognition
Furukawa, T., Scheven, M. T., Misslinger, M., Zhao, C., Hoefgen, S., Gsaller, F., Lau, J., Jöchl, C., Donaldson, I. J., Valiante, V., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa109 · Cited by 38 · see citing works
Involvement of the mitogen activated protein kinase Hog1p in the response of Candida albicansto iron availability
Kaba, H. E., Nimtz, M., Müller, P. P., & Bilitewski, U. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-16 · Cited by 37 · see citing works
“Hap43p i s a transcription factor that is activated under low iron conditions and represses the xpr ssion of Sfu1p and of iron utilization genes so that repression of genes involved in iron uptake is relieved and the limited amount of iron is efficiently used for vital proteins [24].”
Background
Deciphering the Combinatorial DNA-binding Code of the CCAAT-binding Complex and the Iron-regulatory Basic Region Leucine Zipper (bZIP) Transcription Factor HapX
Hortschansky, P., Ando, E., Tuppatsch, K., Arikawa, H., Kobayashi, T., Kato, M., Haas, H., & Brakhage, A. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.628677 · Cited by 36 · see citing works
Molecular basis of the regulation of iron homeostasis in fission and filamentous yeasts
Brault, A., Mourer, T., & Labbé, S. (2015) · IUBMB Life · doi:10.1002/iub.1441 · Cited by 37 · see citing works
Iron‐responsive chromatin remodelling and <scp>MAPK</scp> signalling enhance adhesion in <scp>C</scp>andida albicans
Puri, S., Lai, W. K. M., Rizzo, J. M., Buck, M. J., & Edgerton, M. (2014) · Molecular Microbiology · doi:10.1111/mmi.12659 · Cited by 35 · see citing works
A network of paralogous stress response transcription factors in the human pathogen Candida glabrata
Merhej, J., Thiebaut, A., Blugeon, C., Pouch, J., Ali Chaouche, M. E. A., Camadro, J.-M., Le Crom, S., Lelandais, G., & Devaux, F. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00645 · Cited by 36 · see citing works
Aspergillus fumigatusvirulence through the lens of transcription factors: Table 1.
Bultman, K. M., Kowalski, C. H., & Cramer, R. A. (2016) · Medical Mycology · doi:10.1093/mmy/myw120 · Cited by 35 · see citing works
Heterologous Hsp90 promotes phenotypic diversity through network evolution
Koubková-Yu, T. C.-T., Chao, J.-C., & Leu, J. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006450 · Cited by 34 · see citing works
Robustness analysis on interspecies interaction network for iron and glucose competition between Candida albicans and zebrafish during infection
Lin, C., Lin, C.-N., Wang, Y., Liu, F.-Y., Chien, Y.-W., Chuang, Y., Lan, C., Hsieh, W., & Chen, B.-S. (2014) · BMC Systems Biology · doi:10.1186/1752-0509-8-s5-s6 · Cited by 35 · see citing works
Self-citation
The fungal pathogen Candida glabrata does not depend on surface ferric reductases for iron acquisition
Gerwien, F., Safyan, A., Wisgott, S., Brunke, S., Kasper, L., & Hube, B. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01055 · Cited by 33 · see citing works
Iron and Microbial Growth
Symeonidis, A. S., & Marangos, M. N. (2012) · InTech eBooks · doi:10.5772/34760 · Cited by 33 · see citing works
Environmental responses and the control of iron homeostasis in fungal systems
Canessa, P., & Larrondo, L. F. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4615-x · Cited by 31 · see citing works
Transcriptional Control of Drug Resistance, Virulence and Immune System Evasion in Pathogenic Fungi: A Cross-Species Comparison
Pais, P., Costa, C., Cavalheiro, M., Romão, D., & Teixeira, M. C. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00131 · Cited by 32 · see citing works
Connecting iron regulation and mitochondrial function in Cryptococcus neoformans
Horianopoulos, L. C., & Kronstad, J. W. (2019) · Current Opinion in Microbiology · doi:10.1016/j.mib.2019.04.002 · Cited by 32 · see citing works
A Transcriptional Regulatory Map of Iron Homeostasis Reveals a New Control Circuit for Capsule Formation in Cryptococcus neoformans
Do, E., Cho, Y., Kim, D., Kronstad, J. W., & Jung, W. H. (2020) · Genetics · doi:10.1534/genetics.120.303270 · Cited by 32 · see citing works
Regulators of commensal and pathogenic life‐styles of an opportunistic fungus— Candida albicans
Rai, L. S., van Wijlick, L., Bougnoux, M., Bachellier‐Bassi, S., & d’Enfert, C. (2021) · Yeast · doi:10.1002/yea.3550 · Cited by 36 · see citing works
Coordination of hypoxia adaptation and iron homeostasis in human pathogenic fungi
Chung, D., Haas, H., & Cramer, R. A. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00381 · Cited by 29 · see citing works
The tug-of-war on iron between plant and pathogen
Sun, J., Xiao, S., & Xue, C. (2023) · Phytopathology Research · doi:10.1186/s42483-023-00215-8 · Cited by 28 · see citing works
The regulation of iron homeostasis in the fungal human pathogen Candida glabrata
Devaux, F., & Thiébaut, A. (2019) · Microbiology · doi:10.1099/mic.0.000807 · Cited by 29 · see citing works
Tfp1 is required for ion homeostasis, fluconazole resistance and N-Acetylglucosamine utilization in Candida albicans
Jia, C., Zhang, K., Yu, Q., Zhang, B., Xiao, C., Dong, Y., Chen, Y., Zhang, B., Xing, L., & Li, M. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.08.005 · Cited by 26 · see citing works
The CCAAT-Binding Complex Controls Respiratory Gene Expression and Iron Homeostasis in Candida Glabrata
Thiébaut, A., Delaveau, T., Benchouaia, M., Boeri, J., Garcia, M., Lelandais, G., & Devaux, F. (2017) · Scientific Reports · doi:10.1038/s41598-017-03750-5 · Cited by 26 · see citing works
The adaptive response to iron involves changes in energetic strategies in the pathogen Candida albicans
Duval, C., Macabiou, C., Garcia, C., Lesuisse, E., Camadro, J., & Auchère, F. (2019) · MicrobiologyOpen · doi:10.1002/mbo3.970 · Cited by 24 · see citing works
Alkaline pH, Low Iron Availability, Poor Nitrogen Sources and CWI MAPK Signaling Are Associated with Increased Fusaric Acid Production in Fusarium oxysporum
Palmieri, D., Segorbe, D., López‐Berges, M. S., Curtis, F. D., Lima, G., Pietro, A. D., & Turrà, D. (2023) · Toxins · doi:10.3390/toxins15010050 · Cited by 25 · see citing works
The iron-dependent regulation of the Candida albicans oxidative stress response by the CCAAT-binding factor
Chakravarti, A., Camp, K., McNabb, D. S., & Pinto, I. (2017) · PLOS ONE · doi:10.1371/journal.pone.0170649 · Cited by 24 · see citing works
Aft2, a Novel Transcription Regulator, Is Required for Iron Metabolism, Oxidative Stress, Surface Adhesion and Hyphal Development in Candida albicans
Xu, N., Cheng, X., Yu, Q., Qian, K., Ding, X., Liu, R., Zhang, B., Xing, L., & Li, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062367 · Cited by 24 · see citing works
Rhb1 Regulates the Expression of Secreted Aspartic Protease 2 through the TOR Signaling Pathway in Candida albicans
Chen, Y.-T., Lin, C.-Y., Tsai, P.-W., Yang, C., Hsieh, W., & Lan, C. (2011) · Eukaryotic Cell · doi:10.1128/ec.05200-11 · Cited by 24 · see citing works
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Php4 Is a Key Player for Iron Economy in Meiotic and Sporulating Cells
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Self-citation

Authors: Hsu, P.-C., Yang, C.-Y., & Lan, C.-Y.
Affiliations: Institute of Molecular and Cellular Biology, No. 101, Section 2, Kuang Fu Road, Hsinchu 30013, Taiwan, Republic of China
Animal Technology Institute Taiwan (TW)
National Tsing Hua University (TW)
Corresponding author: Lan, Chung-Yu
ORCID: Hsu, Po-Chen
Yang, Cheng-Yao
Lan, Chung-Yu
Venue: Eukaryotic Cell
Publisher: American Society for Microbiology
Published: 2011-02
Volume: 10
Issue: 2
Pages: 207-225
ISSN: 1535-9778 (ISSN-L)
1535-9786
DOI: 10.1128/ec.00158-10
PMC: PMC3067405
OpenAlex: W2146920262
Cited by: 157
References: 94
Citations by year: 2026: 4 · 2025: 11 · 2024: 10 · 2023: 10 · 2022: 8 · 2021: 10 · 2020: 8 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 10 · 2015: 8 · 2014: 13 · 2013: 14 · 2012: 14
FWCI: 4.82
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Eukaryotic Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
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: Candida albicans, iron starvation, Tup1, iron acquisition, iron-sulfur cluster assembly, mitochondrial respiration, fungal virulence, natural resistance to infection, transcriptional repressor
MeSH terms: Iron Deficiencies, Amino Acid Sequence, Animals, Candida albicans, Candidiasis, Cell Nucleus, Female, Flavins, Fungal Proteins, Humans, Iron, Kidney, Mice, Inbred BALB C, Molecular Sequence Data, Repressor Proteins, Virulence, Gene Expression Regulation, Fungal, Sequence Alignment, Gene Deletion, Sequence Homology, Amino Acid, Two-Hybrid System Techniques, Cell Proliferation, Mice

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Candida albicans Hap43 Is a Repressor Induced under Low-Iron Conditions and Is Essential for Iron-Responsive Transcriptional Regulation and Virulence

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