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- Vacuolar zinc transporter Zrc1 is required for detoxification of excess intracellular zinc in the human fungal pathogen Cryptococcus neoformans
- Minsu Cho , Guanggan Hu , Mélissa Caza , Linda C. Horianopoulos , James W. Kronstad , Won Hee Jung
- J. Microbiol. 2018;56(1):65-71. Published online January 4, 2018
- DOI: https://doi.org/10.1007/s12275-018-7475-y
- 44 View
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- 11 Crossref
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Abstract
- Zinc is an important transition metal in all living organisms and is required for numerous biological processes. However, excess zinc can also be toxic to cells and cause cellular stress. In the model fungus Saccharomyces cerevisiae, a vacuolar zinc transporter, Zrc1, plays important roles in the storage and detoxification of excess intracellular zinc to protect the cell. In this study, we identified an ortholog of the S. cerevisiae ZRC1 gene in the human fungal pathogen Cryptococcus neoformans. Zrc1 was localized in the vacuolar membrane in C. neoformans, and a mutant lacking ZRC1 showed significant growth defects under high-zinc conditions. These results suggested a role for Zrc1 in zinc detoxification. However, contrary to our expectation, the expression of Zrc1 was induced in cells grown in zinc-limited conditions and decreased upon the addition of zinc. These expression patterns were similar to those of Zip1, the high-affinity zinc transporter in the plasma membrane of C. neoformans. Furthermore, we used the zrc1 mutant in a murine model of cryptococcosis to examine whether a mammalian host could inhibit the survival of C. neoformans using zinc toxicity. We found that the mutant showed no difference in virulence compared with the wildtype strain. This result suggests that Zrc1-mediated zinc detoxification is not required for the virulence of C. neoformans, and imply that zinc toxicity may not be an important aspect of the host immune response to the fungus.
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Citations
Citations to this article as recorded by
- CDF family of zinc transporters ZRC-1, MSC-2, and ZRG-17 are involved in survival at high zinc conditions, vegetative development, and cellulase utilization in Neurospora crassa
Serena Ngiimei D, Ranjan Tamuli
Journal of Biosciences.2024;[Epub] CrossRef - “We've got to get out”—Strategies of human pathogenic fungi to escape from phagocytes
Johannes Sonnberger, Lydia Kasper, Theresa Lange, Sascha Brunke, Bernhard Hube
Molecular Microbiology.2024; 121(3): 341. CrossRef - Zinc Starvation Induces Cell Wall Remodeling and Activates the Antioxidant Defense System in Fonsecaea pedrosoi
Tayná Aparecida de Oliveira Santos, Lucas Weba Soares, Lucas Nojosa Oliveira, Dayane Moraes, Millena Silva Mendes, Célia Maria de Almeida Soares, Alexandre Melo Bailão, Mirelle Garcia Silva Bailão
Journal of Fungi.2024; 10(2): 118. CrossRef -
Characterization and functional analysis of zinc trafficking in the human fungal pathogen
Candida parapsilosis
Tamás Takács, Mihály Tibor Németh, Flóra Bohner, Csaba Vágvölgyi, Ferenc Jankovics, Duncan Wilson, Attila Gácser
Open Biology.2022;[Epub] CrossRef - Fungal–Metal Interactions: A Review of Toxicity and Homeostasis
Janelle R. Robinson, Omoanghe S. Isikhuemhen, Felicia N. Anike
Journal of Fungi.2021; 7(3): 225. CrossRef - Zinc at the Host–Fungus Interface: How to Uptake the Metal?
Lucas Weba Soares, Alexandre Melo Bailão, Célia Maria de Almeida Soares, Mirelle Garcia Silva Bailão
Journal of Fungi.2020; 6(4): 305. CrossRef - Transcription factors and transporters in zinc homeostasis: lessons learned from fungi
David J. Eide
Critical Reviews in Biochemistry and Molecular Biology.2020; 55(1): 88. CrossRef - RNase G controls tpiA mRNA abundance in response to oxygen availability in Escherichia coli
Jaejin Lee, Dong-Ho Lee, Che Ok Jeon, Kangseok Lee
Journal of Microbiology.2019; 57(10): 910. CrossRef - The coordinated action of RNase III and RNase G controls enolase expression in response to oxygen availability in Escherichia coli
Minho Lee, Minju Joo, Minji Sim, Se-Hoon Sim, Hyun-Lee Kim, Jaejin Lee, Minkyung Ryu, Ji-Hyun Yeom, Yoonsoo Hahn, Nam-Chul Ha, Jang-Cheon Cho, Kangseok Lee
Scientific Reports.2019;[Epub] CrossRef - TheAspergillus fumigatustranscription factor AceA is involved not only in Cu but also in Zn detoxification through regulating transporters CrpA and ZrcA
Zhendong Cai, Wenlong Du, Zheng Zhang, Luyu Guan, Qiuqiong Zeng, Yanfei Chai, Chuanchao Dai, Ling Lu
Cellular Microbiology.2018; 20(10): e12864. CrossRef - Biphasic zinc compartmentalisation in a human fungal pathogen
Aaron C. Crawford, Laura E. Lehtovirta-Morley, Omran Alamir, Maria J. Niemiec, Bader Alawfi, Mohammad Alsarraf, Volha Skrahina, Anna C. B. P. Costa, Andrew Anderson, Sujan Yellagunda, Elizabeth R. Ballou, Bernhard Hube, Constantin F. Urban, Duncan Wilson,
PLOS Pathogens.2018; 14(5): e1007013. CrossRef
- CDF family of zinc transporters ZRC-1, MSC-2, and ZRG-17 are involved in survival at high zinc conditions, vegetative development, and cellulase utilization in Neurospora crassa
Research Support, Non-U.S. Gov't
- Negative regulation of the vacuole-mediated resistance to K+ stress by a novel C2H2 zinc finger transcription factor encoded by aslA in Aspergillus nidulans
- Dong Soo Park , Yeong Man Yu , Yong Jin Kim , Pil Jae Maeng
- J. Microbiol. 2015;53(2):100-110. Published online January 28, 2015
- DOI: https://doi.org/10.1007/s12275-015-4701-8
- 52 View
- 0 Download
- 16 Crossref
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Abstract
- In fungi and plants, vacuoles function as a storage and sequestration vessel for a wide variety of ions and are responsible for cytosolic ion homeostasis and responses to ionic shock. In the filamentous fungus Aspergillus nidulans, however, little is known about the molecular genetic mechanisms of vacuolar biogenesis and function. In the present study, we analyzed the function of the aslA gene (AN5583) encoding a novel C2H2-type zinc finger transcription factor (TF) in relation to K+ stress resistance, vacuolar morphology, and vacuolar transporters. The mutant lacking aslA showed increased mycelial growth and decreased branching at high K+ concentrations. Deletion of aslA also caused elevated K+ stress-inducible expression of the genes, nhxA (AN2288), vnxA (AN6986), and vcxA (AN0471), encoding putative endosomal and vacuolar cation/H+ exchangers, as well as cpyA and vpsA genes encoding the proteins involved in vacuolar biogenesis. Interestingly, vacuolar fragmentation induced by K+ stress was alleviated by aslA deletion, resulting in persistence of unfragmented vacuoles. In the presence of bafilomycin, an inhibitor of vacuolar H+-ATPase, the mutant phenotype was suppressed in terms of growth rates and vacuolar morphology. These results together suggest that the C2H2- type zinc finger TF AslA attenuates the K+ stress-inducible expression of the genes encoding the ion pumps involved in vacuolar sequestration of K+ ions powered by vacuolar H+- ATPase, as well as the proteins that function in vacuolar biogenesis.
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Citations
Citations to this article as recorded by- The pleiotropic phenotype of FlbA of Aspergillus niger is explained in part by the activity of seven of its downstream-regulated transcription factors
Xiaoyi Chen, Juan P. Moran Torres, Peter Jan Vonk, J. Mirjam A. Damen, Karli R. Reiding, Jan Dijksterhuis, Luis G. Lugones, Han A.B. Wösten
Fungal Genetics and Biology.2024; 172: 103894. CrossRef - Survival Factor A (SvfA) Contributes to Aspergillus nidulans Pathogenicity
Joo-Yeon Lim, Ye-Eun Jung, Hye-Eun Hwang, Cheol-Hee Kim, Nese Basaran-Akgul, Sri Harshini Goli, Steven P. Templeton, Hee-Moon Park
Journal of Fungi.2023; 9(2): 143. CrossRef - A C2H2 Zinc Finger Protein PlCZF1 Is Necessary for Oospore Development and Virulence in Peronophythora litchii
Honghui Zhu, Junjian Situ, Tianfang Guan, Ziyuan Dou, Guanghui Kong, Zide Jiang, Pinggen Xi
International Journal of Molecular Sciences.2022; 23(5): 2733. CrossRef - The Gβ-like Protein AfCpcB Affects Sexual Development, Response to Oxidative Stress and Phagocytosis by Alveolar Macrophages in Aspergillus fumigatus
Joo-Yeon Lim, Yeon-Ju Kim, Hee-Moon Park
Journal of Fungi.2022; 8(1): 56. CrossRef - Characterization of BbKlf1 as a novel transcription factor vital for asexual and infection cycles of Beauveria bassiana
Rehab Abdelmonem Mohamed, Chong‐Tao Guo, Si‐Yuan Xu, Sheng‐Hua Ying, Ming‐Guang Feng
Environmental Microbiology Reports.2022; 14(5): 719. CrossRef - The LAMMER Kinase, LkhA, Affects Aspergillus fumigatus Pathogenicity by Modulating Reproduction and Biosynthesis of Cell Wall PAMPs
Joo-Yeon Lim, Yeon Ju Kim, Seul Ah Woo, Jae Wan Jeong, Yu-Ri Lee, Cheol-Hee Kim, Hee-Moon Park
Frontiers in Cellular and Infection Microbiology.2021;[Epub] CrossRef - Mannitol-1-phosphate dehydrogenase, MpdA, is required for mannitol production in vegetative cells and involved in hyphal branching, heat resistance of conidia and sexual development in Aspergillus nidulans
Joo-Yeon Lim, Seung-Hyun Jang, Hee-Moon Park
Current Genetics.2021; 67(4): 613. CrossRef - The putative C2H2 transcription factor RocA is a novel regulator of development and secondary metabolism in Aspergillus nidulans
Dong Chan Won, Yong Jin Kim, Da Hye Kim, Hee-Moon Park, Pil Jae Maeng
Journal of Microbiology.2020; 58(7): 574. CrossRef - Survival factor SvfA plays multiple roles in differentiation and is essential for completion of sexual development in Aspergillus nidulans
Joo-Yeon Lim, Eun-Hye Kang, Yun-Hee Park, Jun-Ho Kook, Hee-Moon Park
Scientific Reports.2020;[Epub] CrossRef - Fungal oxylipins direct programmed developmental switches in filamentous fungi
Mengyao Niu, Breanne N. Steffan, Gregory J. Fischer, Nandhitha Venkatesh, Nicholas L. Raffa, Molly A. Wettstein, Jin Woo Bok, Claudio Greco, Can Zhao, Erwin Berthier, Ernst Oliw, David Beebe, Michael Bromley, Nancy P. Keller
Nature Communications.2020;[Epub] CrossRef - The Cys2His2 zinc finger protein Zfp1 regulates sexual reproduction and virulence in Cryptococcus neoformans
Cheng-Li Fan, Lian-Tao Han, Su-Ting Jiang, An-Ni Chang, Ze-Yang Zhou, Tong-Bao Liu
Fungal Genetics and Biology.2019; 124: 59. CrossRef - Global gene expression changes reflecting pleiotropic effects of Irpex lacteus induced by low‐intensity electromagnetic field
Ling Sun, Xinyi Li, Haile Ma, Ronghai He, Prince O. Donkor
Bioelectromagnetics.2019; 40(2): 104. CrossRef - Transcription Factors Controlling Primary and Secondary Metabolism in Filamentous Fungi: The β-Lactam Paradigm
Carlos García-Estrada, Rebeca Domínguez-Santos, Katarina Kosalková, Juan-Francisco Martín
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Scientific Reports.2017;[Epub] CrossRef - The signal peptide peptidase SppA is involved in sterol regulatory element‐binding protein cleavage and hypoxia adaptation in Aspergillus nidulans
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Molecular Microbiology.2016; 100(4): 635. CrossRef - ZNF1 Encodes a Putative C2H2 Zinc-Finger Protein Essential for Appressorium Differentiation by the Rice Blast Fungus Magnaporthe oryzae
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Molecular Plant-Microbe Interactions®.2016; 29(1): 22. CrossRef
- The pleiotropic phenotype of FlbA of Aspergillus niger is explained in part by the activity of seven of its downstream-regulated transcription factors
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