Mitochondria in Cryptococcus: an update of mitochondrial transcriptional regulation in Cryptococcus.


Journal

Current genetics
ISSN: 1432-0983
Titre abrégé: Curr Genet
Pays: United States
ID NLM: 8004904

Informations de publication

Date de publication:
Feb 2023
Historique:
received: 27 12 2022
accepted: 19 01 2023
revised: 19 01 2023
pubmed: 3 2 2023
medline: 16 2 2023
entrez: 2 2 2023
Statut: ppublish

Résumé

Encapsulated Cryptococcus species are responsible for approximately 15% of AIDS-related mortality. Numerous intriguing investigations have demonstrated that mitochondria play a crucial role in the pathogen-host axis of microorganisms. Mitochondria are vital energy-generating organelles, but they also regulate a variety of cellular activities, such as fungal adaptability in the host and drug resistance. Mitochondria are also the source of reactive oxygen species, which serve as intracellular messengers but are harmful when produced in excess. Thus, precise and stringent regulation of mitochondrial activity, including oxidative phosphorylation and the ROS detoxification process, is essential to ensure that only the amount required to maintain basic biological activities and prevent ROS toxicity in the cell is maintained. However, the relationship between mitochondria and the pathogenicity of Cryptococcus remains poorly understood. In this review, we focus on transcription regulation and maintenance of mitochondrial function along the pathogen-host interaction axis, as well as prospective antifungal strategies that target mitochondria.

Identifiants

pubmed: 36729179
doi: 10.1007/s00294-023-01261-7
pii: 10.1007/s00294-023-01261-7
doi:

Substances chimiques

Reactive Oxygen Species 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-6

Subventions

Organisme : National Natural Science Foundation of China
ID : 31870140
Organisme : National Key Research and Development Program of China
ID : 2022YFC2303000

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555
Anckar J, Sistonen L (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80:1089–1115
Arbon D, Zeniskova K, Subrtova K, Mach J, Stursa J, Machado M, Zahedifard F, Lestinova T, Hierro-Yap C, Neuzil J et al (2022) Repurposing of mitotam: novel anti-cancer drug candidate exhibits potent activity against major protozoan and fungal pathogens. Antimicrob Agents Chemother 66:e0072722
Attarian R, Hu G, Sanchez-Leon E, Caza M, Croll D, Do E, Bach H, Missall T, Lodge J, Jung WH et al (2018) The monothiol glutaredoxin grx4 regulates iron homeostasis and virulence in cryptococcus neoformans. Mbio. https://doi.org/10.1128/mBio.02377-18
doi: 10.1128/mBio.02377-18
Black B, Lee C, Horianopoulos LC, Jung WH, Kronstad JW (2021) Respiring to infect: Emerging links between mitochondria, the electron transport chain, and fungal pathogenesis. PLoS Pathog 17:e1009661
Braymer JJ, Lill R (2017) Iron-sulfur cluster biogenesis and trafficking in mitochondria. J Biol Chem 292:12754–12763
Byrnes EJ 3rd, Li W, Lewit Y, Ma H, Voelz K, Ren P, Carter DA, Chaturvedi V, Bildfell RJ, May RC et al (2010) Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog 6:e1000850
Byrnes EJ III, Li W, Ren P, Lewit Y, Voelz K, Fraser JA, Dietrich FS, May RC, Chaturvedi S, Chaturvedi V et al (2011) A diverse population of Cryptococcus gattii molecular type VGIII in southern Californian HIV/AIDS patients. PLoS Pathog 7:e1002205
Caza M, Hu G, Price M, Perfect JR, Kronstad JW (2016) The zinc finger protein mig1 regulates mitochondrial function and azole drug susceptibility in the pathogenic fungus cryptococcus neoformans. Msphere. https://doi.org/10.1128/mSphere.00080-15
doi: 10.1128/mSphere.00080-15
Denning DW, Bromley MJ (2015) Infectious disease. how to bolster the antifungal pipeline. Science 347:1414–1416
Ding C, Festa RA, Sun TS, Wang ZY (2014) Iron and copper as virulence modulators in human fungal pathogens. Mol Microbiol 93:10–23
Do E, Park S, Li MH, Wang JM, Ding C, Kronstad JW, Jung WH (2018) The mitochondrial ABC transporter Atm1 plays a role in iron metabolism and virulence in the human fungal pathogen cryptococcus neoformans. Med Mycol 56:458–468
Dong B, Jaeger AM, Hughes PF, Loiselle DR, Hauck JS, Fu Y, Haystead TA, Huang J, Thiele DJ (2020) Targeting therapy-resistant prostate cancer via a direct inhibitor of the human heat shock transcription factor 1. Sci Transl Med 12:574
Gao X, Fu Y, Sun S, Gu T, Li Y, Sun T, Li H, Du W, Suo C, Li C et al (2022) Cryptococcal Hsf3 controls intramitochondrial ROS homeostasis by regulating the respiratory process. Nat Commun 13:5407
Garcia-Santamarina S, Uzarska MA, Festa RA, Lill R, Thiele DJ (2017) Cryptococcus neoformans iron-sulfur protein biogenesis machinery is a novel layer of protection against Cu Stress. Mbio. https://doi.org/10.1128/mBio.01742-17
doi: 10.1128/mBio.01742-17
Gomez-Pastor R, Burchfiel ET, Thiele DJ (2018) Regulation of heat shock transcription factors and their roles in physiology and disease. Nat Rev Mol Cell Biol 19:4–19
Guaragnella N, Coyne LP, Chen XJ, Giannattasio S (2018) Mitochondria-cytosol-nucleus crosstalk: learning from Saccharomyces cerevisiae. FEMS Yeast Res. https://doi.org/10.1093/femsyr/foy088
doi: 10.1093/femsyr/foy088
Horianopoulos LC, Kronstad JW (2019) Connecting iron regulation and mitochondrial function in Cryptococcus neoformans. Curr Opin Microbiol 52:7–13
Idnurm A, Bahn YS, Nielsen K, Lin X, Fraser JA, Heitman J (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 3:753–764
Iyer KR, Revie NM, Fu C, Robbins N, Cowen LE (2021) Treatment strategies for cryptococcal infection: challenges, advances and future outlook. Nat Rev Microbiol 19:454–466
Jaeger AM, Pemble CW, Sistonen L, Thiele DJ (2016) Structures of reveal mechanisms for differential regulation of human heat-shock factors. Nat Struct Mol Biol 23:147–154
Jung WH, Kronstad JW (2011) Iron influences the abundance of the iron regulatory protein Cir1 in the fungal pathogen Cryptococcus neoformans. FEBS Lett 585:3342–3347
Jung WH, Sham A, White R, Kronstad JW (2006) Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biol 4:e410
Jung WH, Saikia S, Hu G, Wang J, Fung CK, D’Souza C, White R, Kronstad JW (2010) HapX positively and negatively regulates the transcriptional response to iron deprivation in Cryptococcus neoformans. PLoS Pathog 6:e1001209
Jung KW, Yang DH, Maeng S, Lee KT, So YS, Hong J, Choi J, Byun HJ, Kim H, Bang S et al (2015) Systematic functional profiling of transcription factor networks in Cryptococcus neoformans. Nat Commun 6:6757
Jung WH, Sanchez-Leon E, Kronstad JW (2021) Coordinated regulation of iron metabolism in Cryptococcus neoformans by GATA and CCAAT transcription factors: connections with virulence. Curr Genet 67:583–593
Kim JH, Haff RP, Faria NC, Martins Mde L, Chan KL, Campbell BC (2013) Targeting the mitochondrial respiratory chain of Cryptococcus through antifungal chemosensitization: a model for control of non-fermentative pathogens. Molecules 18:8873–8894
Kim J, Park M, Do E, Jung WH (2014a) Mitochondrial Protein Nfu1 Influences Homeostasis of Essential Metals in the Human Fungal Pathogen Cryptococcus neoformans. Mycobiology 42:427–431
Kim JH, Lee HO, Cho YJ, Kim J, Chun J, Choi J, Lee Y, Jung WH (2014b) A vanillin derivative causes mitochondrial dysfunction and triggers oxidative stress in Cryptococcus neoformans. PLoS ONE 9:e89122
Koch B, Traven A (2019) Mdivi-1 and mitochondrial fission: recent insights from fungal pathogens. Curr Genet 65:837–845
Kronstad JW, Attarian R, Cadieux B, Choi J, D’Souza CA, Griffiths EJ, Geddes JM, Hu G, Jung WH, Kretschmer M et al (2011) Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat Rev Microbiol 9:193–203
Kronstad JW, Hu G, Jung WH (2013) An encapsulation of iron homeostasis and virulence in cryptococcus neoformans. Trends Microbiol 21:457–465
Li D, She X, Calderone R (2016) Functional diversity of complex I subunits in Candida albicans mitochondria. Curr Genet 62:87–95
Li C, Li Y, Ding C (2019) The role of copper homeostasis at the host-pathogen axis: from bacteria to fungi. Int J Mol Sci 20:175
Liu Y, Okamoto K (2021) Regulatory mechanisms of mitophagy in yeast. Biochim Biophys Acta Gen Subj 1865:129858
Liu Y, Kang M, Wu SY, Ma Y, Chen ZX, Xie Y, Tang JT (2017) Different characteristics of cryptococcal meningitis between HIV-infected and HIV-uninfected patients in the Southwest of China. Med Mycol 55:255–261
Malina C, Larsson C, Nielsen J (2018) Yeast mitochondria: an overview of mitochondrial biology and the potential of mitochondrial systems biology. FEMS Yeast Res. https://doi.org/10.1093/femsyr/foy040
doi: 10.1093/femsyr/foy040
May RC, Stone NR, Wiesner DL, Bicanic T, Nielsen K (2016) Cryptococcus: from environmental saprophyte to global pathogen. Nat Rev Microbiol 14:106–117
Mitsuyama J, Nomura N, Hashimoto K, Yamada E, Nishikawa H, Kaeriyama M, Kimura A, Todo Y, Narita H (2008) In vitro and in vivo antifungal activities of T-2307, a novel arylamidine. Antimicrob Agent Chemother 52:1318–1324
Morano KA, Liu PC, Thiele DJ (1998) Protein chaperones and the heat shock response in saccharomyces cerevisiae. Curr Opin Microbiol 1:197–203
Muhlenhoff U, Hoffmann B, Richter N, Rietzschel N, Spantgar F, Stehling O, Uzarska MA, Lill R (2015) Compartmentalization of iron between mitochondria and the cytosol and its regulation. Eur J Cell Biol 94:292–308
Neef DW, Jaeger AM, Thiele DJ (2011) Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat Rev Drug Discov 10:930–944
Neef DW, Jaeger AM, Gomez-Pastor R, Willmund F, Frydman J, Thiele DJ (2014) A direct regulatory interaction between chaperonin TRiC and stress-responsive transcription factor HSF1. Cell Rep 9:955–966
Nicholls S, Leach MD, Priest CL, Brown AJ (2009) Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. Mol Microbiol 74:844–861
Nishikawa H, Fukuda Y, Mitsuyama J, Tashiro M, Tanaka A, Takazono T, Saijo T, Yamamoto K, Nakamura S, Imamura Y et al (2017) In vitro and in vivo antifungal activities of T-2307, a novel arylamidine, against Cryptococcus gattii: an emerging fungal pathogen. J Antimicrob Chemother 72:1709–1713
Nyhus KJ, Ozaki LS, Jacobson ES (2002) Role of mitochondrial carrier protein Mrs3/4 in iron acquisition and oxidative stress resistance of Cryptococcus neoformans. Med Mycol 40:581–591
Russell OM, Gorman GS, Lightowlers RN, Turnbull DM (2020) Mitochondrial diseases: hope for the future. Cell 181:168–188
Sabharwal SS, Schumacker PT (2014) Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles’ heel? Nat Rev Cancer 14:709–721
Samanovic MI, Ding C, Thiele DJ, Darwin KH (2012) Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11:106–115
Shibata T, Takahashi T, Yamada E, Kimura A, Nishikawa H, Hayakawa H, Nomura N, Mitsuyama J (2012) T-2307 causes collapse of mitochondrial membrane potential in yeast. Antimicrob Agents Chemother 56:5892–5897
Shingu-Vazquez M, Traven A (2011) Mitochondria and fungal pathogenesis: drug tolerance, virulence, and potential for antifungal therapy. Eukaryot Cell 10:1376–1383
Stott KE, Loyse A, Jarvis JN, Alufandika M, Harrison TS, Mwandumba HC, Day JN, Lalloo DG, Bicanic T, Perfect JR et al (2021) Cryptococcal meningoencephalitis: time for action. Lancet Infect Dis 21:e259–e271
Tang C, Cai J, Yin XM, Weinberg JM, Venkatachalam MA, Dong Z (2021) Mitochondrial quality control in kidney injury and repair. Nat Rev Nephrol 17:299–318
Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76:115–158
Verma S, Shakya VPS, Idnurm A (2018) Exploring and exploiting the connection between mitochondria and the virulence of human pathogenic fungi. Virulence 9:426–446
Vyas S, Zaganjor E, Haigis MC (2016) Mitochondria and Cancer. Cell 166:555–566
Wang Y, Xu J (2020) Mitochondrial genome polymorphisms in the human pathogenic fungus cryptococcus neoformans. Front Microbiol 11:706
Wiederhold NP (2021) Review of T-2307, an investigational agent that causes collapse of fungal mitochondrial membrane potential. J Fungi (basel) 7:130
Wiederrecht G, Seto D, Parker CS (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54:841–853
Yamashita K, Miyazaki T, Fukuda Y, Mitsuyama J, Saijo T, Shimamura S, Yamamoto K, Imamura Y, Izumikawa K, Yanagihara K et al (2019) The novel arylamidine T-2307 selectively disrupts yeast mitochondrial function by inhibiting respiratory chain complexes. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00374-19
doi: 10.1128/AAC.00374-19
Yang DH, Jung KW, Bang S, Lee JW, Song MH, Floyd-Averette A, Festa RA, Ianiri G, Idnurm A, Thiele DJ et al (2017) Rewiring of signaling networks modulating thermotolerance in the human pathogen cryptococcus neoformans. Genetics 205:201–219

Auteurs

Yang Meng (Y)

College of Life and Health Sciences, Northeastern University, Shenyang, China.

Chen Ding (C)

College of Life and Health Sciences, Northeastern University, Shenyang, China. dingchen@mail.neu.edu.cn.

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