Fungi’s Swiss Army Knife: Pleiotropic Effect of Melanin in Fungal Pathogenesis during Cattle Mycosis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Research Questions
2.2. Naive Search and Early Keywords
2.3. Obtaining the Final Keyword List
2.4. Bibliographic Main Searches in Specialized Databases
2.5. Creation and Processing of the Corpus
3. Results
3.1. Patterns of Research
3.2. Diversity of Cattle Fungal Disease
3.3. Virulence
4. Discussion
4.1. Diversity of Pathogenic Fungi and Mycoses in Cattle
4.2. Main Virulence Factors of Mammalian Pathogenic Fungi
4.3. Melanin as a Virulence Factor in Fungal Pathogenesis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gonçalves, S.C.; Haelewaters, D.; Furci, G.; Mueller, G.M. Include All Fungi in Biodiversity Goals. Science 2021, 373, 403. [Google Scholar] [CrossRef]
- Rodrigues, M.L.; Nosanchuk, J.D. Fungal Diseases as Neglected Pathogens: A Wake-up Call to Public Health Officials. PLoS Neglected Trop. Dis. 2020, 14, e0007964. [Google Scholar] [CrossRef] [PubMed]
- Seyedmousavi, S.; Guillot, J.; Tolooe, A.; Verweij, P.E.; de Hoog, G.S. Neglected Fungal Zoonoses: Hidden Threats to Man and Animals. Clin. Microbiol. Infect. 2015, 21, 416–425. [Google Scholar] [CrossRef] [PubMed]
- Brown, G.D.; Denning, D.W.; Gow, N.A.R.; Levitz, S.M.; Netea, M.G.; White, T.C. Hidden Killers: Human Fungal Infections. Sci. Transl. Med. 2012, 4, 165rv13. [Google Scholar] [CrossRef] [PubMed]
- Roth, C.; Murray, D.; Scott, A.; Fu, C.; Averette, A.F.; Sun, S.; Heitman, J.; Magwene, P.M. Pleiotropy and Epistasis within and between Signaling Pathways Defines the Genetic Architecture of Fungal Virulence. PLoS Genet. 2021, 17, e1009313. [Google Scholar] [CrossRef]
- Lockhart, S.R.; Etienne, K.A.; Vallabhaneni, S.; Farooqi, J.; Chowdhary, A.; Govender, N.P.; Colombo, A.L.; Calvo, B.; Cuomo, C.A.; Desjardins, C.A.; et al. Simultaneous Emergence of Multidrug-Resistant Candida Auris on 3 Continents Confirmed by Whole-Genome Sequencing and Epidemiological Analyses. Clin. Infect. Dis. 2017, 64, 134–140. [Google Scholar] [CrossRef]
- Casadevall, A.; Kontoyiannis, D.P.; Robert, V. On the Emergence of Candida Auris: Climate Change, Azoles, Swamps, and Birds. mBio 2019, 10, 10–1128. [Google Scholar] [CrossRef]
- Fisher, M.C.; Garner, T.W.J. Chytrid Fungi and Global Amphibian Declines. Nat. Rev. Microbiol. 2020, 18, 332–343. [Google Scholar] [CrossRef]
- Iorizzo, M.; Letizia, F.; Ganassi, S.; Testa, B.; Petrarca, S.; Albanese, G.; Di Criscio, D.; De Cristofaro, A. Recent Advances in the Biocontrol of Nosemosis in Honey Bees (Apis mellifera L.). J. Fungi 2022, 8, 424. [Google Scholar] [CrossRef]
- Marín-García, P.J.; Peyre, Y.; Ahuir-Baraja, A.E.; Garijo, M.M.; Llobat, L. The Role of Nosema ceranae (Microsporidia: Nosematidae) in Honey Bee Colony Losses and Current Insights on Treatment. Vet. Sci. 2022, 9, 130. [Google Scholar] [CrossRef]
- Nardoni, S.; Mancianti, F. Mycotic Diseases in Chelonians. J. Fungi 2023, 9, 518. [Google Scholar] [CrossRef]
- Gleason, F.H.; Allerstorfer, M.; Lilje, O. Newly Emerging Diseases of Marine Turtles, Especially Sea Turtle Egg Fusariosis (SEFT), Caused by Species in the Fusarium solani Complex (FSSC). Mycology 2020, 11, 184–194. [Google Scholar] [CrossRef] [PubMed]
- Gozlan, R.; Marshall, W.; Lilje, O.; Jessop, C.; Gleason, F.; Andreou, D. Current Ecological Understanding of Fungal-like Pathogens of Fish: What Lies Beneath? Front. Microbiol. 2014, 5, 62. [Google Scholar] [CrossRef]
- Hoyt, J.R.; Kilpatrick, A.M.; Langwig, K.E. Ecology and Impacts of White-Nose Syndrome on Bats. Nat. Rev. Microbiol. 2021, 19, 196–210. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef] [PubMed]
- Crous, P.W.; Gams, W.; Stalpers, J.A.; Robert, V.; Stegehuis, G. MycoBank: An Online Initiative to Launch Mycology into the 21st Century. Stud. Mycol. 2004, 50, 19–22. [Google Scholar]
- Robert, V.; Vu, D.; Amor, A.B.H.; van de Wiele, N.; Brouwer, C.; Jabas, B.; Szoke, S.; Dridi, A.; Triki, M.; ben Daoud, S.; et al. MycoBank Gearing up for New Horizons. IMA Fungus 2013, 4, 371–379. [Google Scholar] [CrossRef]
- Pang, K.-L.; Hassett, B.T.; Shaumi, A.; Guo, S.-Y.; Sakayaroj, J.; Chiang, M.W.-L.; Yang, C.-H.; Jones, E.B.G. Pathogenic Fungi of Marine Animals: A Taxonomic Perspective. Fungal Biol. Rev. 2021, 38, 92–106. [Google Scholar] [CrossRef]
- Wasson, K.; Peper, R.L. Mammalian Microsporidiosis. Vet. Pathol. 2000, 37, 113–128. [Google Scholar] [CrossRef]
- R Studio Team. RStudio: Integrated Development for R; R Foundation for Statistical Computing: Vienna, Austria, 2019. [Google Scholar]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020. [Google Scholar]
- Grames, E.M.; Stillman, A.N.; Tingley, M.W.; Elphick, C.S. An Automated Approach to Identifying Search Terms for Systematic Reviews Using Keyword Co-Occurrence Networks. Methods Ecol. Evol. 2019, 10, 1645–1654. [Google Scholar] [CrossRef]
- Benoit, K.; Watanabe, K.; Wang, H.; Nulty, P.; Obeng, A.; Müller, S.; Matsuo, A. Quanteda: An R Package for the Quantitative Analysis of Textual Data. J. Open Source Softw. 2018, 3, 774. [Google Scholar] [CrossRef]
- Speckman, R.A.; Friedly, J.L. Asking Structured, Answerable Clinical Questions Using the Population, Intervention/Comparator, Outcome (PICO) Framework. PMR 2019, 11, 548–553. [Google Scholar] [CrossRef] [PubMed]
- Gusenbauer, M.; Haddaway, N.R. Which Academic Search Systems Are Suitable for Systematic Reviews or Meta-Analyses? Evaluating Retrieval Qualities of Google Scholar, PubMed, and 26 Other Resources. Res. Synth. Methods 2020, 11, 181–217. [Google Scholar] [CrossRef] [PubMed]
- Kanehisa, M.; Furumichi, M.; Sato, Y.; Ishiguro-Watanabe, M.; Tanabe, M. KEGG: Integrating Viruses and Cellular Organisms. Nucleic Acids Res. 2021, 49, D545–D551. [Google Scholar] [CrossRef] [PubMed]
- Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic Local Alignment Search Tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef]
- Ondov, B.D.; Bergman, N.H.; Phillippy, A.M. Interactive Metagenomic Visualization in a Web Browser. BMC Bioinform. 2011, 12, 385. [Google Scholar] [CrossRef]
- Du, J.; Wang, X.; Luo, H.; Wang, Y.; Liu, X.; Zhou, X. Epidemiological Investigation of Non-Albicans Candida Species Recovered from Mycotic Mastitis of Cows in Yinchuan, Ningxia of China. BMC Vet. Res. 2018, 14, 251. [Google Scholar] [CrossRef] [PubMed]
- Fernandes, C.; Mota, M.; Barros, L.; Dias, M.I.; Ferreira, I.C.F.R.; Piedade, A.P.; Casadevall, A.; Gonçalves, T. Pyomelanin Synthesis in Alternaria Alternata Inhibits DHN-Melanin Synthesis and Decreases Cell Wall Chitin Content and Thickness. Front. Microbiol. 2021, 12, 691433. [Google Scholar] [CrossRef]
- Chongkae, S.; Nosanchuk, J.D.; Pruksaphon, K.; Laliam, A.; Pornsuwan, S.; Youngchim, S. Production of Melanin Pigments in Saprophytic Fungi in Vitro and during Infection. J. Basic Microbiol. 2019, 59, 1092–1104. [Google Scholar] [CrossRef]
- Suri, V.; Pandey, S.; Goyal, N.; Rani, H. Cladophialophora bantiana Brain Abscess with Lymphadenitis. BMJ Case Rep. CP 2021, 14, e246108. [Google Scholar] [CrossRef]
- Romsdahl, J.; Schultzhaus, Z.; Cuomo, C.A.; Dong, H.; Abeyratne-Perera, H.; Hervey, W.J.; Wang, Z. Phenotypic Characterization and Comparative Genomics of the Melanin-Producing Yeast Exophiala lecanii-corni Reveals a Distinct Stress Tolerance Profile and Reduced Ribosomal Genetic Content. J. Fungi 2021, 7, 1078. [Google Scholar] [CrossRef]
- Cunha, M.M.; Franzen, A.J.; Seabra, S.H.; Herbst, M.H.; Vugman, N.V.; Borba, L.P.; de Souza, W.; Rozental, S. Melanin in Fonsecaea pedrosoi: A Trap for Oxidative Radicals. BMC Microbiol. 2010, 10, 80. [Google Scholar] [CrossRef] [PubMed]
- Keizer, E.M.; Valdes, I.D.; McCann, B.L.; Bignell, E.M.; Wösten, H.A.B.; de Cock, H. The Protective Role of 1,8-Dihydroxynaphthalene–Melanin on Conidia of the Opportunistic Human Pathogen Aspergillus fumigatus Revisited: No Role in Protection against Hydrogen Peroxide and Superoxides. mSphere 2022, 7, e00874-21. [Google Scholar] [CrossRef] [PubMed]
- Sun, W.; Yu, Y.; Chen, J.; Yu, B.; Chen, T.; Ying, H.; Zhou, S.; Ouyang, P.; Liu, D.; Chen, Y. Light Signaling Regulates Aspergillus niger Biofilm Formation by Affecting Melanin and Extracellular Polysaccharide Biosynthesis. mBio 2021, 12, e03434-20. [Google Scholar] [CrossRef] [PubMed]
- Palonen, E.K.; Raina, S.; Brandt, A.; Meriluoto, J.; Keshavarz, T.; Soini, J.T. Melanisation of Aspergillus terreus—Is Butyrolactone I Involved in the Regulation of Both DOPA and DHN Types of Pigments in Submerged Culture? Microorganisms 2017, 5, 22. [Google Scholar] [CrossRef]
- Babitskaia, V.G.; Shcherba, V.V.; Filimonova, T.V.; Grigorchuk, E.Z. Melanin pigments of the fungi Paecilomyces variotii and Aspergillus carbonarius. Prikl. Biokhimiia Mikrobiol. 2000, 36, 153–159. [Google Scholar]
- Liu, S.; Youngchim, S.; Zamith-Miranda, D.; Nosanchuk, J.D. Fungal Melanin and the Mammalian Immune System. J. Fungi 2021, 7, 264. [Google Scholar] [CrossRef]
- Youngchim, S.; Pornsuwan, S.; Nosanchuk, J.D.; Dankai, W.; Vanittanakom, N. Melanogenesis in Dermatophyte Species in Vitro and during Infection. Microbiology 2011, 157, 2348–2356. [Google Scholar] [CrossRef]
- Ben Tahar, I.; Kus-Liśkiewicz, M.; Lara, Y.; Javaux, E.; Fickers, P. Characterization of a Nontoxic Pyomelanin Pigment Produced by the Yeast Yarrowia lipolytica. Biotechnol. Prog. 2020, 36, e2912. [Google Scholar] [CrossRef]
- Noguchi, H.; Matsumoto, T.; Kimura, U.; Hiruma, M.; Kano, R.; Yaguchi, T.; Fukushima, S.; Ihn, H. Fungal Melanonychia Caused by Candida parapsilosis Successfully Treated with Oral Fosravuconazole. J. Dermatol. 2019, 46, 911–913. [Google Scholar] [CrossRef]
- Jeon, G.; Kim, Y.; Choi, S.Y.; Kim, Y.-H.; Min, J. Melanin Decolorization by Lysosome-Related Extract in Saccharomyces cerevisiae Modified to Overproduce Glutathione Peroxidase. Appl. Microbiol. Biotechnol. 2021, 105, 8715–8725. [Google Scholar] [CrossRef]
- Vijay, K.; Devi, T.S.; Sree, K.K.; Elgorban, A.M.; Kumar, P.; Govarthanan, M.; Kavitha, T. In Vitro Screening and in Silico Prediction of Antifungal Metabolites from Rhizobacterium Achromobacter kerstersii JKP9. Arch. Microbiol. 2020, 202, 2855–2864. [Google Scholar] [CrossRef] [PubMed]
- Youngchim, S.; Nosanchuk, J.D.; Pornsuwan, S.; Kajiwara, S.; Vanittanakom, N. The Role of L-DOPA on Melanization and Mycelial Production in Malassezia Furfur. PLoS ONE 2013, 8, e63764. [Google Scholar] [CrossRef] [PubMed]
- Gaitanis, G.; Magiatis, P.; Hantschke, M.; Bassukas, I.D.; Velegraki, A. The Malassezia Genus in Skin and Systemic Diseases. Clin. Microbiol. Rev. 2012, 25, 106–141. [Google Scholar] [CrossRef]
- Brilhante, R.S.N.; da Rocha, M.G.; de Guedes, G.M.M.; de Oliveira, J.S.; dos Santos Araújo, G.; España, J.D.A.; Sales, J.A.; de Aguiar, L.; de Paiva, M.A.N.; de Cordeiro, R.A.; et al. Malassezia pachydermatis from Animals: Planktonic and Biofilm Antifungal Susceptibility and Its Virulence Arsenal. Vet. Microbiol. 2018, 220, 47–52. [Google Scholar] [CrossRef] [PubMed]
- Danesi, P.; Falcaro, C.; Schmertmann, L.J.; de Miranda, L.H.M.; Krockenberger, M.; Malik, R. Cryptococcus in Wildlife and Free-Living Mammals. J. Fungi 2021, 7, 29. [Google Scholar] [CrossRef] [PubMed]
- Asadzadeh, M.; Ahmad, S.; Ziauddin, K.; Verghese, S.; Joseph, L. Molecular Identification, Genotypic Heterogeneity and Comparative Pathogenicity of Environmental Isolates of Papiliotrema Laurentii. J. Med. Microbiol. 2020, 69, 1285–1292. [Google Scholar] [CrossRef]
- Figueiredo-Carvalho, M.H.G.; dos Santos, F.B.; Nosanchuk, J.D.; Zancope-Oliveira, R.M.; Almeida-Paes, R. L-Dihydroxyphenylalanine Induces Melanin Production by Members of the Genus Trichosporon. FEMS Yeast Res. 2014, 14, 988–991. [Google Scholar] [CrossRef] [PubMed]
- Reyes-Fernández, E.Z.; Shi, Y.-M.; Grün, P.; Bode, H.B.; Bölker, M. An Unconventional Melanin Biosynthesis Pathway in Ustilago maydis. Appl. Environ. Microbiol. 2021, 87, e01510-20. [Google Scholar] [CrossRef]
- Knudtson, W.U.; Kirkbride, C.A. Fungi Associated with Bovine Abortion in the Northern Plains States (USA). J. Vet. Diagn. Investig. 1992, 4, 181–185. [Google Scholar] [CrossRef]
- Jacobsen, I.D. Animal Models to Study Mucormycosis. J. Fungi 2019, 5, 27. [Google Scholar] [CrossRef]
- Thywißen, A.; Heinekamp, T.; Dahse, H.-M.; Schmaler-Ripcke, J.; Nietsche, S.; Zipfel, P.; Brakhage, A. Conidial Dihydroxynaphthalene Melanin of the Human Pathogenic Fungus Aspergillus fumigatus Interferes with the Host Endocytosis Pathway. Front. Microbiol. 2011, 2, 96. [Google Scholar] [CrossRef]
- Friedrich, D.; Zapf, D.; Lohse, B.; Fecher, R.A.; Deepe, G.S.; Rupp, J. The HIF-1α/LC3-II Axis Impacts Fungal Immunity in Human Macrophages. Infect. Immun. 2019, 87, 10–1128. [Google Scholar] [CrossRef]
- Zhang, J.; Wang, L.; Xi, L.; Huang, H.; Hu, Y.; Li, X.; Huang, X.; Lu, S.; Sun, J. Melanin in a Meristematic Mutant of Fonsecaea monophora Inhibits the Production of Nitric Oxide and Th1 Cytokines of Murine Macrophages. Mycopathologia 2013, 175, 515–522. [Google Scholar] [CrossRef] [PubMed]
- Awandkar, S.P.; Kulkarni, M.B.; Agnihotri, A.A.; Chavan, V.G.; Chincholkar, V.V. Novel Fluconazole-Resistant Zoonotic Yeast Isolated from Mastitis. Anim. Biotechnol. 2021, 34, 746–755. [Google Scholar] [CrossRef]
- Elad, D.; Segal, E. Diagnostic Aspects of Veterinary and Human Aspergillosis. Front. Microbiol. 2018, 9, 1303. [Google Scholar] [CrossRef] [PubMed]
- Pesca, C.; Cruciani, D.; Agostini, L.; Rossi, E.; Pavone, S.; Stazi, M.; Mangili, P.; Crotti, S. Simultaneous Detection of Aspergillus nidulans, Aspergillus luchuensis and lichtheimia Sp. in a Bovine Abortion. J. Mycol. Médicale 2020, 30, 100923. [Google Scholar] [CrossRef] [PubMed]
- Seyedmousavi, S.; Guillot, J.; Arné, P.; de Hoog, G.S.; Mouton, J.W.; Melchers, W.J.G.; Verweij, P.E. Aspergillus and Aspergilloses in Wild and Domestic Animals: A Global Health Concern with Parallels to Human Disease. Med. Mycol. 2015, 53, 765–797. [Google Scholar] [CrossRef]
- Carpouron, J.; de Hoog, S.; Gentekaki, E.; Hyde, K. Emerging and Epizootic Fungal Infections in Animals; Seyedmousavi, S., De Hoog, G.S., Guillot, J., Verweij, P.E., Eds.; Springer International Publishing: Cham, Switzerland, 2018; ISBN 978-3-319-72091-3. [Google Scholar]
- Papkou, A.; Schalkowski, R.; Barg, M.-C.; Koepper, S.; Schulenburg, H. Population Size Impacts Host–Pathogen Coevolution. Proc. R. Soc. B Biol. Sci. 2021, 288, 20212269. [Google Scholar] [CrossRef]
- Masri, L.; Branca, A.; Sheppard, A.E.; Papkou, A.; Laehnemann, D.; Guenther, P.S.; Prahl, S.; Saebelfeld, M.; Hollensteiner, J.; Liesegang, H.; et al. Host–Pathogen Coevolution: The Selective Advantage of Bacillus thuringiensis Virulence and Its Cry Toxin Genes. PLoS Biol. 2015, 13, e1002169. [Google Scholar] [CrossRef]
- Woolhouse, M.E.J.; Webster, J.P.; Domingo, E.; Charlesworth, B.; Levin, B.R. Biological and Biomedical Implications of the Co-Evolution of Pathogens and Their Hosts. Nat. Genet. 2002, 32, 569–577. [Google Scholar] [CrossRef] [PubMed]
- Buckingham, L.J.; Ashby, B. Coevolutionary Theory of Hosts and Parasites. J. Evol. Biol. 2022, 35, 205–224. [Google Scholar] [CrossRef]
- Casadevall, A. Fungi and the Rise of Mammals. PLoS Pathog. 2012, 8, e1002808. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, M.; Casadevall, A. Phagosome Extrusion and Host-Cell Survival after Cryptococcus neoformans Phagocytosis by Macrophages. Curr. Biol. 2006, 16, 2161–2165. [Google Scholar] [CrossRef] [PubMed]
- Rosas, Á.L.; Casadevall, A. Melanization Affects Susceptibility of Cryptococcus neoformans to Heat and Cold. FEMS Microbiol. Lett. 1997, 153, 265–272. [Google Scholar] [CrossRef]
- Biegańska, M.J. Two Fundamentals of Mammalian Defense in Fungal Infections: Endothermy and Innate Antifungal Immunity. Pol. J. Vet. Sci. 2014, 17, 555–567. [Google Scholar] [CrossRef]
- Husband, A.J. Overview of the Mammalian Immune System. In Advances in Nutritional Research: Immunological Properties of Milk; Woodward, B., Draper, H.H., Eds.; Advances in Nutritional Research; Springer: Boston, MA, USA, 2001; pp. 3–14. ISBN 978-1-4615-0661-4. [Google Scholar]
- Köhler, J.R.; Hube, B.; Puccia, R.; Casadevall, A.; Perfect, J.R. Fungi That Infect Humans. Microbiol. Spectr. 2017, 5, 3–5. [Google Scholar] [CrossRef] [PubMed]
- Robert, V.A.; Casadevall, A. Vertebrate Endothermy Restricts Most Fungi as Potential Pathogens. J. Infect. Dis. 2009, 200, 1623–1626. [Google Scholar] [CrossRef]
- Casadevall, A. Fungal Virulence, Vertebrate Endothermy, and Dinosaur Extinction: Is There a Connection? Fungal Genet. Biol. 2005, 42, 98–106. [Google Scholar] [CrossRef]
- Blackwell, M. The Fungi: 1, 2, 3 … 5.1 Million Species? Am. J. Bot. 2011, 98, 426–438. [Google Scholar] [CrossRef]
- Casadevall, A. Immunity to Invasive Fungal Diseases. Annu. Rev. Immunol. 2022, 40, 121–141. [Google Scholar] [CrossRef]
- Kappe, R.; Rimek, D. Fungal Diseases. In Antifungal Agents: Advances and Problems; Müller, J., Polak, A., Kappe, R., Rimek, D., Seibold, M., Tintelnot, K., Jucker, E., Eds.; Special Topic; Birkhäuser: Basel, Switzerland, 2003; pp. 13–38. ISBN 978-3-0348-7974-3. [Google Scholar]
- Müller, J.; Polak, A.; Kappe, R.; Rimek, D.; Seibold, M.; Tintelnot, K. Antifungal Agents: Advances and Problems; Jucker, E., Ed.; Birkhäuser: Basel, Switzerland, 2003; ISBN 978-3-7643-6926-2. [Google Scholar]
- Balkema-Buschmann, A.; Fast, C.; Kaatz, M.; Eiden, M.; Ziegler, U.; McIntyre, L.; Keller, M.; Hills, B.; Groschup, M.H. Pathogenesis of Classical and Atypical BSE in Cattle. Prev. Vet. Med. 2011, 102, 112–117. [Google Scholar] [CrossRef]
- Garcia-Solache, M.A.; Casadevall, A. Phylogenetics and Evolution of Virulence in the Kingdom Fungi. In Evolution of Virulence in Eukaryotic Microbes; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2012; pp. 70–90. ISBN 978-1-118-30816-5. [Google Scholar]
- Bultman, K.M.; Kowalski, C.H.; Cramer, R.A. Aspergillus fumigatus Virulence through the Lens of Transcription Factors. Med. Mycol. 2017, 55, 24–38. [Google Scholar] [CrossRef]
- Zaragoza, O. Basic Principles of the Virulence of Cryptococcus. Virulence 2019, 10, 490–501. [Google Scholar] [CrossRef] [PubMed]
- Hohl, T.M. Overview of Vertebrate Animal Models of Fungal Infection. J. Immunol. Methods 2014, 410, 100–112. [Google Scholar] [CrossRef]
- Torres, M.; Pinzón, E.N.; Rey, F.M.; Martinez, H.; Parra Giraldo, C.M.; Celis Ramírez, A.M. Galleria mellonella as a Novelty in Vivo Model of Host-Pathogen Interaction for Malassezia furfur CBS 1878 and Malassezia pachydermatis CBS 1879. Front. Cell. Infect. Microbiol. 2020, 10, 199. [Google Scholar] [CrossRef]
- Brown, N.A.; Goldman, G.H. The Contribution of Aspergillus fumigatus Stress Responses to Virulence and Antifungal Resistance. J. Microbiol. 2016, 54, 243–253. [Google Scholar] [CrossRef] [PubMed]
- Casadevall, A.; Steenbergen, J.N.; Nosanchuk, J.D. ‘Ready Made’ Virulence and ‘Dual Use’ Virulence Factors in Pathogenic Environmental Fungi—The Cryptococcus neoformans Paradigm. Curr. Opin. Microbiol. 2003, 6, 332–337. [Google Scholar] [CrossRef] [PubMed]
- Ma, H.; May, R.C. Chapter 5 Virulence in Cryptococcus Species. In Advances in Applied Microbiology; Academic Press: Cambridge, MA, USA, 2009; Volume 67, pp. 131–190. [Google Scholar]
- de Sousa, H.R.; de Frazão, S.; de Oliveira Júnior, G.P.; Albuquerque, P.; Nicola, A.M. Cryptococcal Virulence in Humans: Learning from Translational Studies with Clinical Isolates. Front. Cell. Infect. Microbiol. 2021, 11, 657502. [Google Scholar] [CrossRef] [PubMed]
- Bouklas, T.; Fries, B.C. Aging: An Emergent Phenotypic Trait That Contributes to the Virulence of Cryptococcus neoformans. Future Microbiol. 2015, 10, 191–197. [Google Scholar] [CrossRef]
- Orner, E.P.; Bhattacharya, S.; Kalenja, K.; Hayden, D.; Del Poeta, M.; Fries, B.C. Cell Wall-Associated Virulence Factors Contribute to Increased Resilience of Old Cryptococcus neoformans Cells. Front. Microbiol. 2019, 10, 2513. [Google Scholar] [CrossRef]
- Bhattacharya, S.; Holowka, T.; Orner, E.P.; Fries, B.C. Gene Duplication Associated with Increased Fluconazole Tolerance in Candida auris Cells of Advanced Generational Age. Sci. Rep. 2019, 9, 5052. [Google Scholar] [CrossRef]
- Bouklas, T.; Alonso-Crisóstomo, L.; Székely, T., Jr.; Diago-Navarro, E.; Orner, E.P.; Smith, K.; Munshi, M.A.; Poeta, M.D.; Balázsi, G.; Fries, B.C. Generational Distribution of a Candida Glabrata Population: Resilient Old Cells Prevail, While Younger Cells Dominate in the Vulnerable Host. PLoS Pathog. 2017, 13, e1006355. [Google Scholar] [CrossRef]
- Silva, V.K.A.; Bhattacharya, S.; Oliveira, N.K.; Savitt, A.G.; Zamith-Miranda, D.; Nosanchuk, J.D.; Fries, B.C. Replicative Aging Remodels the Cell Wall and Is Associated with Increased Intracellular Trafficking in Human Pathogenic Yeasts. mBio 2021, 13, e0019022. [Google Scholar] [CrossRef] [PubMed]
- Cordero, R.J.B.; Casadevall, A. Melanin. Curr. Biol. 2020, 30, R142–R143. [Google Scholar] [CrossRef]
- Eisenman, H.C.; Casadevall, A. Synthesis and Assembly of Fungal Melanin. Appl. Microbiol. Biotechnol. 2012, 93, 931–940. [Google Scholar] [CrossRef]
- Suwannarach, N.; Kumla, J.; Watanabe, B.; Matsui, K.; Lumyong, S. Characterization of Melanin and Optimal Conditions for Pigment Production by an Endophytic Fungus, Spissiomyces endophytica SDBR-CMU319. PLoS ONE 2019, 14, e0222187. [Google Scholar] [CrossRef]
- Casadevall, A.; Rosas, A.L.; Nosanchuk, J.D. Melanin and Virulence in Cryptococcus neoformans. Curr. Opin. Microbiol. 2000, 3, 354–358. [Google Scholar] [CrossRef]
- Smith, D.F.Q.; Casadevall, A. The Role of Melanin in Fungal Pathogenesis for Animal Hosts. In Fungal Physiology and Immunopathogenesis; Rodrigues, M.L., Ed.; Current Topics in Microbiology and Immunology; Springer International Publishing: Cham, Switzerland, 2019; pp. 1–30. ISBN 978-3-030-30237-5. [Google Scholar]
- Gessler, N.N.; Egorova, A.S.; Belozerskaya, T.A. Melanin Pigments of Fungi under Extreme Environmental Conditions (Review). Appl. Biochem. Microbiol. 2014, 50, 105–113. [Google Scholar] [CrossRef]
- Camacho, E.; Vij, R.; Chrissian, C.; Prados-Rosales, R.; Gil, D.; O’Meally, R.N.; Cordero, R.J.B.; Cole, R.N.; McCaffery, J.M.; Stark, R.E.; et al. The Structural Unit of Melanin in the Cell Wall of the Fungal Pathogen Cryptococcus Neoformans. J. Biol. Chem. 2019, 294, 10471–10489. [Google Scholar] [CrossRef] [PubMed]
- Nosanchuk, J.D.; Rosas, A.L.; Casadevall, A. The Antibody Response to Fungal Melanin in Mice. J. Immunol. 1998, 160, 6026–6031. [Google Scholar] [CrossRef] [PubMed]
- Irfan, M.; Almotiri, A.; AlZeyadi, Z.A. Antimicrobial Resistance and Its Drivers—A Review. Antibiotics 2022, 11, 1362. [Google Scholar] [CrossRef]
- Vitiello, A.; Ferrara, F.; Boccellino, M.; Ponzo, A.; Cimmino, C.; Comberiati, E.; Zovi, A.; Clemente, S.; Sabbatucci, M. Antifungal Drug Resistance: An Emergent Health Threat. Biomedicines 2023, 11, 1063. [Google Scholar] [CrossRef] [PubMed]
- Fisher, M.C.; Alastruey-Izquierdo, A.; Berman, J.; Bicanic, T.; Bignell, E.M.; Bowyer, P.; Bromley, M.; Brüggemann, R.; Garber, G.; Cornely, O.A.; et al. Tackling the Emerging Threat of Antifungal Resistance to Human Health. Nat. Rev. Microbiol. 2022, 20, 557–571. [Google Scholar] [CrossRef] [PubMed]
- Bossche, H.V.; Engelen, M.; Rochette, F. Antifungal Agents of Use in Animal Health—Chemical, Biochemical and Pharmacological Aspects. J. Vet. Pharmacol. Ther. 2003, 26, 5–29. [Google Scholar] [CrossRef]
- Bhanderi, B.; Yadav, M.; Roy, A. Antifungal Drug Resistance-Concerns for Veterinarians. Vet. World 2009, 2, 204–207. [Google Scholar] [CrossRef]
- Rossi, G.R.; Cervi, L.A.; García, M.M.; Chiapello, L.S.; Sastre, D.A.; Masih, D.T. Involvement of Nitric Oxide in Protecting Mechanism during Experimental Cryptococcosis. Clin. Immunol. 1999, 90, 256–265. [Google Scholar] [CrossRef]
- Lane, T.E.; Otero, G.C.; Wu-Hsieh, B.A.; Howard, D.H. Expression of Inducible Nitric Oxide Synthase by Stimulated Macrophages Correlates with Their Antihistoplasma Activity. Infect. Immun. 1994, 62, 1478–1479. [Google Scholar] [CrossRef]
- Fernandes, K.S.S.; Coelho, A.L.J.; Bezerra, L.M.L.; Barja-Fidalgo, C. Virulence of Sporothrix schenckii Conidia and Yeast Cells, and Their Susceptibility to Nitric Oxide. Immunology 2000, 101, 563–569. [Google Scholar] [CrossRef]
- de Oliveira Frazão, S.; de Sousa, H.R.; da Silva, L.G.; dos Santos Folha, J.; de Melo Gorgonha, K.C.; de Oliveira, G.P.; Felipe, M.S.S.; Silva-Pereira, I.; Casadevall, A.; Nicola, A.M.; et al. Laccase Affects the Rate of Cryptococcus neoformans Nonlytic Exocytosis from Macrophages. mBio 2020, 11, e02085-20. [Google Scholar] [CrossRef]
- Ma, H.; Croudace, J.E.; Lammas, D.A.; May, R.C. Expulsion of Live Pathogenic Yeast by Macrophages. Curr. Biol. 2006, 16, 2156–2160. [Google Scholar] [CrossRef]
- Cordero, R.J.B.; Camacho, E.; Casadevall, A. Melanization in Cryptococcus neoformans Requires Complex Regulation. mBio 2020, 11, e03313-19. [Google Scholar] [CrossRef] [PubMed]
- Volling, K.; Thywissen, A.; Brakhage, A.A.; Saluz, H.P. Phagocytosis of Melanized Aspergillus Conidia by Macrophages Exerts Cytoprotective Effects by Sustained PI3K/Akt Signalling. Cell. Microbiol. 2011, 13, 1130–1148. [Google Scholar] [CrossRef]
Core Concept | Associated Search Terms |
---|---|
Fungi | aspergillus OR candida OR cryptococcus OR enterocytozoon OR exophiala OR fonsecaea OR fungal OR fungi OR fungus OR histoplasma OR paracoccidioides OR penicillium OR sporothrix OR talaromyces OR trichophyton OR yeast |
Host | bovid OR bovine OR bovino OR bullocks OR bulls OR calves OR cattle OR cow OR dairy OR livestock |
Melanin | melanin OR melanogenesis OR melanotic |
Mycosis | aspergillosis OR blastomycosis OR candidiasis OR chromoblastomycosis OR coccidioidomycosis OR cryptococcosis OR dermatophytosis OR epizootic OR abortions OR keratomycosis OR lymphangitis OR maduromycosis OR mastitis OR mucormycosis OR mycetoma OR mycotic OR mycosis OR mycoses OR paracoccidioidomycosis OR phaeomycosis OR pithomycotoxicosis OR pythiosis OR ringworm OR sporotrichosis OR zygomycosis |
Question | Keywords String | Data Base | Processed Articles | |
---|---|---|---|---|
Q1 | “fungal AND disease AND cattle” | PubMed | 21,794 18,017 15,133 | 54,944 |
“bacterial AND disease AND cattle” | ||||
“viral AND disease AND cattle” | ||||
Q2–Q4 | “associated with the fungi concept” AND “associated with the host concept” AND “associated with the concept mycosis” | PubMed Scopus WoS | 417 758 238 | 1413 |
Q5–Q6 | “associated with the fungi concept” AND “ “associated with the concept melanin” | PubMed Scopus WoS | 187 128 120 | 435 |
Criteria | Type | |
---|---|---|
1 | At least one of the keywords associated with each search concept present in the title or abstract | Automatic |
2 | The article is not duplicated within the corpus | Automatic |
3 | The article is in English | Automatic |
4 | It was selected by context in R (questions Q5–Q6 only) associated with one of the connecting words, established | Automatic |
5 | The article contains some unusual term in capital letters (we did this with the help of the “keep tokens” function and the regular expression “[^[:UPPER:]^]” in R, only questions Q2–Q4) | Automatic |
6 | Explicitly mentions a pathogenic fungal species or describes a melanin-associated virulence mechanism | Manual |
Mycosis Type | Mycosis | Predominant Mycosis-Causing Agent |
---|---|---|
Cutaneous, superficial, ringworm or dermatophytosis | Pheomycosis | Alternaria alternata |
Epizootic Lymphangitis | Trichophyton verrucosum | |
Mycetoma or maduromycosis | Cochliobolus spiciferus | |
Curvularia geniculata | ||
Drechslera rostratum | ||
Madurella mycetomatis | ||
Pseudallescheria boydii | ||
Pythiosis | Pythium insidiosum | |
Keratomycosis | Mortierella wolfii | |
Ringworm | Cladophiolophora bantiana | |
Microsporum canis | ||
Trichophyton mentagrophytes | ||
Subcutaneous | Chromoblastomycosis | Fonsecaea monophora |
Fonsecaea pedrosoi | ||
Sporotrichosis | Sporothrix schenckii and another ssp. | |
Systemic, primary, internal, disseminated or deep | Cattle Mycotic abortion | Aspergillus fumigatus |
Aspergillus nidulans | ||
Candida albicans | ||
Emericella nidulan | ||
Lichtheimia corymbifera | ||
Mortierella wolfii | ||
Rhizomucor pusillus | ||
Rhizopus arrhizus | ||
Aspergillosis | Aspergillus fumigatus and another ssp. | |
Blastomycosis | Blastomyces dermatitidis | |
Candidiasis | Candida albicans and another ssp. | |
Coccidioidomycosis | Coccidioides immitis | |
Cryptococcosis | Cryptococcus neoformans | |
Histoplasmosis | Histoplasma capsulatum | |
Fungal mastitis | Aspergillus fumigatus | |
Aureobasidium pullulans | ||
Candida albicans and another ssp. | ||
Candida parapsilosis | ||
Cryptococcus neoformans | ||
Prototheca zopfii | ||
Trichosporon mucoides | ||
Paracoccidioidomycosis | Paracoccidioides brasiliensis | |
Zygomycosis or Mucormycosis | Syncephalastrum racemosum | |
Cunninghamella bertholletiae | ||
Saksenaea vasiformis |
Division | Species |
---|---|
Ascomycota | Aureobasidium pullulans [29] |
Alternaria alternata [30] | |
Exserohilum rostratum [31] | |
Cladophialophora bantiana [32] | |
Exophiala dermatitidis [33] | |
Fonsecaea pedrosoi [34] | |
Aspergillus flavus [31] | |
Aspergillus fumigatus [33] | |
Aspergillus nidulans [35] | |
Aspergillus niger [36] | |
Aspergillus terreus [37] | |
Paecilomyces variotii [38] | |
Blastomyces dermatitidis [39] | |
Histoplasma capsulatum [39] | |
Paracoccidioides brasiliensis [39] | |
Trichophyton rubrum [40] | |
Yarrowia lipolytica [41] | |
Candida albicans [39] | |
Candida parapsilosis [42] | |
Saccharomyces cerevisiae [43] | |
Fusarium oxysporum [44] | |
Sporothrix schenckii [39] | |
Basidiomycota | Malassezia furfur [45] |
Malassezia obtusa [46] | |
Malassezia pachydermatis [47] | |
Malassezia sympodialis [46] | |
Cryptococcus neoformans [48] | |
Papiliotrema laurentii [49] | |
Trichosporon asahii [50] | |
Ustilago maydis [51] | |
Mortierellomycota | Actinomortierella wolfii [52] |
Mucoromycota | Lichtheimia corymbifera [53] |
Mucor hiemalis [53] | |
Rhizopus arrhizus [53] | |
Rhizopus microsporus [53] |
Fungi | Aspergillus fumigatus | Histoplasma capsulatum | Fonsecaea monophora |
Model | Mus musculus | Homo sapiens | Mus musculus |
Way | Proton-dependent phagolysosomal acidification type V ATPases | Expression of Hypoxia-inducible Factor 1HFI-1 | Type II interferon signaling associated with macrophage activation |
Target | V-type proton ATPases | HIF-1-alpha | Nitric Oxide Synthase, inducible (iNOS) |
Identity B.taurus | 91% | 94% | 88% |
Source | [54] | [55] | [56] |
KEGG link | KEGG T01008: 338038 | KEGG T01008: 281814 | KEGG T01008: 282876 |
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© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Romero, V.; Kalinhoff, C.; Saa, L.R.; Sánchez, A. Fungi’s Swiss Army Knife: Pleiotropic Effect of Melanin in Fungal Pathogenesis during Cattle Mycosis. J. Fungi 2023, 9, 929. https://doi.org/10.3390/jof9090929
Romero V, Kalinhoff C, Saa LR, Sánchez A. Fungi’s Swiss Army Knife: Pleiotropic Effect of Melanin in Fungal Pathogenesis during Cattle Mycosis. Journal of Fungi. 2023; 9(9):929. https://doi.org/10.3390/jof9090929
Chicago/Turabian StyleRomero, Víctor, Carolina Kalinhoff, Luis Rodrigo Saa, and Aminael Sánchez. 2023. "Fungi’s Swiss Army Knife: Pleiotropic Effect of Melanin in Fungal Pathogenesis during Cattle Mycosis" Journal of Fungi 9, no. 9: 929. https://doi.org/10.3390/jof9090929