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Fungal G-Protein Coupled Receptors: Mediators of 2 Pathogenesis and Targets for Disease Control

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Fungal G-Protein Coupled Receptors: Mediators of 2 Pathogenesis and Targets for Disease Control Citation for published version: Brown, N, Schrevens, S, van Dijck, P & Goldman, G 2018, 'Fungal G-protein-coupled receptors: mediators of pathogenesis and targets for disease control', Nature Microbiology, vol. 3, pp. 402–414. https://doi.org/10.1038/s41564-018-0127-5 DOI: 10.1038/s41564-018-0127-5 Publication date: 2018 Document Version Peer reviewed version Link to publication University of Bath Alternative formats If you require this document in an alternative format, please contact: [email protected] General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 29. Sep. 2021 1 Fungal G-protein coupled receptors: mediators of 2 pathogenesis and targets for disease control 3 Neil Andrew Brown1,2*, Sanne Schrevens3,4, Patrick van Dijck3,4, Gustavo Henrique Goldman5* 4 1 Biointeractions and Crop Protection, Rothamsted Research, Hertfordshire, UK. 2 Department of Biology 5 & Biochemistry, University of Bath, Claverton Down, Bath, BA2 7AY, UK. 3 VIB-KU Leuven Center for 6 Microbiology, KU Leuven, Flanders, Belgium. 4 Laboratory of Molecular Cell Biology, Institute of Botany 7 and Microbiology, KU Leuven, B-3001 Leuven, Belgium. 5 Faculdade de Ciências Farmacêuticas, 8 Universidade de São Paulo, Ribeirão Preto, Brazil. 9 *joint corresponding authors 10 Contact details 11 Dr Neil A. Brown Prof Gustavo H. Goldman 12 Biointeractions and Crop Protection Faculdade de Ciências Farmacêuticas 13 Rothamsted Research Universidade de São Paulo 14 Harpenden, Herts, AL5 2JQ, UK Ribeirão Preto, São Paulo, Brazil 15 Telephone: +44 (0) 1582763133 x 2461 Telephone: +55(16)33154280 16 [email protected] [email protected] 17 Manuscript details 18 Length: 5840 words 19 Display items: 4 figures and 1 table 20 References: 143 21 Glossary box 22 G-protein – Guanine nucleotide-binding protein. They often form a heterotrimeric G-protein complex 23 consisting of α, β, and ɣ subunits. G-proteins act as intracellular molecular switches, transmitting signals 24 perceived by cell surface receptors. Activity is modulated by their GTP-GDP bound state. 25 GPCR – G-protein coupled receptors are transmembrane receptors that perceive extracellular stimuli 26 and initiate intracellular signalling events. They commonly have 7 transmembrane domains and are 27 associated with intracellular G-proteins. 28 MAPK – Mitogen-activated protein kinase. MAPK signal transduction cascades are highly conserved and 29 coordinate cellular response to a wide range of stimuli. 1 30 PKA – Protein Kinase A. It is a highly-conserved kinase complex that is activated by cellular cAMP levels, 31 regulating metabolism and development. 32 Ascomyceta/ Basidiomyceta – Phyla of the fungal kingdom, the spores of which develop in asci or 33 basidia respectively. Together they form Dikarya, the higher fungal subkingdom. 34 Dimorphic – Fungal growth in two distinct forms, either yeast-like budding or filamentous growth. 35 Pseudohypha – Elongated yeast cells with a unipolar budding pattern that remain physically attached to 36 each other. They are associated with invasive growth on substrates. 37 Saprophyte – Fungi that use dead or decaying organic matter as a food source. 38 Phytopathogen – Pathogen of plants. 39 Chemotropism – Growth towards an exogenous chemical stimulus. 40 Heterothallic / Homothallic – Mating between different sexes (hetero) to promote outbreeding, or self- 41 fertile mating (homo) to promote inbreeding. 42 Kelch domain – Five to seven repeats of the amino acid kelch motif that form a β-propeller tertiary 43 structure involved in protein–protein interactions. 44 Germination – Hyphal emergence from fungal spores. 45 Conidia / Ascospore – Asexual and sexual reproductive spores. 46 Appressoria – Specialised infection structures produced by some pathogenic fungi that attach to and 47 invade plant hosts. Internal turgor pressure forces underlying penetration hyphae through physical 48 barriers, promoting invasion. 49 Titan cell – Polyploid Cryptococcus neoformans cells that are 5-10 times larger than normal diploid cells. 50 Titan cells are resistant to host immune macrophage phagocytosis and contribute to virulence. 51 Abstract 52 G-protein signalling pathways are involved in sensing the environment, enabling fungi to coordinate cell 53 function, metabolism and development with their surroundings, thereby promoting their survival, 54 propagation and virulence. G-protein coupled receptors (GPCRs) are the largest class of cell surface 55 receptors in fungi. Despite the apparent importance of GPCR signalling to fungal biology and virulence, 56 relatively few GPCR-G-protein interactions, and even fewer receptor-binding ligands, have been 57 identified. Approximately 40% of current pharmaceuticals target human GPCRs, due to their cell surface 58 location and central role in cell signalling. Fungal GPCRs do not belong to any of the mammalian 59 receptor classes, making them druggable targets for antifungal development. This review evaluates 60 developments in our understanding of fungal GPCR-mediated signalling, while substantiating the 2 61 rationale for considering these receptors as potential antifungal targets. The need for insights into the 62 structure-function relationship of receptor-ligand interactions is highlighted, which could facilitate the 63 development of receptor-interfering compounds that could be used in disease control. 64 The threat of fungal pathogens 65 Fungi are ubiquitous throughout nature, where they are fundamental to the decay of organic matter, 66 but some also form commensal and/or pathogenic associations with animal or plant hosts. Fungal 67 diseases of humans range from superficial to invasive life-threatening infections, which occur mostly in 68 humans with a weakened immune system 1. Over 100 million people suffer from serious mucosal fungal 69 diseases, resulting in 1.6 million deaths annually 2. Invasive diseases of humans are primarily caused by 70 infection by four fungal genera Aspergillus, Candida, Cryptococcus and Pneumocystis, which cause over 71 90% of fungal related deaths 1. Fungal diseases also cause extinctions in plants and animal species 72 including frogs, lizards, bats and trees, thereby threatening the stability of natural ecosystems 4. Food 73 security and human malnutrition are tightly linked to disease susceptibility, reduced quality of life and 74 premature death. Persistent low level fungal diseases of crops can cause significant yield reductions 3, 75 which in conjunction with fungal-like oomycetes destroy sufficient crops to feed 600 million people each 76 year 2,3. Cereals, particularly wheat, are the most important providers of human calories 4. Fungal 77 disease epidemics of major cereal crops, such as cereal head blight and rusts, rice and wheat blast, and 78 corn smut, are a serious and growing threat to global food security and in turn human health. Global 79 warming is exacerbating this threat by driving the poleward movement of fungal pathogens, promoting 80 the establishment of new diseases in previously unsuitable geographic regions 5. Fungal toxins 81 (mycotoxins) contaminate 25% of the world’s crops 6, causing food spoilage, while being detrimental to 82 human and animal health, and potentiating the impact of fungal diseases. Major mycotoxin-producing 83 fungal genera include Aspergillus, Fusarium and Penicillium. Acute mycotoxicoses in humans and 84 animals can cause death, while chronic exposure amounts to insidious disorders influencing growth rate, 85 fertility and immunosuppression 7. Monitoring and preventing mycotoxin contamination has a 86 significant and costly impact on food and feed supply chains. Hence, fungal diseases present a growing 87 risk to society through their direct and indirect effects on human, animal and plant health. 88 Human mortality rates for Aspergillosis, Candidiasis and Cryptococcosis range between 20-95% despite 89 their early diagnosis and treatment with the limited number of antifungal drugs available, while if 90 diagnosis is delayed or missed mortality, rates are near 100% 1. Antifungals are also relied upon to 91 protect our food crops from fungal diseases. Septoria tritici Blotch is the most problematic foliar disease 92 of wheat in the EU and annually accounts for 70% of antifungal usage, costing approximately €100 p/ha, 93 yet the disease still causes 5-10% yield losses and quickly evolves resistance to extant antifungal 94 compounds 8,9. The extensive use of antifungals in agriculture has contributed to the rise of multi-drug 95 resistant fungal populations in both the agricultural and clinical settings 10,11. Emerging threats such as 96 multi-drug resistant Candida auris and the Cryptococcus gattii outbreaks in Vancouver Island are a major 97 epidemiological human health concerns 12-14. Our over reliance on a limited number of antifungal drugs 3 98 cannot be neglected, and new approaches are required to protect human, animal, crop and ecosystem 99 health from the threat of fungal disease and mycotoxin contamination. 100 G-protein coupled receptors (GPCRs) are the largest class of cell surface receptors in eukaryotes, sensing 101 environmental
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