Abstract
Extracellular vesicles (EVs) have recently emerged as a key method of communication between cells. In this chapter, we examine the evidence for their role in inter-kingdom communication, in particular in the context of pathogenic fungi and their hosts. We detail what is known about modes of EV-driven communication, the consequences for host-pathogen interactions and the compositional and physical properties of the vesicles themselves. Looking forward, we point to the growing need for a detailed understanding of the heterogeneity of EV populations. This heterogeneity is likely to be key in understanding the diversity of responses to fungal infection in humans.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, Zancope-Oliveira RM, Almeida IC, Nosanchuk JD (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10(8):1695–1710
Bielska E, Sisquella MA, Aldeieg M, Birch C, O’Donoghue EJ, May RC (2018) Pathogen-derived extracellular vesicles mediate virulence in the fatal human pathogen Cryptococcus gattii. Nat Commun 9(1):1556. https://doi.org/10.1038/s41467-018-03991-6
Bleackley MR, Dawson CS, Anderson MA (2019) Fungal extracellular vesicles with a focus on proteomic analysis. Proteomics 19(8):1800232. https://doi.org/10.1002/pmic.201800232
Bleackley MR, Samuel M, Garcia-Ceron D, McKenna JA, Lowe RGT, Pathan M, Zhao K, Ang C-S, Mathivanan S, Anderson MA (2020) Extracellular vesicles from the cotton pathogen Fusarium oxysporum f. sp. vasinfectum induce a phytotoxic response in plants. Front Plant Sci 10:1610. https://www.frontiersin.org/article/10.3389/fpls.2019.01610
Budnik V, Ruiz-Cañada C, Wendler F (2016) Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci 17(3):160–172. https://doi.org/10.1038/nrn.2015.29
Camacho E, Vij R, Chrissian C, Prados-Rosales R, Gil D, O’Meally RN, Cordero RJB, Cole RN, McCaffery JM, Stark RE, Casadevall A (2019) The structural unit of melanin in the cell wall of the fungal pathogen Cryptococcus neoformans. J Biol Chem 294(27):10471–10489. https://doi.org/10.1074/jbc.RA119.008684
Chatterjee SN, Das J (1967) Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. Microbiology 49(1):1–11
Corbeil D, Santos MF, Karbanová J, Kurth T, Rappa G, Lorico A (2020) Uptake and fate of extracellular membrane vesicles: nucleoplasmic reticulum-associated late endosomes as a new gate to intercellular communication. Cell 9(9). https://doi.org/10.3390/cells9091931
de Paula RG, Antoniêto ACC, Nogueira KMV, Ribeiro LFC, Rocha MC, Malavazi I, Almeida F, Silva RN (2019) Extracellular vesicles carry cellulases in the industrial fungus Trichoderma reesei. Biotechnol Biofuels 12(1):146. https://doi.org/10.1186/s13068-019-1487-7
Han L, Lam EW-F, Sun Y (2019) Extracellular vesicles in the tumor microenvironment: old stories, but new tales. Mol Can 18(1):59. https://doi.org/10.1186/s12943-019-0980-8
Lavrin T, Konte T, Kostanjšek R, Sitar S, Sepčič K, Prpar Mihevc S, Žagar E, Župunski V, Lenassi M, Rogelj B, Gunde Cimerman N (2020) The neurotropic black yeast Exophiala dermatitidis induces neurocytotoxicity in neuroblastoma cells and progressive cell death. Cell 9(4). https://doi.org/10.3390/cells9040963
Leone F, Bellani L, Muccifora S, Giorgetti L, Bongioanni P, Simili M, Maserti B, Del Carratore R (2018) Analysis of extracellular vesicles produced in the biofilm by the dimorphic yeast Pichia fermentans. J Cell Physiol 233(4):2759–2767. https://doi.org/10.1002/jcp.25885
Nimrichter L, de Souza MM, Del Poeta M, Nosanchuk JD, Joffe L, Tavares P d M, Rodrigues ML (2016) Extracellular vesicle-associated transitory cell wall components and their impact on the interaction of fungi with host cells. Front Microbiol 7:1034. https://www.frontiersin.org/article/10.3389/fmicb.2016.01034
Oliveira DL, Freire-de-Lima CG, Nosanchuk JD, Casadevall A, Rodrigues ML, Nimrichter L (2010) Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 78(4):1601–1609. https://doi.org/10.1128/IAI.01171-09
Pan B-T, Johnstone RM (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33(3):967–978. https://doi.org/10.1016/0092-8674(83)90040-5
Panepinto J, Komperda K, Frases S, Park Y, Djordjevic JT, Casadevall A, Williamson PR (2009) Sec 6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 71(5):1165–1176
Peres da Silva R, Martins S d T, Rizzo J, Dos Reis FCG, Joffe LS, Vainstein M, Kmetzsch L, Oliveira DL, Puccia R, Goldenberg S (2018) Golgi reassembly and stacking protein (GRASP) participates in vesicle-mediated RNA export in Cryptococcus neoformans. Genes 9(8):400
Rai AK, Johnson PJ (2019) Trichomonas vaginalis extracellular vesicles are internalized by host cells using proteoglycans and caveolin-dependent endocytosis. Proc Natl Acad Sci 116(43):21354–21360. https://doi.org/10.1073/pnas.1912356116
Rodrigues ML, Nimrichter L, Oliveira DL, Frases S, Miranda K, Zaragoza O, Alvarez M, Nakouzi A, Feldmesser M, Casadevall A (2007) Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 6(1):48–59
Rodrigues ML, Nakayasu ES, Oliveira DL, Nimrichter L, Nosanchuk JD, Almeida IC, Casadevall A (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7(1):58–67
Simeone P, Bologna G, Lanuti P, Pierdomenico L, Guagnano MT, Pieragostino D, Del Boccio P, Vergara D, Marchisio M, Miscia S, Mariani-Costantini R (2020) Extracellular vesicles as signaling mediators and disease biomarkers across biological barriers. Int J Mol Sci 21(7):2514. https://doi.org/10.3390/ijms21072514
Souza JAM, de Matos Baltazar L, Carregal VM, Gouveia-Eufrasio L, de Oliveira AG, Dias WG, Campos Rocha M, Rocha de Miranda K, Malavazi I, de Assis Santos D, Frézard FJG, da Glória de Souza D, Teixeira MM, Soriani FM (2019) Characterization of Aspergillus fumigatus extracellular vesicles and their effects on macrophages and neutrophils functions. Front Microbiol 10:2008. https://www.frontiersin.org/article/10.3389/fmicb.2019.02008
Vallejo MC, Matsuo AL, Ganiko L, Medeiros LCS, Miranda K, Silva LS, Freymüller-Haapalainen E, Sinigaglia-Coimbra R, Almeida IC, Puccia R (2011) The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic α-Galactosyl epitopes. Eukaryot Cell 10(3):343–351
Van Niel G, D’Angelo G, Raposo G (2018) Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 19(4):213–228. https://doi.org/10.1038/nrm.2017.125
Vargas G, Rocha JDB, Oliveira DL, Albuquerque PC, Frases S, Santos SS, Nosanchuk JD, Gomes AMO, Medeiros LCAS, Miranda K, Sobreira TJP, Nakayasu ES, Arigi EA, Casadevall A, Guimaraes AJ, Rodrigues ML, Freire-de-Lima CG, Almeida IC, Nimrichter L (2015) Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell Microbiol 17(3):389–407. https://doi.org/10.1111/cmi.12374
Voelz K, Johnston SA, Smith LM, Hall RA, Idnurm A, May RC (2014) “Division of labour” in response to host oxidative burst drives a fatal Cryptococcus gattii outbreak. Nat Commun 5:5194. https://doi.org/10.1038/ncomms6194
Walker L, Sood P, Lenardon MD, Milne G, Olson J, Jensen G, Wolf J, Casadevall A, Adler-Moore J, Gow NAR (2018) The viscoelastic properties of the fungal cell wall allow traffic of ambisome as intact liposome vesicles. MBio 9(1). https://doi.org/10.1128/mBio.02383-17
Wang M, Weiberg A, Jin H (2015) Pathogen small RNAs: a new class of effectors for pathogen attacks. Mol Plant Pathol 16(3):219–223. https://doi.org/10.1111/mpp.12233
Yang B, Wang J, Jiang H, Lin H, Ou Z, Ullah A, Hua Y, Chen J, Lin X, Hu X, Zheng L, Wang Q (2021) Extracellular vesicles derived from talaromyces marneffei yeasts mediate inflammatory response in macrophage cells by bioactive protein components. Front Microbiol 11:3329. https://www.frontiersin.org/article/10.3389/fmicb.2020.603183
Zarnowski R, Sanchez H, Covelli AS, Dominguez E, Jaromin A, Bernhardt J, Mitchell KF, Heiss C, Azadi P, Mitchell A, Andes DR (2018) Candida albicans biofilm-induced vesicles confer drug resistance through matrix biogenesis. PLoS Biol 16(10):e2006872. https://doi.org/10.1371/journal.pbio.2006872
Zhao K, Bleackley M, Chisanga D, Gangoda L, Fonseka P, Liem M, Kalra H, Al Saffar H, Keerthikumar S, Ang C-S, Adda CG, Jiang L, Yap K, Poon IK, Lock P, Bulone V, Anderson M, Mathivanan S (2019) Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling. Commun Biol 2(1):305. https://doi.org/10.1038/s42003-019-0538-8
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Makarova, M., May, R.C. (2021). Fungal Extracellular Vesicles in Interkingdom Communication. In: Rodrigues, M., Janbon, G. (eds) Fungal Extracellular Vesicles. Current Topics in Microbiology and Immunology, vol 432. Springer, Cham. https://doi.org/10.1007/978-3-030-83391-6_8
Download citation
DOI: https://doi.org/10.1007/978-3-030-83391-6_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-83390-9
Online ISBN: 978-3-030-83391-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)