nach oben

Current Fungal Infection Reports

Erschienen in:

26.10.2017 | Fungal Genomics and Pathogenesis (Shmuel Shoham, Section Editor)

What Is New? Recent Knowledge on Fungal Extracellular Vesicles

verfasst von: Juliana Rizzo, Leonardo Nimrichter, Marcio L. Rodrigues

Erschienen in: Current Fungal Infection Reports | Ausgabe 4/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose of Review

Fungal extracellular vesicles (EVs) were first characterized a decade ago. Knowledge in this field expanded rapidly and although several questions remain unanswered, it is now clear that EVs play fundamental biological roles in fungi. In this manuscript, we update the reader with the most recent information on the participation of EVs in fungal physiology and pathogenesis.

Recent Findings

Fungal EVs were initially associated with the transport of macromolecules across the cell wall and extracellular delivery of virulence factors. However, recent findings indicate that they might also participate in prion transmission, response to nutrient availability, RNA export, morphological transition, and stimulation of different phagocytes.

Summary

The recent literature on fungal EVs reinforces the perception that these compartments are involved in intercellular communication and may represent interesting targets for antifungal development and tools for the generation of fungal vaccines.

Choi H, Lee DS. Illuminating the physiology of extracellular vesicles. Stem Cell Res Ther. 2016;7(1):55. https://doi.org/10.1186/s13287-016-0316-1. CrossRefPubMedPubMedCentral

Zamanian M, Fraser LM, Agbedanu PN, Harischandra H, Moorhead AR, Day TA, et al. Release of small RNA-containing exosome-like vesicles from the human filarial parasite Brugia malayi. PLoS Negl Trop Dis. 2015;9(9):e0004069. https://doi.org/10.1371/journal.pntd.0004069.CrossRefPubMedPubMedCentral

Silverman JM, Clos J, de'Oliveira CC, Shirvani O, Fang Y, Wang C, et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci. 2010;123(Pt 6):842–52. https://doi.org/10.1242/jcs.056465. CrossRefPubMed

Prados-Rosales R, Baena A, Martinez LR, Luque-Garcia J, Kalscheuer R, Veeraraghavan U, et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest. 2011;121(4):1471–83. https://doi.org/10.1172/JCI44261. CrossRefPubMedPubMedCentral

Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 2009;5(4):e1000382. https://doi.org/10.1371/journal.ppat.1000382.CrossRefPubMedPubMedCentral

Joffe LS, Nimrichter L, Rodrigues ML, Del Poeta M. Potential roles of fungal extracellular vesicles during infection. mSphere. 2016;1(4) https://doi.org/10.1128/mSphere.00099-16.

Rodrigues ML, Godinho RM, Zamith-Miranda D, Nimrichter L. Traveling into outer space: unanswered questions about fungal extracellular vesicles. PLoS Pathog. 2015;11(12):e1005240. https://doi.org/10.1371/journal.ppat.1005240.CrossRefPubMedPubMedCentral

Nimrichter L, de Souza MM, Del Poeta M, Nosanchuk JD, Joffe L, Tavares Pde M, et al. Extracellular vesicle-associated transitory cell wall components and their impact on the interaction of fungi with host cells. Front Microbiol. 2016;7:1034. https://doi.org/10.3389/fmicb.2016.01034.CrossRefPubMedPubMedCentral

Raab-Traub N, Dittmer DP. Viral effects on the content and function of extracellular vesicles. Nat Rev Microbiol. 2017; https://doi.org/10.1038/nrmicro.2017.60.

10.

Gopal SK, Greening DW, Rai A, Chen M, Xu R, Shafiq A, et al. Extracellular vesicles: their role in cancer biology and epithelial-mesenchymal transition. Biochem J. 2017;474(1):21–45. https://doi.org/10.1042/BCJ20160006. CrossRefPubMed

11.

Fuhrmann G, Neuer AL, Herrmann IK. Extracellular vesicles—a promising avenue for the detection and treatment of infectious diseases? Eur J Pharm Biopharm: Off J Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik eV. 2017;118:56–61. https://doi.org/10.1016/j.ejpb.2017.04.005.CrossRef

12.

Samuel M, Bleackley M, Anderson M, Mathivanan S. Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions. Front Plant Sci. 2015;6:766. https://doi.org/10.3389/fpls.2015.00766.CrossRefPubMedPubMedCentral

13.

Rodrigues ML, Nimrichter L, Oliveira DL, Frases S, Miranda K, Zaragoza O, et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell. 2007;6(1):48–59. https://doi.org/10.1128/EC.00318-06.CrossRefPubMed

14.

Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A. 2010;107(44):19002–7. https://doi.org/10.1073/pnas.1008843107. CrossRefPubMedPubMedCentral

15.

Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, Zancope-Oliveira RM, et al. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol. 2008;10(8):1695–710. https://doi.org/10.1111/j.1462-5822.2008.01160.x.CrossRefPubMedPubMedCentral

16.

Oliveira DL, Nakayasu ES, Joffe LS, Guimaraes AJ, Sobreira TJ, Nosanchuk JD, et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One. 2010;5(6):e11113. https://doi.org/10.1371/journal.pone.0011113.CrossRefPubMedPubMedCentral

17.

Gehrmann U, Qazi KR, Johansson C, Hultenby K, Karlsson M, Lundeberg L, et al. Nanovesicles from Malassezia sympodialis and host exosomes induce cytokine responses—novel mechanisms for host-microbe interactions in atopic eczema. PLoS One. 2011;6(7):e21480. https://doi.org/10.1371/journal.pone.0021480.CrossRefPubMedPubMedCentral

18.

Vallejo MC, Nakayasu ES, Longo LV, Ganiko L, Lopes FG, Matsuo AL, et al. Lipidomic analysis of extracellular vesicles from the pathogenic phase of Paracoccidioides brasiliensis. PLoS One. 2012;7(6):e39463. https://doi.org/10.1371/journal.pone.0039463.CrossRefPubMedPubMedCentral

19.

Vallejo MC, Nakayasu ES, Matsuo AL, Sobreira TJ, Longo LV, Ganiko L, et al. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteome Res. 2012;11(3):1676–85. https://doi.org/10.1021/pr200872s.CrossRefPubMedPubMedCentral

20.

Vallejo MC, Matsuo AL, Ganiko L, Medeiros LC, Miranda K, Silva LS, et al. The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic alpha-Galactosyl epitopes. Eukaryot Cell. 2011;10(3):343–51. https://doi.org/10.1128/EC.00227-10.CrossRefPubMedPubMedCentral

21.

Wolf JM, Espadas J, Luque-Garcia J, Reynolds T, Casadevall A. Lipid biosynthetic genes affect Candida albicans extracellular vesicle morphology, cargo, and immunostimulatory properties. Eukaryot Cell. 2015;14(8):745–54. https://doi.org/10.1128/EC.00054-15.CrossRefPubMedPubMedCentral

22.

Vargas G, Rocha JD, Oliveira DL, Albuquerque PC, Frases S, Santos SS, et al. Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell Microbiol. 2015;17(3):389–407. https://doi.org/10.1111/cmi.12374.CrossRefPubMed

23.

Gil-Bona A, Llama-Palacios A, Parra CM, Vivanco F, Nombela C, Monteoliva L, et al. Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans. J Proteome Res. 2015;14(1):142–53. https://doi.org/10.1021/pr5007944.CrossRefPubMed

24.

Silva BM, Prados-Rosales R, Espadas-Moreno J, Wolf JM, Luque-Garcia JL, Goncalves T, et al. Characterization of Alternaria infectoria extracellular vesicles. Med Mycol. 2014;52(2):202–10. https://doi.org/10.1093/mmy/myt003.CrossRefPubMed

25.

• Leone F, Bellani L, Mucciflora S, Giorgetti L, Bongioanni P, Simili M, et al. Analysis of extracellular vesicles produced in the biofilm by the dimorphic yeast Pichia fermentans. J Cell Physiol. 2017; https://doi.org/10.1002/jcp.25885. First association between fungal EVs, biofilms and morphological transition

26.

Rodrigues ML, Nakayasu ES, Almeida IC, Nimrichter L. The impact of proteomics on the understanding of functions and biogenesis of fungal extracellular vesicles. J Proteome. 2014;97:177–86. https://doi.org/10.1016/j.jprot.2013.04.001.CrossRef

27.

Brown L, Wolf JM, Prados-Rosales R, Casadevall A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol. 2015;13(10):620–30. https://doi.org/10.1038/nrmicro3480.CrossRefPubMedPubMedCentral

28.

Wolf JM, Casadevall A. Challenges posed by extracellular vesicles from eukaryotic microbes. Curr Opin Microbiol. 2014;22:73–8. https://doi.org/10.1016/j.mib.2014.09.012.CrossRefPubMedPubMedCentral

29.

Casadevall A, Nosanchuk JD, Williamson P, Rodrigues ML. Vesicular transport across the fungal cell wall. Trends Microbiol. 2009;17(4):158–62. https://doi.org/10.1016/j.tim.2008.12.005.CrossRefPubMedPubMedCentral

30.

Rodrigues ML, Oliveira DL, Vargas G, Girard-Dias W, Franzen AJ, Frases S, et al. Analysis of yeast extracellular vesicles. Methods Mol Biol. 2016;1459:175–90. https://doi.org/10.1007/978-1-4939-3804-9_12.CrossRefPubMed

31.

Gibson RK, Peberdy JF. Fine structure of protoplasts of Aspergillus nidulans. J Gen Microbiol. 1972;72(3):529–38. https://doi.org/10.1099/00221287-72-3-529.CrossRefPubMed

32.

Takeo K, Uesaka I, Uehira K, Nishiura M. Fine structure of Cryptococcus neoformans grown in vivo as observed by freeze-etching. J Bacteriol. 1973;113(3):1449–54.PubMedPubMedCentral

33.

Takeo K, Uesaka I, Uehira K, Nishiura M. Fine structure of Cryptococcus neoformans grown in vitro as observed by freeze-etching. J Bacteriol. 1973;113(3):1442–8.PubMedPubMedCentral

34.

Zha QB, Yao YF, Ren ZJ, Li XJ, Tang JH. Extracellular vesicles: an overview of biogenesis, function, and role in breast cancer. Tumour Biol: J Int Soc Oncodevelopmental Biol Med. 2017;39(2):1010428317691182. https://doi.org/10.1177/1010428317691182. CrossRef

35.

Anderson J, Mihalik R, Soll DR. Ultrastructure and antigenicity of the unique cell wall pimple of the Candida opaque phenotype. J Bacteriol. 1990;172(1):224–35.CrossRefPubMedPubMedCentral

36.

Osumi M. The ultrastructure of yeast: cell wall structure and formation. Micron. 1998;29(2–3):207–33.CrossRefPubMed

37.

Rodrigues ML, Travassos LR, Miranda KR, Franzen AJ, Rozental S, de Souza W, et al. Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infect Immun. 2000;68(12):7049–60.CrossRefPubMedPubMedCentral

38.

Cox RA, Best GK. Cell wall composition of two strains of Blastomyces dermatitidis exhibiting differences in virulence for mice. Infect Immun. 1972;5(4):449–53.PubMedPubMedCentral

39.

• Peres da Silva R, Heiss C, Black I, Azadi P, Gerlach JQ, Travassos LR, et al. Extracellular vesicles from Paracoccidioides pathogenic species transport polysaccharide and expose ligands for DC-SIGN receptors. Sci Rep. 2015;5:14213. https://doi.org/10.1038/srep14213. Description of biologically active glycans in P. brasiliensis EVs CrossRefPubMed

40.

Albuquerque PC, Cordero RJ, Fonseca FL, Peres da Silva R, Ramos CL, Miranda KR, et al. A Paracoccidioides brasiliensis glycan shares serologic and functional properties with cryptococcal glucuronoxylomannan. Fungal Genet Biol: FG & B. 2012;49(11):943–54. https://doi.org/10.1016/j.fgb.2012.09.002. CrossRef

41.

Liebman SW, Chernoff YO. Prions in yeast. Genetics. 2012;191(4):1041–72. https://doi.org/10.1534/genetics.111.137760.CrossRefPubMedPubMedCentral

42.

Wickner RB, Shewmaker FP, Bateman DA, Edskes HK, Gorkovskiy A, Dayani Y, et al. Yeast prions: structure, biology, and prion-handling systems. Microbiology and molecular biology reviews : MMBR. 2015;79(1):1–17. https://doi.org/10.1128/MMBR.00041-14. CrossRefPubMedPubMedCentral

43.

Liu S, Hossinger A, Gobbels S, Vorberg IM. Prions on the run: how extracellular vesicles serve as delivery vehicles for self-templating protein aggregates. Prion. 2017;11(2):98–112. https://doi.org/10.1080/19336896.2017.1306162.CrossRefPubMedPubMedCentral

44.

•• Liu S, Hossinger A, Hofmann JP, Denner P, Vorberg IM. Horizontal transmission of cytosolic Sup35 prions by extracellular vesicles. MBio. 2016;7(4) https://doi.org/10.1128/mBio.00915-16. Demonstration that biologically active prions are exported in fungal EVs

45.

•• Kabani M, Melki R. Sup35p in its soluble and prion states is packaged inside extracellular vesicles. MBio. 2015;6(4) https://doi.org/10.1128/mBio.01017-15. First association between fungal prions and EVs

46.

Thompson AG, Gray E, Heman-Ackah SM, Mager I, Talbot K, Andaloussi SE, et al. Extracellular vesicles in neurodegenerative disease–pathogenesis to biomarkers. Nat Rev Neurol. 2016;12(6):346–57. https://doi.org/10.1038/nrneurol.2016.68.CrossRefPubMed

47.

Kabani M, Melki R. More than just trash bins? Potential roles for extracellular vesicles in the vertical and horizontal transmission of yeast prions. Curr Genet. 2016;62(2):265–70. https://doi.org/10.1007/s00294-015-0534-6.CrossRefPubMed

48.

•• Peres da Silva R, Puccia R, Rodrigues ML, Oliveira DL, Joffe LS, Cesar GV, et al. Extracellular vesicle-mediated export of fungal RNA. Sci Rep. 2015;5:7763. https://doi.org/10.1038/srep07763. First demonstration of RNA export in fungal EVs CrossRefPubMedPubMedCentral

49.

Yonezawa H, Osaki T, Kurata S, Fukuda M, Kawakami H, Ochiai K, et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 2009;9:197. https://doi.org/10.1186/1471-2180-9-197.CrossRefPubMedPubMedCentral

50.

Manning AJ, Kuehn MJ. Functional advantages conferred by extracellular prokaryotic membrane vesicles. J Mol Microbiol Biotechnol. 2013;23(1–2):131–41. https://doi.org/10.1159/000346548.CrossRefPubMedPubMedCentral

51.

Rayner S, Bruhn S, Vallhov H, Andersson A, Billmyre RB, Scheynius A. Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis. Sci Rep. 2017;7:39742. https://doi.org/10.1038/srep39742.CrossRefPubMedPubMedCentral

52.

Rodrigues ML, Nakayasu ES, Oliveira DL, Nimrichter L, Nosanchuk JD, Almeida IC, et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell. 2008;7(1):58–67. https://doi.org/10.1128/EC.00370-07.CrossRefPubMed

53.

•• Matos Baltazar L, Nakayasu ES, Sobreira TJ, Choi H, Casadevall A, Nimrichter L, et al. Antibody binding alters the characteristics and contents of extracellular vesicles released by Histoplasma capsulatum. mSphere. 2016;1(2) https://doi.org/10.1128/mSphere.00085-15. Proof of concept that humoral responses can affect the composition of fungal EVs

54.

Giardina BJ, Stein K, Chiang HL. The endocytosis gene END3 is essential for the glucose-induced rapid decline of small vesicles in the extracellular fraction in Saccharomyces cerevisiae. J Extracellular Vesicles. 2014;3 https://doi.org/10.3402/jev.v3.23497.

55.

Rodrigues ML, Franzen AJ, Nimrichter L, Miranda K. Vesicular mechanisms of traffic of fungal molecules to the extracellular space. Curr Opin Microbiol. 2013;16(4):414–20. https://doi.org/10.1016/j.mib.2013.04.002.CrossRefPubMed

56.

Giardina BJ, Chiang HL. The key gluconeogenic enzyme fructose-1,6-bisphosphatase is secreted during prolonged glucose starvation and is internalized following glucose re-feeding via the non-classical secretory and internalizing pathways in Saccharomyces cerevisiae. Plant Signal Behav. 2013;8(8) https://doi.org/10.4161/psb.24936.

57.

Alibhoy AA, Giardina BJ, Dunton DD, Chiang HL. Vps34p is required for the decline of extracellular fructose-1,6-bisphosphatase in the vacuole import and degradation pathway. J Biol Chem. 2012;287(39):33080–93. https://doi.org/10.1074/jbc.M112.360412. CrossRefPubMedPubMedCentral

58.

Stein K, Chiang HL. Exocytosis and endocytosis of small vesicles across the plasma membrane in Saccharomyces cerevisiae. Membranes. 2014;4(3):608–29. https://doi.org/10.3390/membranes4030608.CrossRefPubMedPubMedCentral

59.

Giardina BJ, Stanley BA, Chiang HL. Glucose induces rapid changes in the secretome of Saccharomyces cerevisiae. Proteome Sci. 2014;12(1):9. https://doi.org/10.1186/1477-5956-12-9.CrossRefPubMedPubMedCentral

60.

Stein K, Winters C, Chiang HL. Vps15p regulates the distribution of cup-shaped organelles containing the major eisosome protein Pil1p to the extracellular fraction required for endocytosis of extracellular vesicles carrying metabolic enzymes. Biol Cell. 2017;109(5):190–209. https://doi.org/10.1111/boc.201600060.CrossRefPubMed

61.

Oliveira DL, Freire-de-Lima CG, Nosanchuk JD, Casadevall A, Rodrigues ML, Nimrichter L. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun. 2010;78(4):1601–9. https://doi.org/10.1128/IAI.01171-09.CrossRefPubMedPubMedCentral

62.

Huang SH, CH W, Chang YC, Kwon-Chung KJ, Brown RJ, Jong A. Cryptococcus neoformans-derived microvesicles enhance the pathogenesis of fungal brain infection. PLoS One. 2012;7(11):e48570. https://doi.org/10.1371/journal.pone.0048570.CrossRefPubMedPubMedCentral

63.

da Silva TA, Roque-Barreira MC, Casadevall A, Almeida F. Extracellular vesicles from Paracoccidioides brasiliensis induced M1 polarization in vitro. Sci Rep. 2016;6:35867. https://doi.org/10.1038/srep35867.CrossRefPubMedPubMedCentral

64.

• Rizzo J, Albuquerque PC, Wolf JM, Nascimento R, Pereira MD, Nosanchuk JD, et al. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol. 2017;121(6–7):602–14. https://doi.org/10.1016/j.funbio.2017.04.002. First association between fungal EVs and antimicrobial activity of environmental predators CrossRefPubMed

Titel: What Is New? Recent Knowledge on Fungal Extracellular Vesicles
verfasst von: Juliana Rizzo
Leonardo Nimrichter
Marcio L. Rodrigues
Publikationsdatum: 26.10.2017
Verlag: Springer US
Erschienen in: Current Fungal Infection Reports / Ausgabe 4/2017
Print ISSN: 1936-3761
Elektronische ISSN: 1936-377X
DOI: https://doi.org/10.1007/s12281-017-0293-6

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

Reizdarmsyndrom: Diäten wirksamer als Medikamente

29.04.2024 Reizdarmsyndrom Nachrichten

Bei Reizdarmsyndrom scheinen Diäten, wie etwa die FODMAP-arme oder die kohlenhydratreduzierte Ernährung, effektiver als eine medikamentöse Therapie zu sein. Das hat eine Studie aus Schweden ergeben, die die drei Therapieoptionen im direkten Vergleich analysierte.

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Bei schweren Reaktionen auf Insektenstiche empfiehlt sich eine spezifische Immuntherapie

25.04.2024 Allergien und Intoleranzreaktionen Nachrichten

Insektenstiche sind bei Erwachsenen die häufigsten Auslöser einer Anaphylaxie. Einen wirksamen Schutz vor schweren anaphylaktischen Reaktionen bietet die allergenspezifische Immuntherapie. Jedoch kommt sie noch viel zu selten zum Einsatz.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Purpose of Review

Recent Findings

Summary

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2017

Onychomycoses in a Military Population in Brazil

Candida haemulonii sensu lato: Update of the Determination of Susceptibility Profile in Argentina and Literature Review

The Management of Chronic Pulmonary Aspergillosis: The UK National Aspergillosis Centre Approach

Cryptococcus neoformans Epidemiological Cutoff Values

Clinical Implications of Candida Biofilms