Abstract
Extracellular vesicles (EVs) are membranous structures surrounded by a lipid bilayer required for the export of fungal proteins, lipids, toxins, nucleic acids, pigments, and polysaccharides. Proteomic studies of the content of fungal EVs revealed the presence of molecules involved in cell metabolism, signal transduction, and virulence, among others. EVs are evolutionarily conserved in all three domains of life and play important roles in cell-cell communication. Recently, the bidirectional transport of EVs was characterized through the demonstration that EVs can be released and captured by fungal cells. In fungi, EVs participate in immunomodulation through the delivery of virulence factors, antigens and allergens, but further studies are necessary to investigate their potential roles as carriers of diagnostic biomarkers and in drug delivery or antifungal resistance transmission. In this review, we discuss the roles of fungal EVs and their cargo in cell-cell communication, host-pathogen interactions, and environmental perception. The functions of EVs as vehicles for transporting fungal proteins and virulence factors are also addressed, as well as their use as biomarkers for the diagnosis of diseases and possible participation in antifungal responses.
Keywords: Fungi, extracellular vesicle, protein export, lipids, toxins, pigments.
Graphical Abstract
[1]
Ofir-Birin, Y.; Heidenreich, M.; Regev-Rudzki, N. Pathogen derived extracellular vesicles coordinate social behaviour and host manipulation. Semin. Cell Dev. Biol., 2017, 67, 83-90.
[2]
Honigberg, S.M. Cell signals, cell contacts, and the organization of yeast communities. Eukaryot. Cell, 2011, 10(4), 466-473.
[3]
Bielska, E.; Sisquella, M.A.; Aldeieg, M.; Birch, C.; O’Donoghue, E.J.; May, R.C. Pathogen-derived extracellular vesicles mediate virulence in the fatal human pathogen Cryptococcus gattii. Nat. Commun., 2018, 9(1), 1556.
[4]
Joffe, L.S.; Nimrichter, L.; Rodrigues, M.L.; Del Poeta, M. Potential roles of fungal extracellular vesicles during infection. MSphere, 2016, 1(4), 1.
[5]
Regente, M.; Pinedo, M.; San Clemente, H.; Balliau, T.; Jamet, E.; de la Canal, L. Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. J. Exp. Bot., 2017, 68(20), 5485-5495.
[6]
Gill, S.; Catchpole, R.; Forterre, P. Extracellular membrane vesicles in the three domains of life and beyond. FEMS Microbiol. Rev., 2019, 43(3), 273-303.
[7]
Kabani, M.; Melki, R. Sup35p in its soluble and prion states is packaged inside extracellular vesicles. MBio, 2015, 6(4), 6.
[8]
Rodrigues, M.L.; Nimrichter, L.; Oliveira, D.L.; Frases, S.; Miranda, K.; Zaragoza, O.; Alvarez, M.; Nakouzi, A.; Feldmesser, M.; Casadevall, A. 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.
[9]
Brown, L.; Wolf, J.M.; Prados-Rosales, R.; Casadevall, A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol., 2015, 13(10), 620-630.
[10]
Yáñez-Mó, M.; Siljander, P.R-M.; Andreu, Z.; Zavec, A.B.; Borràs, F.E.; Buzas, E.I.; Buzas, K.; Casal, E.; Cappello, F.; Carvalho, J.; Colás, E.; Silva, A.C.; Fais, S.; Falcon-Perez, J.M.; Ghobrial, I.M.; Giebel, B.; Gimona, M.; Graner, M.; Gursel, I.; Gursel, M.; Heegaard, N.H.H.; Hendrix, A.; Kierulf, P.; Kokubun, K.; Kosanovic, M.; Kralj-Iglic, V.; Krämer-Albers, E-M.; Laitinen, S.; Lässer, C.; Lener, T.; Ligeti, E.; Linē, A.; Lipps, G.; Llorente, A.; Lötvall, J.; Manček-Keber, M.; Marcilla, A.; Mittelbrunn, M.; Nazarenko, I.; Hoen, E.N. Nolte, -’t; Nyman, T.A.; O’Driscoll, L.; Olivan, M.; Oliveira, C.; Pállinger, É.; del Portillo, H.A.; Reventós, J.; Rigau, M.; Rohde, E.; Sammar, M.; Sánchez-Madrid, F.; Santarém, N.; Schallmoser, K.; Ostenfeld, M.S.; Stoorvogel, W.; Stukelj, R.; Van der Grein, S.G.; Vasconcelos, M.H.; Wauben, M.H.M.; De Wever, O. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 2015, 4.
[11]
Schorey, J.S.; Cheng, Y.; Singh, P.P.; Smith, V.L. Exosomes and other extracellular vesicles in host-pathogen interactions. EMBO Rep., 2015, 16(1), 24-43.
[12]
Gil-Bona, A.; Amador-García, A.; Gil, C.; Monteoliva, L. The external face of Candida albicans: A proteomic view of the cell surface and the extracellular environment. J. Proteomics, 2018, 180, 70-79.
[13]
Maas, S.L.N.; Breakefield, X.O.; Weaver, A.M. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol., 2017, 27(3), 172-188.
[14]
Hoshino, A.; Costa-Silva, B.; Shen, T-L.; Rodrigues, G.; Hashimoto, A.; Tesic Mark, M.; Molina, H.; Kohsaka, S.; Di Giannatale, A.; Ceder, S.; Singh, S.; Williams, C.; Soplop, N.; Uryu, K.; Pharmer, L.; King, T.; Bojmar, L.; Davies, A.E.; Ararso, Y.; Zhang, T.; Zhang, H.; Hernandez, J.; Weiss, J.M.; Dumont-Cole, V.D.; Kramer, K.; Wexler, L.H.; Narendran, A.; Schwartz, G.K.; Healey, J.H.; Sandstrom, P.; Labori, K.J.; Kure, E.H.; Grandgenett, P.M.; Hollingsworth, M.A.; de Sousa, M.; Kaur, S.; Jain, M.; Mallya, K.; Batra, S.K.; Jarnagin, W.R.; Brady, M.S.; Fodstad, O.; Muller, V.; Pantel, K.; Minn, A.J.; Bissell, M.J.; Garcia, B.A.; Kang, Y.; Rajasekhar, V.K.; Ghajar, C.M.; Matei, I.; Peinado, H.; Bromberg, J.; Lyden, D. Tumour exosome integrins determine organotropic metastasis. Nature, 2015, 527(7578), 329-335.
[15]
Mulcahy, L.A.; Pink, R.C.; Carter, D.R.F. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles, 2014, 3, 3.
[16]
Albuquerque, P.C.; Nakayasu, E.S.; Rodrigues, M.L.; Frases, S.; Casadevall, A.; Zancope-Oliveira, R.M.; Almeida, I.C.; Nosanchuk, J.D. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell. Microbiol., 2008, 10(8), 1695-1710.
[17]
Zarnowski, R.; Sanchez, H.; Covelli, A.S.; Dominguez, E.; Jaromin, A.; Bernhardt, J.; Mitchell, K.F.; Heiss, C.; Azadi, P.; Mitchell, A.; Andes, D.R. Candida albicans biofilm-induced vesicles confer drug resistance through matrix biogenesis. PLoS Biol., 2018, 16(10)e2006872
[18]
Ikeda, M.A.K.; de Almeida, J.R.F.; Jannuzzi, G.P.; Cronemberger-Andrade, A.; Torrecilhas, A.C.T.; Moretti, N.S.; da Cunha, J.P.C.; de Almeida, S.R.; Ferreira, K.S. Extracellular vesicles from Sporothrix brasiliensis are an important virulence factor that induce an increase in fungal burden in experimental sporotrichosis. Front. Microbiol., 2018, 9, 2286.
[19]
da Silva, T.A.; Roque-Barreira, M.C.; Casadevall, A.; Almeida, F. Extracellular vesicles from Paracoccidioides brasiliensis induced M1 polarization in vitro. Sci. Rep., 2016, 6, 35867.
[20]
Johansson, H.J.; Vallhov, H.; Holm, T.; Gehrmann, U.; Andersson, A.; Johansson, C.; Blom, H.; Carroni, M.; Lehtiö, J.; Scheynius, A. Extracellular nanovesicles released from the commensal yeast Malassezia sympodialis are enriched in allergens and interact with cells in human skin. Sci. Rep., 2018, 8(1), 9182.
[21]
Silva, B.M.A.; Prados-Rosales, R.; Espadas-Moreno, J.; Wolf, J.M.; Luque-Garcia, J.L.; Gonçalves, T.; Casadevall, A. Characterization of Alternaria infectoria extracellular vesicles. Med. Mycol., 2014, 52(2), 202-210.
[22]
Leone, F.; Bellani, L.; Muccifora, S.; Giorgetti, L.; Bongioanni, P.; Simili, M.; Maserti, B.; Del Carratore, R. Analysis of extracellular vesicles produced in the biofilm by the dimorphic yeast Pichia fermentans. J. Cell. Physiol., 2018, 233(4), 2759-2767.
[23]
Nimrichter, L.; de Souza, M.M.; Del Poeta, M.; Nosanchuk, J.D.; Joffe, L.; Tavares, P. de M.; Rodrigues, M.L. Extracellular vesicle associated transitory cell wall components and their impact on the interaction of fungi with host cells. Front. Microbiol., 2016, 7, 1034.
[24]
Rodrigues, M.L.; Nakayasu, E.S.; Oliveira, D.L.; Nimrichter, L.; Nosanchuk, J.D.; Almeida, I.C.; Casadevall, A. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell, 2008, 7(1), 58-67.
[25]
Vargas, G.; Rocha, J.D.B.; Oliveira, D.L.; Albuquerque, P.C.; Frases, S.; Santos, S.S.; Nosanchuk, J.D.; Gomes, A.M.O.; Medeiros, L.C.A.S.; Miranda, K.; Sobreira, T.J.P.; Nakayasu, E.S.; Arigi, E.A.; Casadevall, A.; Guimaraes, A.J.; Rodrigues, M.L.; Freire-de-Lima, C.G.; Almeida, I.C.; Nimrichter, L. Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell. Microbiol., 2015, 17(3), 389-407.
[26]
Peres da Silva, R.; Puccia, R.; Rodrigues, M.L.; Oliveira, D.L.; Joffe, L.S.; César, G.V.; Nimrichter, L.; Goldenberg, S.; Alves, L.R. Extracellular vesicle-mediated export of fungal RNA. Sci. Rep., 2015, 5, 7763.
[27]
Eisenman, H.C.; Frases, S.; Nicola, A.M.; Rodrigues, M.L.; Casadevall, A. Vesicle-associated melanization in Cryptococcus neoformans. Microbiology, 2009, 155(Pt 12), 3860-3867.
[28]
Vallejo, M.C.; Nakayasu, E.S.; Matsuo, A.L.; Sobreira, T.J.P.; Longo, L.V.G.; Ganiko, L.; Almeida, I.C.; Puccia, R. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J. Proteome Res., 2012, 11(3), 1676-1685.
[29]
Panepinto, J.; Komperda, K.; Frases, S.; Park, Y-D.; Djordjevic, J.T.; Casadevall, A.; Williamson, P.R. Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol. Microbiol., 2009, 71(5), 1165-1176.
[30]
Zaragoza, O.; Rodrigues, M.L.; De Jesus, M.; Frases, S.; Dadachova, E.; Casadevall, A. The capsule of the fungal pathogen Cryptococcus neoformans. Adv. Appl. Microbiol., 2009, 68, 133-216.
[31]
Huang, S-H.; Wu, C-H.; Chang, Y.C.; Kwon-Chung, K.J.; Brown, R.J.; Jong, A. Cryptococcus neoformans-derived microvesicles enhance the pathogenesis of fungal brain infection. PLoS One, 2012, 7(11)e48570
[32]
Rizzo, J.; Albuquerque, P.C.; Wolf, J.M.; Nascimento, R.; Pereira, M.D.; Nosanchuk, J.D.; Rodrigues, M.L. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol., 2017, 121(6-7), 602-614.
[33]
Della Terra, P.P.; Rodrigues, A.M.; Fernandes, G.F.; Nishikaku, A.S.; Burger, E.; de Camargo, Z.P. Exploring virulence and immunogenicity in the emerging pathogen Sporothrix brasiliensis. PLoS Negl. Trop. Dis., 2017, 11(8)e0005903
[34]
Rayner, S.; Bruhn, S.; Vallhov, H.; Andersson, A.; Billmyre, R.B.; Scheynius, A. Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis. Sci. Rep., 2017, 7, 39742.
[35]
Alves, L.R.; Peres da Silva, R.; Sanchez, D.A.; Zamith-Miranda, D.; Rodrigues, M.L.; Goldenberg, S.; Puccia, R.; Nosanchuk, J.D. Extracellular vesicle-mediated RNA release in Histoplasma capsulatum. MSphere, 2019, 4(2), e00176-e19.
[36]
Peres da Silva, R.; Martins, S.T.; Rizzo, J.; Dos Reis, F.C.G.; Joffe, L.S.; Vainstein, M.; Kmetzsch, L.; Oliveira, D.L.; Puccia, R.; Goldenberg, S.; Rodrigues, M.L.; Alves, L.R. Golgi Reassembly and Stacking Protein (GRASP) participates in vesicle-mediated RNA export in Cryptococcus neoformans. Genes (Basel), 2018, 9(8), 9.
[37]
Wong, J.; Gao, L.; Yang, Y.; Zhai, J.; Arikit, S.; Yu, Y.; Duan, S.; Chan, V.; Xiong, Q.; Yan, J.; Li, S.; Liu, R.; Wang, Y.; Tang, G.; Meyers, B.C.; Chen, X.; Ma, W. Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J., 2014, 79(6), 928-940.
[38]
Zhou, J.; Fu, Y.; Xie, J.; Li, B.; Jiang, D.; Li, G.; Cheng, J. Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol. Genet. Genomics, 2012, 287(4), 275-282.
[39]
Lee, H-C.; Li, L.; Gu, W.; Xue, Z.; Crosthwaite, S.K.; Pertsemlidis, A.; Lewis, Z.A.; Freitag, M.; Selker, E.U.; Mello, C.C.; Liu, Y. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell, 2010, 38(6), 803-814.
[40]
Nunes, C.C.; Gowda, M.; Sailsbery, J.; Xue, M.; Chen, F.; Brown, D.E.; Oh, Y.; Mitchell, T.K.; Dean, R.A. Diverse and tissue enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genomics, 2011, 12, 288.
[41]
Cai, Q.; Qiao, L.; Wang, M.; He, B.; Lin, F-M.; Palmquist, J.; Huang, S-D.; Jin, H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science, 2018, 360(6393), 1126-1129.
[42]
Schaar, V.; Nordström, T.; Mörgelin, M.; Riesbeck, K. Moraxella catarrhalis outer membrane vesicles carry β-lactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin. Antimicrob. Agents Chemother., 2011, 55(8), 3845-3853.
[43]
Manning, A.J.; Kuehn, M.J. Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol., 2011, 11, 258.
[44]
Park, A.J.; Surette, M.D.; Khursigara, C.M. Antimicrobial targets localize to the extracellular vesicle-associated proteome of Pseudomonas aeruginosa grown in a biofilm. Front. Microbiol., 2014, 5, 464.
[45]
Medvedeva, E.S.; Baranova, N.B.; Mouzykantov, A.A.; Grigorieva, T.Y.; Davydova, M.N.; Trushin, M.V.; Chernova, O.A.; Chernov, V.M. Adaptation of mycoplasmas to antimicrobial agents: Acholeplasma laidlawii extracellular vesicles mediate the export of ciprofloxacin and a mutant gene related to the antibiotic target. Sci World J., 2014, 2014150615
[46]
Taff, H.T.; Mitchell, K.F.; Edward, J.A.; Andes, D.R. Mechanisms of Candida biofilm drug resistance. Future Microbiol., 2013, 8(10), 1325-1337.
[47]
Mukherjee, P.K.; Zhou, G.; Munyon, R.; Ghannoum, M.A. Candida biofilm: a well-designed protected environment. Med. Mycol., 2005, 43(3), 191-208.
[48]
Li, H.; Goh, B.N.; Teh, W.K.; Jiang, Z.; Goh, J.P.Z.; Goh, A.; Wu, G.; Hoon, S.S.; Raida, M.; Camattari, A.; Yang, L.; O’Donoghue, A.J.; Dawson, T.L. Jr Skin commensal Malassezia globosa secreted protease attenuates Staphylococcus aureus biofilm formation. J. Invest. Dermatol., 2018, 138(5), 1137-1145.
[49]
Zhang, Y-J.; Han, Y.; Sun, Y-Z.; Jiang, H-H.; Liu, M.; Qi, R-Q.; Gao, X-H. Extracellular vesicles derived from Malassezia furfur stimulate IL-6 production in keratinocytes as demonstrated in in vitro and in vivo models. J. Dermatol. Sci., 2019, 93(3), 168-175.
[50]
Bitencourt, T.A.; Rezende, C.P.; Quaresemin, N.R.; Moreno, P.; Hatanaka, O.; Rossi, A.; Martinez-Rossi, N.M.; Almeida, F. Extracellular vesicles from the dermatophyte Trichophyton interdigitale modulate macrophage and keratinocyte functions. Front. Immunol., 2018, 9, 2343.
[51]
Oliveira, D.L.; Nakayasu, E.S.; Joffe, L.S.; Guimarães, A.J.; Sobreira, T.J.P.; Nosanchuk, J.D.; Cordero, R.J.B.; Frases, S.; Casadevall, A.; Almeida, I.C.; Nimrichter, L.; Rodrigues, M.L. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One, 2010, 5(6)e11113
[52]
Matos Baltazar, L.; Nakayasu, E.S.; Sobreira, T.J.P.; Choi, H.; Casadevall, A.; Nimrichter, L.; Nosanchuk, J.D. Antibody binding alters the characteristics and contents of extracellular vesicles released by Histoplasma capsulatum. MSphere, 2016, 1(2), 1.
[53]
Reales-Calderón, J.A.; Vaz, C.; Monteoliva, L.; Molero, G.; Gil, C. Candida albicans modifies the protein composition and size distribution of THP-1 macrophage-derived extracellular vesicles. J. Proteome Res., 2017, 16(1), 87-105.
[54]
Rodrigues, M.L.; Nakayasu, E.S.; Almeida, I.C.; Nimrichter, L. The impact of proteomics on the understanding of functions and biogenesis of fungal extracellular vesicles. J. Proteomics, 2014, 97, 177-186.
[55]
Barbosa, M.S.; Báo, S.N.; Andreotti, P.F.; de Faria, F.P.; Felipe, M.S.S.; dos Santos Feitosa, L.; Mendes-Giannini, M.J.S.; Soares, C.M. Glyceraldehyde-3-phosphate dehydrogenase of Paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect. Immun., 2006, 74(1), 382-389.
[56]
Mendes-Giannini, M.J.S.; Andreotti, P.F.; Vincenzi, L.R.; da Silva, J.L.M.; Lenzi, H.L.; Benard, G.; Zancopé-Oliveira, R.; de Matos Guedes, H.L.; Soares, C.P. Binding of extracellular matrix proteins to Paracoccidioides brasiliensis. Microbes Infect., 2006, 8(6), 1550-1559.
[57]
Puccia, R.; Vallejo, M.C.; Longo, L.V.G. The cell wall-associated proteins in the dimorphic pathogenic species of Paracoccidioides. Curr. Protein Pept. Sci., 2017, 18(11), 1074-1089.
[58]
da Silva, J. de F.; de Oliveira, H.C.; Marcos, C.M.; da Silva, R.A.M.; da Costa, T.A.; Calich, V.L.G.; Almeida, A.M.F.; Mendes-Giannini, M.J.S. Paracoccidoides brasiliensis 30 kDa adhesin: identification as a 14-3-3 protein, cloning and subcellular localization in infection models. PLoS One, 2013, 8(4)e62533
[59]
Knutsen, A.P.; Bush, R.K.; Demain, J.G.; Denning, D.W.; Dixit, A.; Fairs, A.; Greenberger, P.A.; Kariuki, B.; Kita, H.; Kurup, V.P.; Moss, R.B.; Niven, R.M.; Pashley, C.H.; Slavin, R.G.; Vijay, H.M.; Wardlaw, A.J. Fungi and allergic lower respiratory tract diseases. J. Allergy Clin. Immunol., 2012, 129(2), 280-291.
[60]
Aragón-Miguel, R.; Calleja-Algarra, A.; Morales-Raya, C.; López-Medrano, F.; Pérez-Ayala, A.; Rodríguez-Peralto, J.L.; Ortiz-Romero, P.L.; Maroñas-Jiménez, L. Alternaria infectoria skin infection in a renal transplant recipient: an emerging phaeohyphomycosis of occidental countries? Int. J. Dermatol., 2017, 56(7), e153-e155.
[61]
Baltazar, L.M.; Zamith-Miranda, D.; Burnet, M.C.; Choi, H.; Nimrichter, L.; Nakayasu, E.S.; Nosanchuk, J.D. Concentration-dependent protein loading of extracellular vesicles released by Histoplasma capsulatum after antibody treatment and its modulatory action upon macrophages. Sci. Rep., 2018, 8(1), 8065.
[62]
Gil-Bona, A.; Llama-Palacios, A.; Parra, C.M.; Vivanco, F.; Nombela, C.; Monteoliva, L.; Gil, C. Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans. J. Proteome Res., 2015, 14(1), 142-153.
[63]
Winters, C.M.; Chiang, H-L. Yeast as a model system to study trafficking of small vesicles carrying signal-less proteins in and out of the cell. Curr. Protein Pept. Sci., 2016, 17(8), 808-820.
[64]
Paszkowski, U.; Kroken, S.; Roux, C.; Briggs, S.P. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA, 2002, 99(20), 13324-13329.
[65]
Javot, H.; Pumplin, N.; Harrison, M.J. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ., 2007, 30(3), 310-322.
[66]
Yang, S-Y.; Grønlund, M.; Jakobsen, I.; Grotemeyer, M.S.; Rentsch, D.; Miyao, A.; Hirochika, H.; Kumar, C.S.; Sundaresan, V.; Salamin, N.; Catausan, S.; Mattes, N.; Heuer, S.; Paszkowski, U. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell, 2012, 24(10), 4236-4251.
[67]
Choi, J.; Summers, W.; Paszkowski, U. Mechanisms underlying establishment of arbuscular mycorrhizal symbioses. Annu. Rev. Phytopathol., 2018, 56, 135-160.
[68]
Roth, R.; Hillmer, S.; Funaya, C.; Chiapello, M.; Schumacher, K.; Lo Presti, L.; Kahmann, R.; Paszkowski, U. Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nat. Plants, 2019, 5(2), 204-211.
[69]
Shi, R.; Wang, P-Y.; Li, X-Y.; Chen, J-X.; Li, Y.; Zhang, X-Z.; Zhang, C-G.; Jiang, T.; Li, W-B.; Ding, W.; Cheng, S-J. Exosomal levels of miRNA-21 from cerebrospinal fluids associated with poor prognosis and tumor recurrence of glioma patients. Oncotarget, 2015, 6(29), 26971-26981.
[70]
Liu, Q.; Yu, Z.; Yuan, S.; Xie, W.; Li, C.; Hu, Z.; Xiang, Y.; Wu, N.; Wu, L.; Bai, L.; Li, Y. Circulating exosomal microRNAs as prognostic biomarkers for non-small-cell lung cancer. Oncotarget, 2017, 8(8), 13048-13058.
[71]
Goto, T.; Fujiya, M.; Konishi, H.; Sasajima, J.; Fujibayashi, S.; Hayashi, A.; Utsumi, T.; Sato, H.; Iwama, T.; Ijiri, M.; Sakatani, A.; Tanaka, K.; Nomura, Y.; Ueno, N.; Kashima, S.; Moriichi, K.; Mizukami, Y.; Kohgo, Y.; Okumura, T. An elevated expression of serum exosomal microRNA-191, - 21, -451a of pancreatic neoplasm is considered to be efficient diagnostic marker. BMC Cancer, 2018, 18(1), 116.
[72]
Lee, H.; Park, H.; Noh, G.J.; Lee, E.S. pH-responsive hyaluronate-anchored extracellular vesicles to promote tumor-targeted drug delivery. Carbohydr. Polym., 2018, 202, 323-333.
[73]
Yousafzai, N.A.; Wang, H.; Wang, Z.; Zhu, Y.; Zhu, L.; Jin, H.; Wang, X. Exosome mediated multidrug resistance in cancer. Am. J. Cancer Res., 2018, 8(11), 2210-2226.
[74]
O’Neill, C.P.; Gilligan, K.E.; Dwyer, R.M. Role of extracellular vesicles (EVs) in cell stress response and resistance to cancer therapy. Cancers (Basel), 2019, 11(2), 11.
[75]
Wei, F.; Ma, C.; Zhou, T.; Dong, X.; Luo, Q.; Geng, L.; Ding, L.; Zhang, Y.; Zhang, L.; Li, N.; Li, Y.; Liu, Y. Exosomes derived from gemcitabine-resistant cells transfer malignant phenotypic traits via delivery of miRNA-222-3p. Mol. Cancer, 2017, 16(1), 132.
[76]
Santangelo, L.; Bordoni, V.; Montaldo, C.; Cimini, E.; Zingoni, A.; Battistelli, C.; D’Offizi, G.; Capobianchi, M.R.; Santoni, A.; Tripodi, M.; Agrati, C. Hepatitis C virus direct-acting antivirals therapy impacts on extracellular vesicles microRNAs content and on their immunomodulating properties. Liver Int., 2018, 38(10), 1741-1750.
[77]
Bhatnagar, S.; Shinagawa, K.; Castellino, F.J.; Schorey, J.S. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood, 2007, 110(9), 3234-3244.
[78]
Bhatnagar, S.; Schorey, J.S. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J. Biol. Chem., 2007, 282(35), 25779-25789.
[79]
Colino, J.; Snapper, C.M. Exosomes from bone marrow dendritic cells pulsed with diphtheria toxoid preferentially induce type 1 antigen-specific IgG responses in naive recipients in the absence of free antigen. J. Immunol., 2006, 177(6), 3757-3762.
[80]
Colino, J.; Snapper, C.M. Dendritic cell-derived exosomes express a Streptococcus pneumoniae capsular polysaccharide type 14 cross-reactive antigen that induces protective immunoglobulin responses against pneumococcal infection in mice. Infect. Immun., 2007, 75(1), 220-230.
[81]
Cheng, Y.; Schorey, J.S. Exosomes carrying mycobacterial antigens can protect mice against Mycobacterium tuberculosis infection. Eur. J. Immunol., 2013, 43(12), 3279-3290.
[82]
Gaillard, M.E.; Bottero, D.; Errea, A.; Ormazábal, M.; Zurita, M.E.; Moreno, G.; Rumbo, M.; Castuma, C.; Bartel, E.; Flores, D.; van der Ley, P.; van der Ark, A.; Hozbor, F. D. Acellular pertussis vaccine based on outer membrane vesicles capable of conferring both long-lasting immunity and protection against different strain genotypes. Vaccine, 2014, 32(8), 931-937.
[83]
Andrews, S.M.; Pollard, A.J. A vaccine against serogroup B Neisseria meningitidis: dealing with uncertainty. Lancet Infect. Dis., 2014, 14(5), 426-434.
[84]
Colombo, A.C.; Rella, A.; Normile, T.; Joffe, L.S.; Tavares, P.M. de S Araújo, G.R.; Frases, S.; Orner, E.P.; Farnoud, A.M.; Fries, B.C.; Sheridan, B.; Nimrichter, L.; Rodrigues, M.L.; Del Poeta, M. Cryptococcus neoformans glucuronoxylomannan and sterylglucoside are required for host protection in an animal vaccination model. MBio, 2019, 10(2), e02909-18.
[85]
van Dommelen, S.M.; Vader, P.; Lakhal, S.; Kooijmans, S.A.; van Solinge, W.W.; Wood, M.J.A.; Schiffelers, R.M. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J. Control. Release, 2012, 161(2), 635-644.
[86]
Lee, C-H. Im, E.J.; Moon, P.G.; Baek, M.C. Discovery of a diagnostic biomarker for colon cancer through proteomic profiling of small extracellular vesicles. BMC Cancer, 2018, 18(1), 1058.
[87]
Millard, M.; Yakavets, I.; Piffoux, M.; Brun, A.; Gazeau, F.; Guigner, J-M.; Jasniewski, J.; Lassalle, H-P.; Wilhelm, C.; Bezdetnaya, L. mTHPC-loaded extracellular vesicles outperform liposomal and free mTHPC formulations by an increased stability, drug delivery efficiency and cytotoxic effect in tridimensional model of tumors. Drug Deliv., 2018, 25(1), 1790-1801.
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