Extracellular vesicles from Paracoccidioides pathogenic species transport polysaccharide and expose ligands for DC-SIGN receptors

da Silva, Roberta Peres; Heiss, Christian; Black, Ian; Azadi, Parastoo; Gerlach, Jared Q.; Travassos, Luiz R.; Joshi, Lokesh; Kilcoyne, Michelle; Puccia, Rosana

doi:10.1038/srep14213

Title: Extracellular vesicles from Paracoccidioides pathogenic species transport polysaccharide and expose ligands for DC-SIGN receptors

Journal Article · 20 September 2015 · Scientific Reports

DOI: https://doi.org/10.1038/srep14213 · OSTI ID:1324971

da Silva, Roberta Peres ^[1]; Heiss, Christian ^[2]; Black, Ian ^[2]; Azadi, Parastoo ^[2]; Gerlach, Jared Q. ^[3]; Travassos, Luiz R. ^[4]; Joshi, Lokesh ^[3]; Kilcoyne, Michelle ^[5]; Puccia, Rosana ^[4]

Escola Paulista de Medicina-Univ. Federal de Sao Paulo, Sao Paulo (Brazil); University of Georgia
Univ. of Georgia, Athens, GA (United States)
National Centre for Biomedical Engineering Science, NUI Galway (Ireland)
Escola Paulista de Medicina-Univ. Federal de Sao Paulo, Sao Paulo (Brazil)
National Centre for Biomedical Engineering Science, NUI Galway (Ireland); National Univ. of Ireland, Galway (Ireland)

Extracellular vesicles (EVs) mediate non-conventional transport of molecules across the fungal cell wall. We aimed at describing the carbohydrate composition and surface carbohydrate epitopes of EVs isolated from the pathogenic fungi Paracoccidioides brasiliensis and P. lutzii using standard procedures. Total EV carbohydrates were ethanol-precipitated from preparations depleted of lipids and proteins, then analyzed by chemical degradation, gas chromatography-mass spectrometry, nuclear magnetic resonance and size-exclusion chromatography. EV glycosyl residues of Glc, Man, and Gal comprised most probably two major components: a high molecular mass 4,6-α-glucan and a galactofuranosylmannan, possibly an oligomer, bearing a 2-α-Manp main chain linked to β-Galf (1,3) and α-Manp (1,6) end units. The results also suggested the presence of small amounts of a (1→6)- Manp polymer, (1→3)-glucan and (1→6)-glucan. Glycan microarrays allowed identification of EV surface lectin(s), while plant lectin microarray profiling revealed terminal Man and GlcNAc residues exposed at the EVs surface. Mammalian lectin microarray profiling showed that DC-SIGN receptors recognized surface carbohydrate in Paracoccidioides EVs. Our results suggest that oligosaccharides, cytoplasmic storage, and cell wall polysaccharides can be exported in fungal EVs, which also expose surface PAMPs and lectins. As a result, the role of these newly identified components in the interaction with the host remains to be unraveled.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Georgia, Athens, GA (United States). Analytical Services & Training Lab. Complex Carbohydrate Research Center

Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-93ER20097

OSTI ID:: 1324971

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Vol. 5; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (98)

A simple and rapid method for the permethylation of carbohydrates Ciucanu, Ionel; Kerek, Francisc Carbohydrate Research, Vol. 131, Issue 2, p. 209-217 https://doi.org/10.1016/0008-6215(84)85242-8	journal	August 1984
Cell-wall glucans of Cryptococcus neoformans CAP 67 James, Paul G.; Cherniak, Robert; Jones, Ronald G. Carbohydrate Research, Vol. 198, Issue 1 https://doi.org/10.1016/0008-6215(90)84273-w	journal	April 1990
A Paracoccidioides brasiliensis glycan shares serologic and functional properties with cryptococcal glucuronoxylomannan Albuquerque, Priscila C.; Cordero, Radames J. B.; Fonseca, Fernanda L. Fungal Genetics and Biology, Vol. 49, Issue 11 https://doi.org/10.1016/j.fgb.2012.09.002	journal	November 2012
The impact of proteomics on the understanding of functions and biogenesis of fungal extracellular vesicles Rodrigues, Marcio L.; Nakayasu, Ernesto S.; Almeida, Igor C. Journal of Proteomics, Vol. 97 https://doi.org/10.1016/j.jprot.2013.04.001	journal	January 2014
Vesicular mechanisms of traffic of fungal molecules to the extracellular space Rodrigues, Marcio L.; Franzen, Anderson J.; Nimrichter, Leonardo Current Opinion in Microbiology, Vol. 16, Issue 4 https://doi.org/10.1016/j.mib.2013.04.002	journal	August 2013
Paracoccin, a GlcNAc-binding lectin from Paracoccidioides brasiliensis, binds to laminin and induces TNF-α production by macrophages Coltri, Kely C.; Casabona-Fortunato, Analia S.; Gennari-Cardoso, Margareth L. Microbes and Infection, Vol. 8, Issue 3 https://doi.org/10.1016/j.micinf.2005.09.008	journal	March 2006
Paracoccin, an N-acetyl-glucosamine-binding lectin of Paracoccidioides brasiliensis, is involved in fungal growth Ganiko, L.; Puccia, R.; Mariano, V. Microbes and Infection, Vol. 9, Issue 6 https://doi.org/10.1016/j.micinf.2007.02.012	journal	May 2007
Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus Teixeira, Marcus M.; Theodoro, Raquel C.; de Carvalho, Maria J. A. Molecular Phylogenetics and Evolution, Vol. 52, Issue 2 https://doi.org/10.1016/j.ympev.2009.04.005	journal	August 2009
Definition of the Extracellular Proteome of Pathogenic-Phase Histoplasma capsulatum Holbrook, Eric D.; Edwards, Jessica A.; Youseff, Brian H. Journal of Proteome Research, Vol. 10, Issue 4 https://doi.org/10.1021/pr1011697	journal	April 2011
Immunity to fungal infections Romani, Luigina Nature Reviews Immunology, Vol. 11, Issue 4 https://doi.org/10.1038/nri2939	journal	March 2011
Extracellular vesicle-mediated export of fungal RNA Peres da Silva, Roberta; Puccia, Rosana; Rodrigues, Marcio L. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep07763	journal	January 2015
Microarray evaluation of the effects of lectin and glycoprotein orientation and data filtering on glycoform discrimination Gerlach, Jared Q.; Kilcoyne, Michelle; Joshi, Lokesh Anal. Methods, Vol. 6, Issue 2 https://doi.org/10.1039/c3ay40936h	journal	January 2014
The composition of the cell wall of Fusicoccum amygdali Buck, K. W.; Obaidah, M. A. Biochemical Journal, Vol. 125, Issue 2 https://doi.org/10.1042/bj1250461	journal	November 1971
Histoplasma capsulatum -(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor Rappleye, C. A.; Eissenberg, L. G.; Goldman, W. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 4 https://doi.org/10.1073/pnas.0609848104	journal	January 2007
A Single UDP-galactofuranose Transporter Is Required for Galactofuranosylation in Aspergillus fumigatus Engel, Jakob; Schmalhorst, Philipp S.; Dörk-Bousset, Thilo Journal of Biological Chemistry, Vol. 284, Issue 49 https://doi.org/10.1074/jbc.m109.070219	journal	October 2009
Experimental murine paracoccidiodomycosis induced by the inhalation of conidia McEwen, Juan G.; Bedoya, Victor; Patiño, Maria M. Medical Mycology, Vol. 25, Issue 3 https://doi.org/10.1080/02681218780000231	journal	January 1987
Galactofuranose containing molecules in Aspergillus fumigatus Latge, Jean-Paul Medical Mycology, Vol. 47, Issue s1 https://doi.org/10.1080/13693780802258832	journal	January 2009
Cell wall glucan synthases and GTPases in Paracoccidioides brasiliensis Sorais, Francoise; Barreto, Laura; Leal, Juan Antonio Medical Mycology https://doi.org/10.1080/13693780802713356	journal	January 2009
The habitat of Paracoccidioides brasiliensis : how far from solving the riddle? Restrepo, A.; McEwen, J. G.; Castañeda, E. Medical Mycology, Vol. 39, Issue 3 https://doi.org/10.1080/mmy.39.3.233.241	journal	January 2001
Compositional and immunobiological analyses of extracellular vesicles released by C andida albicans : Extracellular vesicles from Vargas, Gabriele; Rocha, Juliana D. B.; Oliveira, Debora Leite Cellular Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/cmi.12374	journal	November 2014
NMR evidence for oligosaccharide release from the dendritic-cell specific intercellular adhesion molecule 3-grabbing non-integrin-related (CLEC4M) carbohydrate recognition domain at low pH Probert, Fay; Mitchell, Daniel A.; Dixon, Ann M. FEBS Journal, Vol. 281, Issue 16 https://doi.org/10.1111/febs.12899	journal	July 2014
Vesicular transport in Histoplasma capsulatum : an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes Albuquerque, Priscila Costa; Nakayasu, Ernesto S.; Rodrigues, Marcio L. Cellular Microbiology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1462-5822.2008.01160.x	journal	August 2008
Immunochemical analysis of the H and M glycoproteins from Histoplasma capsulatum. Zancopé-Oliveira, R. M.; Bragg, S. L.; Reiss, E. Clinical and diagnostic laboratory immunology, Vol. 1, Issue 5 https://doi.org/10.1128/cdli.1.5.563-568.1994	journal	January 1994
The Pathogenic Fungus Paracoccidioides brasiliensis Exports Extracellular Vesicles Containing Highly Immunogenic α-Galactosyl Epitopes Vallejo, Milene C.; Matsuo, Alisson L.; Ganiko, Luciane Eukaryotic Cell, Vol. 10, Issue 3 https://doi.org/10.1128/ec.00227-10	journal	January 2011
Vesicular Polysaccharide Export in Cryptococcus neoformans Is a Eukaryotic Solution to the Problem of Fungal Trans-Cell Wall Transport Rodrigues, Marcio L.; Nimrichter, Leonardo; Oliveira, Débora L. Eukaryotic Cell, Vol. 6, Issue 1 https://doi.org/10.1128/ec.00318-06	journal	November 2006
Distribution and conformation of crystalline nigeran in hyphal walls of Aspergillus niger and Aspergillus awamori. Bobbitt, T. F.; Nordin, J. H.; Roux, M. Journal of Bacteriology, Vol. 132, Issue 2 https://doi.org/10.1128/jb.132.2.691-703.1977	journal	January 1977
Characterization of the carbohydrate component of fraction I in the Neurospora crassa cell wall. Cardemil, L.; Pincheira, G. Journal of Bacteriology, Vol. 137, Issue 3 https://doi.org/10.1128/jb.137.3.1067-1072.1979	journal	January 1979
Microsatellite Analysis of Three Phylogenetic Species of Paracoccidioides brasiliensis Matute, D. R.; Sepulveda, V. E.; Quesada, L. M. Journal of Clinical Microbiology, Vol. 44, Issue 6 https://doi.org/10.1128/jcm.02540-05	journal	June 2006
Cell Wall Assembly in Saccharomyces cerevisiae Lesage, G.; Bussey, H. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/mmbr.00038-05	journal	June 2006
Diversity in unconventional protein secretion Rabouille, Catherine; Malhotra, Vivek; Nickel, Walter Journal of Cell Science, Vol. 125, Issue 22 https://doi.org/10.1242/jcs.103630	journal	November 2012
Recombinant Paracoccin Reproduces the Biological Properties of the Native Protein and Induces Protective Th1 Immunity against Paracoccidioides brasiliensis Infection Alegre, Ana Claudia Paiva; Oliveira, Aline Ferreira; Dos Reis Almeida, Fausto Bruno PLoS Neglected Tropical Diseases, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pntd.0002788	journal	April 2014
Influence of N-Glycosylation on the Morphogenesis and Growth of Paracoccidioides brasiliensis and on the Biological Activities of Yeast Proteins Dos Reis Almeida, Fausto Bruno; Carvalho, Fernanda Caroline; Mariano, Vânia Sammartino PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0029216	journal	December 2011
Surface Glycosylation Profiles of Urine Extracellular Vesicles Gerlach, Jared Q.; Krüger, Anja; Gallogly, Susan PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074801	journal	September 2013
Expression of Paracoccidioides brasiliensis AMY1 in a Histoplasma capsulatum amy1 Mutant, Relates an α-(1,4)-Amylase to Cell Wall α-(1,3)-Glucan Synthesis E., Sepulveda, Victoria; E., Goldman, William; Emma, Camacho, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/nawd-p054	text	January 2012
Vesicular transport systems in fungi Rodrigues, Marcio L.; Nosanchuk, Joshua D.; Schrank, Augusto Future Microbiology, Vol. 6, Issue 11 https://doi.org/10.2217/fmb.11.112	journal	November 2011
Paracoccidioides lutziisp. nov.: biological and clinical implications Teixeira, Marcus De Melo; Theodoro, Raquel Cordeiro; Oliveira, Fabiana Freire Mendes De Medical Mycology https://doi.org/10.3109/13693786.2013.794311	journal	June 2013
Sweeten PAMPs: role of sugar complexed PAMPs in innate immunity and vaccine biology Mahla, Ranjeet Singh Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00248	journal	January 2013
Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes Crescitelli, Rossella; Lässer, Cecilia; Szabó, Tamas G. Journal of Extracellular Vesicles, Vol. 2, Issue 1 https://doi.org/10.3402/jev.v2i0.20677	journal	January 2013
α ‐(1,4)‐Amylase, but not α ‐ and β ‐(1,3)‐glucanases, may be responsible for the impaired growth and morphogenesis of Paracoccidioides brasiliensis induced by N ‐glycosylation inhibition Dos Reis Almeida, Fausto Bruno; Pigosso, Laurine Lacerda; Damásio, André Ricardo Yeast, Vol. 31, Issue 1 https://doi.org/10.1002/yea.2983	journal	November 2013
Glycogen?a covalently linked component of the cell wall inSaccharomyces cerevisiae Arvindekar, Akalpita U.; Patil, Narayan B. Yeast, Vol. 19, Issue 2 https://doi.org/10.1002/yea.802	journal	January 2002
Non-carbohydrate-Mediated Interaction of Lectins with Plant Proteins Gerlach, Jared Q.; Kilcoyne, Michelle; Eaton, Seron Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-1-4419-7877-6_12	book	January 2011
A simple and rapid method for the permethylation of carbohydrates Ciucanu, Ionel; Kerek, Francisc Carbohydrate Research, Vol. 131, Issue 2, p. 209-217 https://doi.org/10.1016/0008-6215(84)85242-8	journal	August 1984
Cell-wall glucans of Cryptococcus neoformans CAP 67 James, Paul G.; Cherniak, Robert; Jones, Ronald G. Carbohydrate Research, Vol. 198, Issue 1 https://doi.org/10.1016/0008-6215(90)84273-W	journal	April 1990
[1] Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry Merkle, Roberta K.; Poppe, Izabella Methods in Enzymology https://doi.org/10.1016/0076-6879(94)30003-8	book	January 1994
DC-SIGN, a Dendritic Cell–Specific HIV-1-Binding Protein that Enhances trans-Infection of T Cells Geijtenbeek, Teunis B. H.; Kwon, Douglas S.; Torensma, Ruurd Cell, Vol. 100, Issue 5 https://doi.org/10.1016/S0092-8674(00)80694-7	journal	March 2000
Targeting C-type lectin receptors with multivalent carbohydrate ligands Lepenies, Bernd; Lee, Junghoon; Sonkaria, Sanjiv Advanced Drug Delivery Reviews, Vol. 65, Issue 9 https://doi.org/10.1016/j.addr.2013.05.007	journal	August 2013
A Paracoccidioides brasiliensis glycan shares serologic and functional properties with cryptococcal glucuronoxylomannan Albuquerque, Priscila C.; Cordero, Radames J. B.; Fonseca, Fernanda L. Fungal Genetics and Biology, Vol. 49, Issue 11 https://doi.org/10.1016/j.fgb.2012.09.002	journal	November 2012
The impact of proteomics on the understanding of functions and biogenesis of fungal extracellular vesicles Rodrigues, Marcio L.; Nakayasu, Ernesto S.; Almeida, Igor C. Journal of Proteomics, Vol. 97 https://doi.org/10.1016/j.jprot.2013.04.001	journal	January 2014
Vesicular mechanisms of traffic of fungal molecules to the extracellular space Rodrigues, Marcio L.; Franzen, Anderson J.; Nimrichter, Leonardo Current Opinion in Microbiology, Vol. 16, Issue 4 https://doi.org/10.1016/j.mib.2013.04.002	journal	August 2013
Virulence of Paracoccidioides brasiliensis and gp43 expression in isolates bearing known PbGP43 genotype Carvalho, Kátia C.; Ganiko, Luciane; Batista, Wagner L. Microbes and Infection, Vol. 7, Issue 1 https://doi.org/10.1016/j.micinf.2004.09.008	journal	January 2005
Paracoccin, a GlcNAc-binding lectin from Paracoccidioides brasiliensis, binds to laminin and induces TNF-α production by macrophages Coltri, Kely C.; Casabona-Fortunato, Analia S.; Gennari-Cardoso, Margareth L. Microbes and Infection, Vol. 8, Issue 3 https://doi.org/10.1016/j.micinf.2005.09.008	journal	March 2006
Paracoccin, an N-acetyl-glucosamine-binding lectin of Paracoccidioides brasiliensis, is involved in fungal growth Ganiko, L.; Puccia, R.; Mariano, V. Microbes and Infection, Vol. 9, Issue 6 https://doi.org/10.1016/j.micinf.2007.02.012	journal	May 2007
Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus Teixeira, Marcus M.; Theodoro, Raquel C.; de Carvalho, Maria J. A. Molecular Phylogenetics and Evolution, Vol. 52, Issue 2 https://doi.org/10.1016/j.ympev.2009.04.005	journal	August 2009
Colorimetric Method for Determination of Sugars and Related Substances DuBois, Michel.; Gilles, K. A.; Hamilton, J. K. Analytical Chemistry, Vol. 28, Issue 3, p. 350-356 https://doi.org/10.1021/ac60111a017	journal	March 1956
Definition of the Extracellular Proteome of Pathogenic-Phase Histoplasma capsulatum Holbrook, Eric D.; Edwards, Jessica A.; Youseff, Brian H. Journal of Proteome Research, Vol. 10, Issue 4 https://doi.org/10.1021/pr1011697	journal	April 2011
Vesicle and Vesicle-Free Extracellular Proteome of Paracoccidioides brasiliensis : Comparative Analysis with Other Pathogenic Fungi Vallejo, Milene C.; Nakayasu, Ernesto S.; Matsuo, Alisson L. Journal of Proteome Research, Vol. 11, Issue 3 https://doi.org/10.1021/pr200872s	journal	January 2012
Immunity to fungal infections Romani, Luigina Nature Reviews Immunology, Vol. 11, Issue 4 https://doi.org/10.1038/nri2939	journal	March 2011
Extracellular vesicle-mediated export of fungal RNA Peres da Silva, Roberta; Puccia, Rosana; Rodrigues, Marcio L. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep07763	journal	January 2015
Microarray evaluation of the effects of lectin and glycoprotein orientation and data filtering on glycoform discrimination Gerlach, Jared Q.; Kilcoyne, Michelle; Joshi, Lokesh Anal. Methods, Vol. 6, Issue 2 https://doi.org/10.1039/C3AY40936H	journal	January 2014
Surface chemistry and linker effects on lectin–carbohydrate recognition for glycan microarrays Kilcoyne, Michelle; Gerlach, Jared Q.; Kane, Marian Analytical Methods, Vol. 4, Issue 9 https://doi.org/10.1039/c2ay25532d	journal	January 2012
The composition of the cell wall of Fusicoccum amygdali Buck, K. W.; Obaidah, M. A. Biochemical Journal, Vol. 125, Issue 2 https://doi.org/10.1042/bj1250461	journal	November 1971
Histoplasma capsulatum -(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor Rappleye, C. A.; Eissenberg, L. G.; Goldman, W. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 4 https://doi.org/10.1073/pnas.0609848104	journal	January 2007
A Single UDP-galactofuranose Transporter Is Required for Galactofuranosylation in Aspergillus fumigatus Engel, Jakob; Schmalhorst, Philipp S.; Dörk-Bousset, Thilo Journal of Biological Chemistry, Vol. 284, Issue 49 https://doi.org/10.1074/jbc.M109.070219	journal	October 2009
Ultrastructure of spore formation in Paracoccidioides brasiliensis San-Blas, Felipe Medical Mycology, Vol. 24, Issue 3 https://doi.org/10.1080/02681218680000301	journal	January 1986
Experimental murine paracoccidiodomycosis induced by the inhalation of conidia McEwen, Juan G.; Bedoya, Victor; Patiño, Maria M. Medical Mycology, Vol. 25, Issue 3 https://doi.org/10.1080/02681218780000231	journal	January 1987
Galactofuranose containing molecules in Aspergillus fumigatus Latge, Jean-Paul Medical Mycology, Vol. 47, Issue s1 https://doi.org/10.1080/13693780802258832	journal	January 2009
The habitat of Paracoccidioides brasiliensis : how far from solving the riddle? Restrepo, A.; McEwen, J. G.; Castañeda, E. Medical Mycology, Vol. 39, Issue 3 https://doi.org/10.1080/mmy.39.3.233.241	journal	January 2001
The structure of cell wall -glucan from fission yeast Grun, C. H. Glycobiology, Vol. 15, Issue 3 https://doi.org/10.1093/glycob/cwi002	journal	September 2004
Cross-platform comparison of glycan microarray formats Wang, Linlin; Cummings, Richard D.; Smith, David F. Glycobiology, Vol. 24, Issue 6 https://doi.org/10.1093/glycob/cwu019	journal	March 2014
Eukaryotic starch degradation: integration of plastidial and cytosolic pathways Fettke, Joerg; Hejazi, Mahdi; Smirnova, Julia Journal of Experimental Botany, Vol. 60, Issue 10 https://doi.org/10.1093/jxb/erp054	journal	March 2009
Membrane Transport in Primitive Cells Mansy, S. S. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 8 https://doi.org/10.1101/cshperspect.a002188	journal	April 2010
Compositional and immunobiological analyses of extracellular vesicles released by C andida albicans : Extracellular vesicles from Vargas, Gabriele; Rocha, Juliana D. B.; Oliveira, Debora Leite Cellular Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/cmi.12374	journal	November 2014
NMR evidence for oligosaccharide release from the dendritic-cell specific intercellular adhesion molecule 3-grabbing non-integrin-related (CLEC4M) carbohydrate recognition domain at low pH Probert, Fay; Mitchell, Daniel A.; Dixon, Ann M. FEBS Journal, Vol. 281, Issue 16 https://doi.org/10.1111/febs.12899	journal	July 2014
An ?-(1,4)-amylase is essential for ?-(1,3)-glucan production and virulence in Histoplasma capsulatum Marion, Christopher L.; Rappleye, Chad A.; Engle, Jacquelyn T. Molecular Microbiology, Vol. 62, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05436.x	journal	November 2006
Vesicular transport in Histoplasma capsulatum : an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes Albuquerque, Priscila Costa; Nakayasu, Ernesto S.; Rodrigues, Marcio L. Cellular Microbiology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1462-5822.2008.01160.x	journal	August 2008
Tasting the fungal cell wall: Tasting fungal cell wall Latgé, Jean-Paul Cellular Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-5822.2010.01474.x	journal	May 2010
Immunochemical analysis of the H and M glycoproteins from Histoplasma capsulatum. Zancopé-Oliveira, R. M.; Bragg, S. L.; Reiss, E. Clinical and diagnostic laboratory immunology, Vol. 1, Issue 5 https://doi.org/10.1128/CDLI.1.5.563-568.1994	journal	January 1994
The Pathogenic Fungus Paracoccidioides brasiliensis Exports Extracellular Vesicles Containing Highly Immunogenic α-Galactosyl Epitopes Vallejo, Milene C.; Matsuo, Alisson L.; Ganiko, Luciane Eukaryotic Cell, Vol. 10, Issue 3 https://doi.org/10.1128/EC.00227-10	journal	January 2011
Vesicular Polysaccharide Export in Cryptococcus neoformans Is a Eukaryotic Solution to the Problem of Fungal Trans-Cell Wall Transport Rodrigues, Marcio L.; Nimrichter, Leonardo; Oliveira, Débora L. Eukaryotic Cell, Vol. 6, Issue 1 https://doi.org/10.1128/EC.00318-06	journal	November 2006
A Yeast under Cover: the Capsule of Cryptococcus neoformans Bose, Indrani; Reese, Amy J.; Ory, Jeramia J. Eukaryotic Cell, Vol. 2, Issue 4 https://doi.org/10.1128/EC.2.4.655-663.2003	journal	August 2003
Distribution and conformation of crystalline nigeran in hyphal walls of Aspergillus niger and Aspergillus awamori. Bobbitt, T. F.; Nordin, J. H.; Roux, M. Journal of Bacteriology, Vol. 132, Issue 2 https://doi.org/10.1128/JB.132.2.691-703.1977	journal	January 1977
Characterization of the carbohydrate component of fraction I in the Neurospora crassa cell wall. Cardemil, L.; Pincheira, G. Journal of Bacteriology, Vol. 137, Issue 3 https://doi.org/10.1128/JB.137.3.1067-1072.1979	journal	January 1979
Microsatellite Analysis of Three Phylogenetic Species of Paracoccidioides brasiliensis Matute, D. R.; Sepulveda, V. E.; Quesada, L. M. Journal of Clinical Microbiology, Vol. 44, Issue 6 https://doi.org/10.1128/JCM.02540-05	journal	June 2006
Cell Wall Assembly in Saccharomyces cerevisiae Lesage, G.; Bussey, H. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/MMBR.00038-05	journal	June 2006
Immunochemical analysis of the H and M glycoproteins from Histoplasma capsulatum. Zancopé-Oliveira, R. M.; Bragg, S. L.; Reiss, E. Clinical and diagnostic laboratory immunology, Vol. 1, Issue 5 https://doi.org/10.1128/cdli.1.5.563-568.1994	journal	January 1994
Distribution and conformation of crystalline nigeran in hyphal walls of Aspergillus niger and Aspergillus awamori. Bobbitt, T. F.; Nordin, J. H.; Roux, M. Journal of Bacteriology, Vol. 132, Issue 2 https://doi.org/10.1128/jb.132.2.691-703.1977	journal	January 1977
Characterization of the carbohydrate component of fraction I in the Neurospora crassa cell wall. Cardemil, L.; Pincheira, G. Journal of Bacteriology, Vol. 137, Issue 3 https://doi.org/10.1128/jb.137.3.1067-1072.1979	journal	January 1979
Diversity in unconventional protein secretion Rabouille, Catherine; Malhotra, Vivek; Nickel, Walter Journal of Cell Science, Vol. 125, Issue 22 https://doi.org/10.1242/jcs.103630	journal	November 2012
Recombinant Paracoccin Reproduces the Biological Properties of the Native Protein and Induces Protective Th1 Immunity against Paracoccidioides brasiliensis Infection Alegre, Ana Claudia Paiva; Oliveira, Aline Ferreira; Dos Reis Almeida, Fausto Bruno PLoS Neglected Tropical Diseases, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pntd.0002788	journal	April 2014
Influence of N-Glycosylation on the Morphogenesis and Growth of Paracoccidioides brasiliensis and on the Biological Activities of Yeast Proteins Dos Reis Almeida, Fausto Bruno; Carvalho, Fernanda Caroline; Mariano, Vânia Sammartino PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0029216	journal	December 2011
Lipidomic Analysis of Extracellular Vesicles from the Pathogenic Phase of Paracoccidioides brasiliensis Vallejo, Milene C.; Nakayasu, Ernesto S.; Longo, Larissa V. G. PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039463	journal	June 2012
Expression of Paracoccidioides brasiliensis AMY1 in a Histoplasma capsulatum amy1 Mutant, Relates an α-(1,4)-Amylase to Cell Wall α-(1,3)-Glucan Synthesis Camacho, Emma; Sepulveda, Victoria E.; Goldman, William E. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0050201	journal	November 2012
Surface Glycosylation Profiles of Urine Extracellular Vesicles Gerlach, Jared Q.; Krüger, Anja; Gallogly, Susan PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074801	journal	September 2013
Vesicular transport systems in fungi Rodrigues, Marcio L.; Nosanchuk, Joshua D.; Schrank, Augusto Future Microbiology, Vol. 6, Issue 11 https://doi.org/10.2217/fmb.11.112	journal	November 2011
Cell wall glucan synthases and GTPases in Paracoccidioides brasiliensis Sorais, Françoise; Barreto, Laura; Leal, Juan Antonio Medical Mycology, Vol. 48, Issue 1 https://doi.org/10.3109/13693780802713356	journal	February 2010
Sweeten PAMPs: role of sugar complexed PAMPs in innate immunity and vaccine biology Mahla, Ranjeet Singh Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00248	journal	January 2013
Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes Crescitelli, Rossella; Lässer, Cecilia; Szabó, Tamas G. Journal of Extracellular Vesicles, Vol. 2, Issue 1 https://doi.org/10.3402/jev.v2i0.20677	journal	January 2013
Biogenesis of extracellular vesicles in yeast: Many questions with few answers Oliveira, Débora L.; Nakayasu, Ernesto S.; Joffe, Luna S. Communicative & Integrative Biology, Vol. 3, Issue 6 https://doi.org/10.4161/cib.3.6.12756	journal	November 2010

Cited By (27)

REG3β modifies cell tumor function by impairing extracellular vesicle uptake Bonjoch, Laia; Gironella, Meritxell; Iovanna, Juan Lucio Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03244-4	journal	June 2017
Down-regulation of TUFM impairs host cell interaction and virulence by Paracoccidioides brasiliensis Marcos, Caroline Maria; Tamer, Gabrielle; de Oliveira, Haroldo Cesar Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-51540-y	journal	November 2019
Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling Zhao, Kening; Bleackley, Mark; Chisanga, David Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0538-8	journal	August 2019
Extracellular vesicles from Paracoccidioides brasiliensis induced M1 polarization in vitro da Silva, Thiago Aparecido; Roque-Barreira, Maria Cristina; Casadevall, Arturo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35867	journal	October 2016
A Novel Protocol for the Isolation of Fungal Extracellular Vesicles Reveals the Participation of a Putative Scramblase in Polysaccharide Export and Capsule Construction in Cryptococcus gattii Reis, Flavia C. G.; Borges, Beatriz S.; Jozefowicz, Luísa J. mSphere, Vol. 4, Issue 2 https://doi.org/10.1128/msphere.00080-19	journal	March 2019
Potential Roles of Fungal Extracellular Vesicles during Infection Joffe, Luna S.; Nimrichter, Leonardo; Rodrigues, Marcio L. mSphere, Vol. 1, Issue 4 https://doi.org/10.1128/msphere.00099-16	journal	June 2016
Fungal Extracellular Vesicles as Potential Targets for Immune Interventions Freitas, Mateus Silveira; Bonato, Vânia Luiza Deperon; Pessoni, Andre Moreira mSphere, Vol. 4, Issue 6 https://doi.org/10.1128/msphere.00747-19	journal	October 2019
Anti-Immune Strategies of Pathogenic Fungi Marcos, Caroline M.; de Oliveira, Haroldo C.; de Melo, Wanessa de Cássia M. Antunes Frontiers in Cellular and Infection Microbiology, Vol. 6 https://doi.org/10.3389/fcimb.2016.00142	journal	November 2016
Tumor-Derived Apoptotic Vesicles: With Death They Do Part Muhsin-Sharafaldine, Morad-Remy; McLellan, Alexander D. Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00957	journal	May 2018
Extracellular Vesicle-Associated Transitory Cell Wall Components and Their Impact on the Interaction of Fungi with Host Cells Nimrichter, Leonardo; de Souza, Marcio M.; Del Poeta, Maurizio Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01034	journal	July 2016
Comparison of the RNA Content of Extracellular Vesicles Derived from Paracoccidioides brasiliensis and Paracoccidioides lutzii Peres da Silva, Roberta; Longo, Larissa G. V.; Cunha, Julia P. C. da Cells, Vol. 8, Issue 7 https://doi.org/10.3390/cells8070765	journal	July 2019
Assessing Bacterial Interactions Using Carbohydrate-Based Microarrays Flannery, Andrea; Gerlach, Jared; Joshi, Lokesh Microarrays, Vol. 4, Issue 4 https://doi.org/10.3390/microarrays4040690	journal	December 2015
Extracellular Vesicles in Fungi: Composition and Functions de Toledo Martins, Sharon; Szwarc, Paulo; Goldenberg, Samuel Fungal Physiology and Immunopathogenesis https://doi.org/10.1007/82_2018_141	book	January 2018
Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling Zhao, Kening; Bleackley, Mark; Chisanga, David Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0538-8	journal	August 2019
Synthesis of oligosaccharides related to galactomannans from Aspergillus fumigatus and their NMR spectral data Krylov, V. B.; Argunov, D. A.; Solovev, A. S. Organic & Biomolecular Chemistry, Vol. 16, Issue 7 https://doi.org/10.1039/c7ob02734f	journal	January 2018
Biotoxic Effect of Chromium (VI) on Plant Growth-Promoting Traits of Novel Cellulosimicrobium funkei Strain AR8 Isolated from Phaseolus vulgaris Rhizosphere Karthik, Chinnannan; Arulselvi, P. Indra Geomicrobiology Journal https://doi.org/10.1080/01490451.2016.1219429	journal	October 2016
DC-SIGN and VDR polymorphisms are associated with chronic form of paracoccidioidomycosis with oral manifestations Alves Pereira Neto, Tertuliano; Costa Pereira, Alessandro Antônio; Costa Hanemann, João Adolfo Mycoses, Vol. 62, Issue 2 https://doi.org/10.1111/myc.12866	journal	November 2018
Evaluation of (1 → 3)‐β‐D‐glucan assay for diagnosing paracoccidioidomycosis Melo, Analy Salles de Azevedo; Santos, Daniel Wagner de Castro Lima; Lima, Soraia Lopes Mycoses, Vol. 63, Issue 1 https://doi.org/10.1111/myc.13007	journal	November 2019
A Novel Protocol for the Isolation of Fungal Extracellular Vesicles Reveals the Participation of a Putative Scramblase in Polysaccharide Export and Capsule Construction in Cryptococcus gattii Reis, Flavia C. G.; Borges, Beatriz S.; Jozefowicz, Luísa J. mSphere, Vol. 4, Issue 2 https://doi.org/10.1128/msphere.00080-19	journal	March 2019
Potential Roles of Fungal Extracellular Vesicles during Infection Joffe, Luna S.; Nimrichter, Leonardo; Rodrigues, Marcio L. mSphere, Vol. 1, Issue 4 https://doi.org/10.1128/msphere.00099-16	journal	June 2016
Fungal Extracellular Vesicles as Potential Targets for Immune Interventions Freitas, Mateus Silveira; Bonato, Vânia Luiza Deperon; Pessoni, Andre Moreira mSphere, Vol. 4, Issue 6 https://doi.org/10.1128/msphere.00747-19	journal	October 2019
Anti-Immune Strategies of Pathogenic Fungi Marcos, Caroline M.; de Oliveira, Haroldo C.; de Melo, Wanessa de Cássia M. Antunes Frontiers in Cellular and Infection Microbiology, Vol. 6 https://doi.org/10.3389/fcimb.2016.00142	journal	November 2016
Extracellular Vesicle-Associated Transitory Cell Wall Components and Their Impact on the Interaction of Fungi with Host Cells Nimrichter, Leonardo; de Souza, Marcio M.; Del Poeta, Maurizio Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01034	journal	July 2016
Pathogen-Derived Extracellular Vesicle-Associated Molecules That Affect the Host Immune System: An Overview Kuipers, Marije E.; Hokke, Cornelis H.; Smits, Hermelijn H. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02182	journal	September 2018
Extracellular Vesicles from the Protozoa Acanthamoeba castellanii: Their Role in Pathogenesis, Environmental Adaptation and Potential Applications Gonçalves, Diego; Ferreira, Marina; Guimarães, Allan Bioengineering, Vol. 6, Issue 1 https://doi.org/10.3390/bioengineering6010013	journal	February 2019
Comparison of the RNA Content of Extracellular Vesicles Derived from Paracoccidioides brasiliensis and Paracoccidioides lutzii Peres da Silva, Roberta; Longo, Larissa G. V.; Cunha, Julia P. C. da Cells, Vol. 8, Issue 7 https://doi.org/10.3390/cells8070765	journal	July 2019
Assessing Bacterial Interactions Using Carbohydrate-Based Microarrays Flannery, Andrea; Gerlach, Jared; Joshi, Lokesh Microarrays, Vol. 4, Issue 4 https://doi.org/10.3390/microarrays4040690	journal	December 2015

Similar Records

Characterization of the Kingella kingae Polysaccharide Capsule and Exopolysaccharide

Journal Article · 2013 · PLoS ONE · OSTI ID:1904589

Starr, Kimberly F.; Porsch, Eric A.; Heiss, Christian; +3 more

Subcellular localization of glycosidases and glycosyltransferases involved in the processing of N-linked oligosaccharides

Journal Article · 1987 · Plant Physiol.; (United States) · OSTI ID:5642213

Sturm, A; Johnson, K D; Szumilo, T; +2 more

Structure and mechanism of biosynthesis of Streptococcus mutans cell wall polysaccharide

Journal Article · 2025 · Nature Communications · OSTI ID:2530521

Rush, Jeffrey S.; Zamakhaeva, Svetlana; Murner, Nicholas R.; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
fungal biology
glycoconjugates
membrane trafficking
polysaccharides

Title: Extracellular vesicles from Paracoccidioides pathogenic species transport polysaccharide and expose ligands for DC-SIGN receptors

Citation Formats

References (98)

Cited By (27)

Similar Records

Related Subjects