Omics Approaches for Understanding Biogenesis, Composition and Functions of Fungal Extracellular Vesicles

Zamith-Miranda, Daniel; Peres da Silva, Roberta; Couvillion, Sneha P.; Bredeweg, Erin L.; Burnet, Meagan C.; Coelho, Carolina; Camacho, Emma; Nimrichter, Leonardo; Puccia, Rosana; Almeida, Igor C.; Casadevall, Arturo; Rodrigues, Marcio L.; Alves, Lysangela R.; Nosanchuk, Joshua D.; Nakayasu, Ernesto S.

doi:10.3389/fgene.2021.648524

Title: Omics Approaches for Understanding Biogenesis, Composition and Functions of Fungal Extracellular Vesicles

Journal Article · Mon May 03 00:00:00 UTC 2021 · Frontiers in Genetics

DOI: https://doi.org/10.3389/fgene.2021.648524 · OSTI ID:1787842

Zamith-Miranda, Daniel ^[1]; Peres da Silva, Roberta ^[2]; Couvillion, Sneha P. ^[3];

^[3]; Burnet, Meagan C. ^[3]; Coelho, Carolina ^[2]; Camacho, Emma ^[4]; Nimrichter, Leonardo ^[5]; Puccia, Rosana ^[6]; Almeida, Igor C. ^[7]; Casadevall, Arturo ^[4]; Rodrigues, Marcio L. ^[8]; Alves, Lysangela R. ^[9]; Nosanchuk, Joshua D. ^[1];

^[3]

Albert Einstein College of Medicine, Bronx, NY (United States)
Univ. of Exeter (United Kingdom)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Johns Hopkins Bloomberg School of Public Health, Baltimore, MD (United States)
Univ. Federal do Rio de Janeiro (Brazil)
Escola Paulista de Medicina-Univ. Federal de São Paulo (Brazil)
Univ. of Texas at El Paso, TX (United States)
Inst. Carlos Chagas-FIOCRUZ PR, Curitiba (Brazil); Univ. Federal do Rio de Janeiro (Brazil)
Inst. Carlos Chagas-FIOCRUZ PR, Curitiba (Brazil)

Extracellular vesicles (EVs) are lipid bilayer structures released by organisms from all kingdoms of life. The diverse biogenesis pathways of EVs result in a wide variety of physical properties and functions across different organisms. Fungal EVs were first described in 2007 and different omics approaches have been fundamental to understand their composition, biogenesis, and function. In this review, we discuss the role of omics in elucidating fungal EVs biology. Transcriptomics, proteomics, metabolomics, and lipidomics have each enabled the molecular characterization of fungal EVs, providing evidence that these structures serve a wide array of functions, ranging from key carriers of cell wall biosynthetic machinery to virulence factors. Omics in combination with genetic approaches have been instrumental in determining both biogenesis and cargo loading into EVs. We also discuss how omics technologies are being employed to elucidate the role of EVs in antifungal resistance, disease biomarkers, and their potential use as vaccines. Finally, we review recent advances in analytical technology and multi-omic integration tools, which will help to address key knowledge gaps in EVs biology and translate basic research information into urgently needed clinical applications such as diagnostics, and immuno- and chemotherapies to fungal infections.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: NIH; NIH/NIMHD; USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1787842

Report Number(s):: PNNL-SA--161136

Journal Information:: Frontiers in Genetics, Journal Name: Frontiers in Genetics Vol. 12; ISSN 1664-8021

Publisher:: Frontiers Media S.A.Copyright Statement

Country of Publication:: United States

Language:: English

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Structural and Functional Analysis of a Platelet-Activating Lysophosphatidylcholine of Trypanosoma cruzi Gazos-Lopes, Felipe; Oliveira, Mauricio M.; Hoelz, Lucas V. B. PLoS Neglected Tropical Diseases, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pntd.0003077	journal	August 2014
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Nanovesicles from Malassezia sympodialis and Host Exosomes Induce Cytokine Responses – Novel Mechanisms for Host-Microbe Interactions in Atopic Eczema Gehrmann, Ulf; Qazi, Khaleda Rahman; Johansson, Catharina PLoS ONE, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pone.0021480	journal	July 2011
Exosomes from Plasmodium yoelii-Infected Reticulocytes Protect Mice from Lethal Infections Martin-Jaular, Lorena; Nakayasu, Ernesto S.; Ferrer, Mireia PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026588	journal	October 2011
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Cryptococcus neoformans-Derived Microvesicles Enhance the Pathogenesis of Fungal Brain Infection Huang, Sheng-He; Wu, Chun-Hua; Chang, Yun C. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0048570	journal	November 2012
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Lysophosphatidylcholine Triggers TLR2- and TLR4-Mediated Signaling Pathways but Counteracts LPS-Induced NO Synthesis in Peritoneal Macrophages by Inhibiting NF-κB Translocation and MAPK/ERK Phosphorylation Carneiro, Alan Brito; Iaciura, Bruna Maria Ferreira; Nohara, Lilian Lie PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0076233	journal	September 2013
Macrophage Interaction with Paracoccidioides brasiliensis Yeast Cells Modulates Fungal Metabolism and Generates a Response to Oxidative Stress Parente-Rocha, Juliana Alves; Parente, Ana Flávia Alves; Baeza, Lilian Cristiane PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0137619	journal	September 2015
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Plasma-Derived Extracellular Vesicles as Potential Biomarkers in Heart Transplant Patient with Chronic Chagas Disease Cortes-Serra, Nuria; Mendes, Maria Tays; Mazagatos, Clara Emerging Infectious Diseases, Vol. 26, Issue 8 https://doi.org/10.3201/eid2608.191042	journal	August 2020
A Perspective on Extracellular Vesicles Proteomics Rosa-Fernandes, Livia; Rocha, Victória Bombarda; Carregari, Victor Corasolla Frontiers in Chemistry, Vol. 5 https://doi.org/10.3389/fchem.2017.00102	journal	November 2017
Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives Rizzo, Juliana; Rodrigues, Marcio L.; Janbon, Guilhem Frontiers in Cellular and Infection Microbiology, Vol. 10 https://doi.org/10.3389/fcimb.2020.00346	journal	July 2020
Tetraspanins in Extracellular Vesicle Formation and Function Andreu, Zoraida; YÃ¡Ã±ez-MÃ³, MarÃa Frontiers in Immunology, Vol. 5 https://doi.org/10.3389/fimmu.2014.00442	journal	September 2014
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
Extracellular Vesicles From Sporothrix brasiliensis Are an Important Virulence Factor That Induce an Increase in Fungal Burden in Experimental Sporotrichosis Ikeda, Marcelo Augusto Kazuo; de Almeida, José Roberto Fogaça; Jannuzzi, Grasielle Pereira Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02286	journal	October 2018
The Still Underestimated Problem of Fungal Diseases Worldwide Almeida, Fausto; Rodrigues, Marcio L.; Coelho, Carolina Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00214	journal	February 2019
Characterization of Aspergillus fumigatus Extracellular Vesicles and Their Effects on Macrophages and Neutrophils Functions Souza, Jéssica Amanda Marques; Baltazar, Ludmila de Matos; Carregal, Virgínia Mendes Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02008	journal	September 2019
Extracellular Vesicles From the Cotton Pathogen Fusarium oxysporum f. sp. vasinfectum Induce a Phytotoxic Response in Plants Bleackley, Mark R.; Samuel, Monisha; Garcia-Ceron, Donovan Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01610	journal	January 2020
Evaluation of Unconventional Protein Secretion by Saccharomyces cerevisiae and other Fungi Miura, Natsuko; Ueda, Mitsuyoshi Cells, Vol. 7, Issue 9 https://doi.org/10.3390/cells7090128	journal	August 2018
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
Characteristics of Extracellular Vesicles Released by the Pathogenic Yeast-Like Fungi Candida glabrata, Candida parapsilosis and Candida tropicalis Karkowska-Kuleta, Justyna; Kulig, Kamila; Karnas, Elzbieta Cells, Vol. 9, Issue 7 https://doi.org/10.3390/cells9071722	journal	July 2020
Golgi Reassembly and Stacking Protein (GRASP) Participates in Vesicle-Mediated RNA Export in Cryptococcus Neoformans Peres da Silva, Roberta; Martins, Sharon de Toledo; Rizzo, Juliana Genes, Vol. 9, Issue 8 https://doi.org/10.3390/genes9080400	journal	August 2018
Functional Diversity of RNAi-Associated sRNAs in Fungi Nicolás, Francisco; Ruiz-Vázquez, Rosa International Journal of Molecular Sciences, Vol. 14, Issue 8 https://doi.org/10.3390/ijms140815348	journal	July 2013
Extracellular Vesicles—Connecting Kingdoms Woith, Eric; Fuhrmann, Gregor; Melzig, Matthias F. International Journal of Molecular Sciences, Vol. 20, Issue 22 https://doi.org/10.3390/ijms20225695	journal	November 2019
Special Issue: Fungal Cell Wall Beauvais, Anne; Latgé, Jean-Paul Journal of Fungi, Vol. 4, Issue 3 https://doi.org/10.3390/jof4030091	journal	August 2018
Remodeling of the Histoplasma Capsulatum Membrane Induced by Monoclonal Antibodies Burnet, Meagan C.; Zamith-Miranda, Daniel; Heyman, Heino M. Vaccines, Vol. 8, Issue 2 https://doi.org/10.3390/vaccines8020269	journal	June 2020
Extracellular vesicles in parasitic diseases Marcilla, Antonio; Martin-Jaular, Lorena; Trelis, Maria Journal of Extracellular Vesicles, Vol. 3, Issue 1 https://doi.org/10.3402/jev.v3.25040	journal	January 2014
Ceramide-Induced TCR Up-Regulation Menné, Charlotte; Lauritsen, Jens Peter H.; Dietrich, Jes The Journal of Immunology, Vol. 165, Issue 6 https://doi.org/10.4049/jimmunol.165.6.3065	journal	September 2000
Extracellular vesicles: the next generation of biomarkers for liquid biopsy-based prostate cancer diagnosis Pang, Bairen; Zhu, Ying; Ni, Jie Theranostics, Vol. 10, Issue 5 https://doi.org/10.7150/thno.39486	journal	January 2020

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