TY - JOUR
T1 - Omics Approaches for Understanding Biogenesis, Composition and Functions of Fungal Extracellular Vesicles
AU - Zamith-Miranda, Daniel
AU - Peres da Silva, Roberta
AU - Couvillion, Sneha P.
AU - Bredeweg, Erin L.
AU - Burnet, Meagan C.
AU - Coelho, Carolina
AU - Camacho, Emma
AU - Nimrichter, Leonardo
AU - Puccia, Rosana
AU - Almeida, Igor C.
AU - Casadevall, Arturo
AU - Rodrigues, Marcio L.
AU - Alves, Lysangela R.
AU - Nosanchuk, Joshua D.
AU - Nakayasu, Ernesto S.
N1 - Funding Information:
This review is dedicated to the memory of Luiz Rodolpho Raja Gabaglia Travassos (1938–2020; Universidade Federal de Sao Paulo, Escola Paulista de Medicina, Brazil), who made numerous seminal contributions to the fields of fungal molecular and cellular biology, and glycobiology. Travassos was one the first investigators who proposed extracellular vesicles as carriers of fungal cell wall, plasma membrane, and intracellular bioactive molecules that could eventually modulate mammalian host infection and immune response, and fungal immunoevasion mechanisms. Funding. DZ-M, JN, and EN were supported by NIH R21 AI124797. EB and EN were supported by a Laboratory Directed Research and Development project from Pacific Northwest National Laboratory (PNNL). AC was supported in part by NIH grants AI052733, AI15207, and HL059842. We were also very grateful to the Biomolecule Analysis and Omics Unit (formerly, Biomolecule Analysis Core Facility), supported by the NIH/NIMHD grants 2G12MD007592-21 and 5U54MD007592 (to Robert A. Kirken), for the access to mass spectrometry systems and other analytical instruments used in several of the studies described here. IA was partially supported by NIH/NIMHD grant 5U54MD007592, and a Special Visiting Researcher of the CNPq/Science Without Borders Science Program, Brazil. EC and AC were funded by the Johns Hopkins Malaria Research Institute Pilot Grant Casadevall_123. RPu was supported by the Brazilian funding agencies FAPESP, CAPES, and CNPq. RPe and CC were funded by Medical Research Council Centre for Medical Mycology at University of Exeter (MR/N006364/2). Parts of this work were performed in the Environmental Molecular Science Laboratory, a United States Department of Energy (DOE) national scientific user facility at PNNL in Richland, WA, United States. EC and AC are funded by NIAID R01 AI052733. EN was also supported by R01 AI127465 from NIAID.
Funding Information:
DZ-M, JN, and EN were supported by NIH R21 AI124797. EB and EN were supported by a Laboratory Directed Research and Development project from Pacific Northwest National Laboratory (PNNL). AC was supported in part by NIH grants AI052733, AI15207, and HL059842. We were also very grateful to the Biomolecule Analysis and Omics Unit (formerly, Biomolecule Analysis Core Facility), supported by the NIH/NIMHD grants 2G12MD007592-21 and 5U54MD007592 (to Robert A. Kirken), for the access to mass spectrometry systems and other analytical instruments used in several of the studies described here. IA was partially supported by NIH/NIMHD grant 5U54MD007592, and a Special Visiting Researcher of the CNPq/Science Without
Publisher Copyright:
© Copyright © 2021 Zamith-Miranda, Peres da Silva, Couvillion, Bredeweg, Burnet, Coelho, Camacho, Nimrichter, Puccia, Almeida, Casadevall, Rodrigues, Alves, Nosanchuk and Nakayasu.
PY - 2021/5/3
Y1 - 2021/5/3
N2 - 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.
AB - 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.
KW - extracellular vesicles
KW - fungi
KW - lipidomics
KW - metabolomics
KW - proteomics
KW - systems biology
KW - transcriptomics
KW - virulence
UR - http://www.scopus.com/inward/record.url?scp=85106017279&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85106017279&partnerID=8YFLogxK
U2 - 10.3389/fgene.2021.648524
DO - 10.3389/fgene.2021.648524
M3 - Review article
C2 - 34012462
AN - SCOPUS:85106017279
SN - 1664-8021
VL - 12
JO - Frontiers in Genetics
JF - Frontiers in Genetics
M1 - 648524
ER -