Comprehensive characterization of extracellular vesicles produced by environmental (Neff) and clinical (T4) strains of Acanthamoeba castellanii

Medeiros, Elisa Gonçalves; Valente, Michele Ramos; Honorato, Leandro; Ferreira, Marina Silva; Mendoza, Susana Ruiz; Gonçalves, Diego Souza; Martins Alcântara, Lucas; Gomes, Kamilla Xavier; Pinto, Marcia Ribeiro; Nakayasu, Ernesto S.; Clair, Geremy CD.; da Rocha, Isadora Munhoz; dos Reis, Flavia G.; Rodrigues, Marcio L.; Alves, Lysangela R.; Nimrichter, Leonardo; Casadevall, Arturo; Guimarães, Allan Jefferson

doi:10.1128/msystems.01226-23

Title: Comprehensive characterization of extracellular vesicles produced by environmental (Neff) and clinical (T4) strains of Acanthamoeba castellanii

Journal Article · 07 May 2024 · mSystems

DOI: https://doi.org/10.1128/msystems.01226-23 · OSTI ID:2476846

Medeiros, Elisa Gonçalves ^[1]; Valente, Michele Ramos ^[1]; Honorato, Leandro ^[2]; Ferreira, Marina Silva ^[3]; Mendoza, Susana Ruiz ^[3]; Gonçalves, Diego Souza ^[2]; Martins Alcântara, Lucas ^[1]; Gomes, Kamilla Xavier ^[3]; Pinto, Marcia Ribeiro ^[1];

^[4];

^[4]; da Rocha, Isadora Munhoz ^[5]; dos Reis, Flavia G. ^[6]; Rodrigues, Marcio L. ^[7];

^[5]; Nimrichter, Leonardo ^[8];

^[9];

^[10]

Universidade Federal Fluminense, Niterói, Rio de Janeiro (Brazil)
Universidade Federal do Rio de Janeiro (UFRJ) (Brazil)
Universidade Federal Fluminense, Niterói, Rio de Janeiro (Brazil); Universidade Federal do Rio de Janeiro (UFRJ) (Brazil)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Fundação Oswaldo Cruz, Fiocruz, Curitiba, Paraná (Brazil)
Fundação Oswaldo Cruz, Fiocruz, Curitiba, Paraná (Brazil); Centro de Desenvolvimento Tecnológico em Saúde (CDTS), Fiocruz, Rio de Janeiro (Brazil)
Fundação Oswaldo Cruz, Fiocruz, Curitiba, Paraná (Brazil)l; Instituto de Microbiologia Paulo de Góes, UFRJ, Rio de Janeiro (Brazil)
Universidade Federal do Rio de Janeiro (UFRJ) (Brazil); Rede Micologia RJ–Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Rio de Janeiro (Brazil)
Johns Hopkins Bloomberg School of Public Health, Baltimore, MD (United States)
Universidade Federal Fluminense, Niterói, Rio de Janeiro (Brazil); Universidade Federal do Rio de Janeiro (UFRJ) (Brazil); Rede Micologia RJ–Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (Brazil)

We conducted a comprehensive comparative analysis of extracellular vesicles (EVs) from two Acanthamoeba castellanii strains, Neff (environmental) and T4 (clinical). Morphological analysis via transmission electron microscopy revealed slightly larger Neff EVs (average = 194.5 nm) compared to more polydisperse T4 EVs (average = 168.4 nm). Nanoparticle tracking analysis (NTA) and dynamic light scattering validated these differences. Proteomic analysis of the EVs identified 1,352 proteins, with 1,107 common, 161 exclusive in Neff, and 84 exclusively in T4 EVs. Gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) mapping revealed distinct molecular functions and biological processes and notably, the T4 EVs enrichment in serine proteases, aligned with its pathogenicity. Lipidomic analysis revealed a prevalence of unsaturated lipid species in Neff EVs, particularly triacylglycerols, phosphatidylethanolamines (PEs), and phosphatidylserine, while T4 EVs were enriched in diacylglycerols and diacylglyceryl trimethylhomoserine, phosphatidylcholine and less unsaturated PEs, suggesting differences in lipid metabolism and membrane permeability. Metabolomic analysis indicated Neff EVs enrichment in glycerolipid metabolism, glycolysis, and nucleotide synthesis, while T4 EVs, methionine metabolism. Furthermore, RNA-seq of EVs revealed differential transcript between the strains, with Neff EVs enriched in transcripts related to gluconeogenesis and translation, suggesting gene regulation and metabolic shift, while in the T4 EVs transcripts were associated with signal transduction and protein kinase activity, indicating rapid responses to environmental changes. In this novel study, data integration highlighted the differences in enzyme profiles, metabolic processes, and potential origins of EVs in the two strains shedding light on the diversity and complexity of A. castellanii EVs and having implications for understanding host-pathogen interactions and developing targeted interventions for Acanthamoeba-related diseases.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

Sponsoring Organization:: Conselho Nacional de Desenvolvimento Científico e Tecnológico; Fundação Carlos Chagas de Amparo à Pesquisa no Estado do Rio de Janeiro; USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2476846

Report Number(s):: PNNL-SA--201186

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 6 Vol. 9; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (101)

Distinct immunomodulatory properties of extracellular vesicles released by different strains of Acanthamoeba Costa, Adriana Oliveira; Chagas, Isabela Aurora Rodrigues; de Menezes‐Neto, Armando Cell Biology International, Vol. 45, Issue 5 https://doi.org/10.1002/cbin.11551	journal	February 2021
Updating MISEV: Evolving the minimal requirements for studies of extracellular vesicles Witwer, Kenneth W.; Goberdhan, Deborah CI; O'Driscoll, Lorraine Journal of Extracellular Vesicles, Vol. 10, Issue 14 https://doi.org/10.1002/jev2.12182	journal	December 2021
Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches Welsh, Joshua A.; Goberdhan, Deborah C. I.; O'Driscoll, Lorraine Journal of Extracellular Vesicles, Vol. 13, Issue 2 https://doi.org/10.1002/jev2.12404	journal	February 2024
Current knowledge on exosome biogenesis and release Hessvik, Nina Pettersen; Llorente, Alicia Cellular and Molecular Life Sciences, Vol. 75, Issue 2 https://doi.org/10.1007/s00018-017-2595-9	journal	July 2017
Experimental infection of T4 Acanthamoeba genotype determines the pathogenic potential Alves, Daniella de Sousa Mendes Moreira; Moraes, Aline Silva; Alves, Luciano Moreira Parasitology Research, Vol. 115, Issue 9 https://doi.org/10.1007/s00436-016-5105-3	journal	May 2016
Characterization of extracellular proteases of Acanthamoeba genotype T4 isolated from different sources in Iran Mahdavi Poor, Behroz; Dalimi, Abdolhossein; Ghafarifar, Fatemeh Parasitology Research, Vol. 116, Issue 12 https://doi.org/10.1007/s00436-017-5656-y	journal	October 2017
Genotype distribution of Acanthamoeba in keratitis: a systematic review Diehl, Maria Luisa Nunes; Paes, Júlia; Rott, Marilise Brittes Parasitology Research, Vol. 120, Issue 9 https://doi.org/10.1007/s00436-021-07261-1	journal	August 2021
Dictyostelium Extracellular Vesicles Containing Hoechst 33342 Transfer the Dye into the Nuclei of Living Cells: A Fluorescence Study Tatischeff, Irène; Lavialle, Françoise; Pigaglio-Deshayes, Sophie Journal of Fluorescence, Vol. 18, Issue 2 https://doi.org/10.1007/s10895-007-0271-4	journal	December 2007
War of the microbial world: Acanthamoeba spp. interactions with microorganisms Mungroo, Mohammad Ridwane; Siddiqui, Ruqaiyyah; Khan, Naveed Ahmed Folia Microbiologica, Vol. 66, Issue 5 https://doi.org/10.1007/s12223-021-00889-7	journal	June 2021
“Feast-Fit-Fist-Feat”: Overview of Free-living Amoeba Interactions with Fungi and Virulence as a Foundation for Success in Battle da Silva Ferreira, Marina; de Souza Gonçalves, Diego; Medeiros, Elisa Gonçalves Current Tropical Medicine Reports, Vol. 8, Issue 1 https://doi.org/10.1007/s40475-020-00220-3	journal	January 2021
Membrane proteins significantly restrict exosome mobility Skliar, Mikhail; Chernyshev, Vasiliy S.; Belnap, David M. Biochemical and Biophysical Research Communications, Vol. 501, Issue 4 https://doi.org/10.1016/j.bbrc.2018.05.107	journal	July 2018
Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies Subra, Caroline; Laulagnier, Karine; Perret, Bertrand Biochimie, Vol. 89, Issue 2 https://doi.org/10.1016/j.biochi.2006.10.014	journal	February 2007
Control of protein synthesis and mRNA degradation by microRNAs Liu, Jidong Current Opinion in Cell Biology, Vol. 20, Issue 2 https://doi.org/10.1016/j.ceb.2008.01.006	journal	April 2008
Recovery of an Acanthamoeba strain with two group I introns in the nuclear 18S rRNA gene Corsaro, Daniele; Köhsler, Martina; Venditti, Danielle European Journal of Protistology, Vol. 68 https://doi.org/10.1016/j.ejop.2019.01.007	journal	April 2019
Acanthamoeba: Could it be an environmental host of Shigella? Jeong, Hae Jin; Jang, Eun Seong; Han, Byung In Experimental Parasitology, Vol. 115, Issue 2 https://doi.org/10.1016/j.exppara.2006.08.002	journal	February 2007
Acanthamoeba culbertsoni: Analysis of amoebic adhesion and invasion on extracellular matrix components collagen I and laminin-1 Rocha-Azevedo, Bruno da; Jamerson, Melissa; Cabral, Guy A. Experimental Parasitology, Vol. 126, Issue 1 https://doi.org/10.1016/j.exppara.2009.08.004	journal	September 2010
Acanthamoeba is an evolutionary ancestor of macrophages: A myth or reality? Siddiqui, Ruqaiyyah; Khan, Naveed Ahmed Experimental Parasitology, Vol. 130, Issue 2 https://doi.org/10.1016/j.exppara.2011.11.005	journal	February 2012
Exosome and Exosomal MicroRNA: Trafficking, Sorting, and Function Zhang, Jian; Li, Sha; Li, Lu Genomics, Proteomics & Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1016/j.gpb.2015.02.001	journal	February 2015
Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals Schuster, Frederick L.; Visvesvara, Govinda S. International Journal for Parasitology, Vol. 34, Issue 9 https://doi.org/10.1016/j.ijpara.2004.06.004	journal	August 2004
The Evolution of Aggregative Multicellularity and Cell–Cell Communication in the Dictyostelia Du, Qingyou; Kawabe, Yoshinori; Schilde, Christina Journal of Molecular Biology, Vol. 427, Issue 23 https://doi.org/10.1016/j.jmb.2015.08.008	journal	November 2015
Metabolomic analysis of Entamoeba: applications and implications Jeelani, Ghulam; Nozaki, Tomoyoshi Current Opinion in Microbiology, Vol. 20 https://doi.org/10.1016/j.mib.2014.05.016	journal	August 2014
Emerging roles for extracellular vesicles in parasitic infections Marti, Matthias; Johnson, Patricia J. Current Opinion in Microbiology, Vol. 32 https://doi.org/10.1016/j.mib.2016.04.008	journal	August 2016
Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence Guimaraes, Allan J.; Gomes, Kamilla Xavier; Cortines, Juliana Reis Microbiological Research, Vol. 193 https://doi.org/10.1016/j.micres.2016.08.001	journal	December 2016
Thai Acanthamoeba isolate (T4) induced apoptotic death in neuroblastoma cells via the Bax-mediated pathway Chusattayanond, Araya Dharmkrong-at; Boonsilp, Siriphan; Kasisit, Jitra Parasitology International, Vol. 59, Issue 4 https://doi.org/10.1016/j.parint.2010.06.007	journal	December 2010
Possible Roles of Phospholipase A2 in the Biological Activities of Acanthamoeba castellanii (T4 Genotype) Mortazavi, Parisa Nakhostin; Keisary, Ehud; Loh, Lip Nam Protist, Vol. 162, Issue 1 https://doi.org/10.1016/j.protis.2010.03.005	journal	January 2011
The Neff strain of Acanthamoeba castellanii, a tool for testing the virulence of Mycobacterium kansasii Goy, Geneviève; Thomas, Vincent; Rimann, Katia Research in Microbiology, Vol. 158, Issue 4, p. 393-397 https://doi.org/10.1016/j.resmic.2007.01.003	journal	May 2007
A preliminary proteomic characterisation of extracellular vesicles released by the ovine parasitic nematode, Teladorsagia circumcincta Tzelos, Thomas; Matthews, Jacqueline B.; Buck, Amy H. Veterinary Parasitology, Vol. 221 https://doi.org/10.1016/j.vetpar.2016.03.008	journal	May 2016
Cell signaling during development of Dictyostelium Loomis, William F. Developmental Biology, Vol. 391, Issue 1 https://doi.org/10.1016/j.ydbio.2014.04.001	journal	July 2014
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian Analytical Chemistry, Vol. 81, Issue 9 https://doi.org/10.1021/ac802689c	journal	May 2009
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup Analytical Chemistry, Vol. 81, Issue 24 https://doi.org/10.1021/ac9019522	journal	December 2009
Improved Particle Size Distribution Measurements Using Multiangle Dynamic Light Scattering. 2. Refinements and Applications Bryant, Gary; Abeynayake, Canicious; Thomas, John C. Langmuir, Vol. 12, Issue 26 https://doi.org/10.1021/la960224o	journal	January 1996
The ceramide pathway is involved in the survival, apoptosis and exosome functions of human multiple myeloma cells in vitro Cheng, Qian; Li, Xin; Wang, Yue Acta Pharmacologica Sinica, Vol. 39, Issue 4 https://doi.org/10.1038/aps.2017.118	journal	August 2017
Membrane vesicle-mediated bacterial communication Toyofuku, Masanori; Morinaga, Kana; Hashimoto, Yohei The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.13	journal	March 2017
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Cox, Jürgen; Mann, Matthias Nature Biotechnology, Vol. 26, Issue 12 https://doi.org/10.1038/nbt.1511	journal	November 2008
Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Valadi, Hadi; Ekström, Karin; Bossios, Apostolos Nature Cell Biology, Vol. 9, Issue 6 https://doi.org/10.1038/ncb1596	journal	May 2007
Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity Buck, Amy H.; Coakley, Gillian; Simbari, Fabio Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6488	journal	November 2014
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Sending a message: extracellular vesicles of pathogenic protozoan parasites Szempruch, Anthony J.; Dennison, Lauren; Kieft, Rudo Nature Reviews Microbiology, Vol. 14, Issue 11 https://doi.org/10.1038/nrmicro.2016.110	journal	September 2016
MPLEx: a method for simultaneous pathogen inactivation and extraction of samples for multi-omics profiling Burnum-Johnson, Kristin E.; Kyle, Jennifer E.; Eisfeld, Amie J. The Analyst, Vol. 142, Issue 3 https://doi.org/10.1039/C6AN02486F	journal	January 2017
Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization Laulagnier, Karine; Motta, Claude; Hamdi, Safouane Biochemical Journal, Vol. 380, Issue 1 https://doi.org/10.1042/BJ20031594	journal	May 2004
Capsule of Cryptococcus neoformans grows by enlargement of polysaccharide molecules Frases, S.; Pontes, B.; Nimrichter, L. Proceedings of the National Academy of Sciences, Vol. 106, Issue 4 https://doi.org/10.1073/pnas.0808995106	journal	January 2009
Cryptococcus neoformansinteractions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages Steenbergen, J. N.; Shuman, H. A.; Casadevall, A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 26 https://doi.org/10.1073/pnas.261418798	journal	December 2001
Proteolipidic Composition of Exosomes Changes during Reticulocyte Maturation Carayon, Kévin; Chaoui, Karima; Ronzier, Elsa Journal of Biological Chemistry, Vol. 286, Issue 39 https://doi.org/10.1074/jbc.M111.257444	journal	September 2011
Cloning and Characterization of a Novel Mannose-binding Protein of Acanthamoeba Garate, Marco; Cao, Zhiyi; Bateman, Erik Journal of Biological Chemistry, Vol. 279, Issue 28 https://doi.org/10.1074/jbc.M402334200	journal	July 2004
Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles Coelho, Carolina; Brown, Lisa; Maryam, Maria Journal of Biological Chemistry, Vol. 294, Issue 4 https://doi.org/10.1074/jbc.RA118.006472	journal	November 2018
Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines Théry, Clotilde; Witwer, Kenneth W.; Aikawa, Elena Journal of Extracellular Vesicles, Vol. 7, Issue 1 https://doi.org/10.1080/20013078.2018.1535750	journal	November 2018
Extracellular vesicle measurements with nanoparticle tracking analysis – An accuracy and repeatability comparison between NanoSight NS300 and ZetaView Bachurski, Daniel; Schuldner, Maximiliane; Nguyen, Phuong‐Hien Journal of Extracellular Vesicles, Vol. 8, Issue 1 https://doi.org/10.1080/20013078.2019.1596016	journal	April 2019
Extracellular vesicles and vesicle-free secretome of the protozoa Acanthamoeba castellanii under homeostasis and nutritional stress and their damaging potential to host cells Gonçalves, Diego de Souza; Ferreira, Marina da Silva; Liedke, Susie Coutinho Virulence, Vol. 9, Issue 1 https://doi.org/10.1080/21505594.2018.1451184	journal	May 2018
Extracellular vesicles: Exosomes, microvesicles, and friends Raposo, Graça; Stoorvogel, Willem The Journal of Cell Biology, Vol. 200, Issue 4 https://doi.org/10.1083/jcb.201211138	journal	February 2013
LIQUID: an-open source software for identifying lipids in LC-MS/MS-based lipidomics data Kyle, Jennifer E.; Crowell, Kevin L.; Casey, Cameron P. Bioinformatics, Vol. 33, Issue 11 https://doi.org/10.1093/bioinformatics/btx046	journal	January 2017
Lipid Mini-On: mining and ontology tool for enrichment analysis of lipidomic data Clair, Geremy; Reehl, Sarah; Stratton, Kelly G. Bioinformatics, Vol. 35, Issue 21 https://doi.org/10.1093/bioinformatics/btz250	journal	April 2019
Carcinogenic Liver Fluke Secretes Extracellular Vesicles That Promote Cholangiocytes to Adopt a Tumorigenic Phenotype Chaiyadet, Sujittra; Sotillo, Javier; Smout, Michael Journal of Infectious Diseases, Vol. 212, Issue 10 https://doi.org/10.1093/infdis/jiv291	journal	May 2015
DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update) Sherman, Brad T.; Hao, Ming; Qiu, Ju Nucleic Acids Research, Vol. 50, Issue W1 https://doi.org/10.1093/nar/gkac194	journal	March 2022
MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis Chong, Jasmine; Soufan, Othman; Li, Carin Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky310	journal	May 2018
A descriptive case of persistent Acanthamoeba keratitis: raising awareness of this complex ocular disease Connelly, Lisa; Anijeet, Deepa; Alexander, Claire L. Access Microbiology, Vol. 2, Issue 3 https://doi.org/10.1099/acmi.0.000084	journal	March 2020
Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication Heidel, A. J.; Lawal, H. M.; Felder, M. Genome Research, Vol. 21, Issue 11 https://doi.org/10.1101/gr.121137.111	journal	July 2011
Unravelling the interactions of the environmental hostAcanthamoeba castellaniiwith fungi through the recognition by mannose‐binding proteins Gonçalves, Diego de Souza; Ferreira, Marina da Silva; Gomes, Kamilla Xavier Cellular Microbiology, Vol. 21, Issue 10 https://doi.org/10.1111/cmi.13066	journal	June 2019
Acanthamoeba Interaction with Extracellular Matrix Glycoproteins: Biological and Biochemical Characterization and Role in Cytotoxicity and Invasiveness Rocha‐Azevedo, Bruno Da; Jamerson, Melissa; Cabral, Guy A. Journal of Eukaryotic Microbiology, Vol. 56, Issue 3 https://doi.org/10.1111/j.1550-7408.2009.00399.x	journal	May 2009
The role of proteases in the differentiation ofAcanthamoeba castellanii Dudley, Ricky; Alsam, Selwa; Khan, Naveed Ahmed FEMS Microbiology Letters, Vol. 286, Issue 1 https://doi.org/10.1111/j.1574-6968.2008.01249.x	journal	September 2008
Twenty Years of Acanthamoeba Diagnostics in Austria Walochnik, Julia; Scheikl, Ute; Haller‐Schober, Eva‐Maria Journal of Eukaryotic Microbiology, Vol. 62, Issue 1 https://doi.org/10.1111/jeu.12149	journal	September 2014
A two‐way road: novel roles for fungal extracellular vesicles Rodrigues, Marcio L.; Casadevall, Arturo Molecular Microbiology, Vol. 110, Issue 1 https://doi.org/10.1111/mmi.14095	journal	October 2018
The role of lipids in exosome biology and intercellular communication: Function, analytics and applications Donoso‐Quezada, Javier; Ayala‐Mar, Sergio; González‐Valdez, José Traffic, Vol. 22, Issue 7 https://doi.org/10.1111/tra.12803	journal	June 2021
Characterization of Extracellular Vesicles from Entamoeba histolytica Identifies Roles in Intercellular Communication That Regulates Parasite Growth and Development Sharma, Manu; Morgado, Pedro; Zhang, Hanbang Infection and Immunity, Vol. 88, Issue 10 https://doi.org/10.1128/IAI.00349-20	journal	September 2020
Proteases as Markers for Differentiation of Pathogenic and Nonpathogenic Species of Acanthamoeba Khan, Naveed A.; Jarroll, Edward L.; Panjwani, Noorjahan Journal of Clinical Microbiology, Vol. 38, Issue 8 https://doi.org/10.1128/JCM.38.8.2858-2861.2000	journal	August 2000
Cryptococcus neoformans-Infected Macrophages Release Proinflammatory Extracellular Vesicles: Insight into Their Components by Multi-omics Zhang, Lei; Zhang, Keming; Li, Hang mBio, Vol. 12, Issue 2 https://doi.org/10.1128/mBio.00279-21	journal	April 2021
Amoeba Predation of Cryptococcus neoformans Results in Pleiotropic Changes to Traits Associated with Virulence Fu, Man Shun; Liporagi-Lopes, Livia C.; dos Santos, Samuel R. mBio, Vol. 12, Issue 2 https://doi.org/10.1128/mBio.00567-21	journal	April 2021
Antibody Binding Alters the Characteristics and Contents of Extracellular Vesicles Released by Histoplasma capsulatum Matos Baltazar, Ludmila; Nakayasu, Ernesto S.; Sobreira, Tiago J. P. mSphere, Vol. 1, Issue 2 https://doi.org/10.1128/mSphere.00085-15	journal	March 2016
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses Nakayasu, Ernesto S.; Nicora, Carrie D.; Sims, Amy C. mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00043-16	journal	May 2016
Multi-omics Signature of Candida auris , an Emerging and Multidrug-Resistant Pathogen Zamith-Miranda, Daniel; Heyman, Heino M.; Cleare, Levi G. mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/mSystems.00257-19	journal	June 2019
Comparative Molecular and Immunoregulatory Analysis of Extracellular Vesicles from Candida albicans and Candida auris Zamith-Miranda, Daniel; Heyman, Heino M.; Couvillion, Sneha P. mSystems, Vol. 6, Issue 4 https://doi.org/10.1128/mSystems.00822-21	journal	August 2021
A Comparative Genomic Approach to Determine the Virulence Factors and Horizontal Gene Transfer Events of Clinical Acanthamoeba Isolates Gu, Xiaobin; Lu, Xiuhai; Lin, Shudan Microbiology Spectrum, Vol. 10, Issue 2 https://doi.org/10.1128/spectrum.00025-22	journal	April 2022
Reevaluating the Role ofAcanthamoebaProteases in Tissue Invasion: Observation of Cytopathogenic Mechanisms on MDCK Cell Monolayers and Hamster Corneal Cells Omaña-Molina, Maritza; González-Robles, Arturo; Iliana Salazar-Villatoro, Lizbeth BioMed Research International, Vol. 2013 https://doi.org/10.1155/2013/461329	journal	January 2013
Proteomic Analysis of Human Lung Development Clair, Geremy; Bramer, Lisa M.; Misra, Ravi American Journal of Respiratory and Critical Care Medicine, Vol. 205, Issue 2 https://doi.org/10.1164/rccm.202008-3303OC	journal	January 2022
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
Exocytosis and protein secretion in Trypanosoma Geiger, Anne; Hirtz, Christophe; Bécue, Thierry BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-20	journal	January 2010
VANTED v2: a framework for systems biology applications Rohn, Hendrik; Junker, Astrid; Hartmann, Anja BMC Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1186/1752-0509-6-139	journal	January 2012
Biology and pathogenesis of Acanthamoeba Siddiqui, Ruqaiyyah; Khan, Naveed Ahmed Parasites & Vectors, Vol. 5, Issue 1 https://doi.org/10.1186/1756-3305-5-6	journal	January 2012
Quantitative proteomic analysis and functional characterization of Acanthamoeba castellanii exosome-like vesicles Lin, Wei-Chen; Tsai, Chia-Yun; Huang, Jian-Ming Parasites & Vectors, Vol. 12, Issue 1 https://doi.org/10.1186/s13071-019-3725-z	journal	October 2019
The roles of small RNAs: insights from bacterial quorum sensing Fu, Hongchang; Elena, Rosalía Cardós; Marquez, Paola Handal ExRNA, Vol. 1, Issue 1 https://doi.org/10.1186/s41544-019-0027-8	journal	September 2019
Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis Fitzner, Dirk; Schnaars, Mareike; van Rossum, Denise Journal of Cell Science, Vol. 124, Issue 3 https://doi.org/10.1242/jcs.074088	journal	February 2011
Assets of the non-pathogenic microorganism Dictyostelium discoideum as a model for the study of eukaryotic extracellular vesicles Tatischeff, Irène F1000Research, Vol. 2 https://doi.org/10.12688/f1000research.2-73.v1	journal	March 2013
Extracellular Vesicles from Parasitic Helminths Contain Specific Excretory/Secretory Proteins and Are Internalized in Intestinal Host Cells Marcilla, Antonio; Trelis, María; Cortés, Alba PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0045974	journal	September 2012
Exosomal Lipids Impact Notch Signaling and Induce Death of Human Pancreatic Tumoral SOJ-6 Cells Beloribi, Sadia; Ristorcelli, Elodie; Breuzard, Gilles PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0047480	journal	October 2012
PURIFICATION AND CHARACTERIZATION OF IRON SUPEROXIDE DISMUTASE AND COPPER–ZINC SUPEROXIDE DISMUTASE FROMACANTHAMOEBA CASTELLANII Choi, Dong-Ho; Na, Byoung-Kuk; Seo, Min-Seok Journal of Parasitology, Vol. 86, Issue 5 https://doi.org/10.1645/0022-3395(2000)086[0899:PACOIS]2.0.CO;2	journal	October 2000
Phospholipase Activities in Clinical and Environmental Isolates ofAcanthamoeba Matin, Abdul; Jung, Suk-Yul The Korean Journal of Parasitology, Vol. 49, Issue 1 https://doi.org/10.3347/kjp.2011.49.1.1	journal	January 2011
Recognition of Cell Wall Mannosylated Components as a Conserved Feature for Fungal Entrance, Adaptation and Survival Within Trophozoites of Acanthamoeba castellanii and Murine Macrophages Ferreira, Marina da Silva; Mendoza, Susana Ruiz; Gonçalves, Diego de Souza Frontiers in Cellular and Infection Microbiology, Vol. 12 https://doi.org/10.3389/fcimb.2022.858979	journal	May 2022
Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression Willms, Eduard; Cabañas, Carlos; Mäger, Imre Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00738	journal	April 2018
Biological characteristics and pathogenicity of Acanthamoeba Wang, Yuehua; Jiang, Linzhe; Zhao, Yitong Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1147077	journal	April 2023
Characterization of the extracellular vesicles, ultrastructural morphology, and intercellular interactions of multiple clinical isolates of the brain-eating amoeba, Naegleria fowleri Russell, A. Cassiopeia; Bush, Peter; Grigorean, Gabriela Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1264348	journal	September 2023
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
Characterization of Extracellular Vesicles Secreted by a Clinical Isolate of Naegleria fowleri and Identification of Immunogenic Components within Their Protein Cargo Retana Moreira, Lissette; Steller Espinoza, María Fernanda; Chacón Camacho, Natalia Biology, Vol. 11, Issue 7 https://doi.org/10.3390/biology11070983	journal	June 2022
Extracellular Vesicles and Matrix Remodeling Enzymes: The Emerging Roles in Extracellular Matrix Remodeling, Progression of Diseases and Tissue Repair Nawaz, Muhammad; Shah, Neelam; Zanetti, Bruna Cells, Vol. 7, Issue 10 https://doi.org/10.3390/cells7100167	journal	October 2018
Dictyostelium: A Model for Studying the Extracellular Vesicle Messengers Involved in Human Health and Disease Tatischeff, Irène Cells, Vol. 8, Issue 3 https://doi.org/10.3390/cells8030225	journal	March 2019
Role of Ceramides and Lysosomes in Extracellular Vesicle Biogenesis, Cargo Sorting and Release Horbay, Rostyslav; Hamraghani, Ali; Ermini, Leonardo International Journal of Molecular Sciences, Vol. 23, Issue 23 https://doi.org/10.3390/ijms232315317	journal	December 2022
The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis Casadevall, Arturo; Fu, Man; Guimaraes, Allan Journal of Fungi, Vol. 5, Issue 1 https://doi.org/10.3390/jof5010010	journal	January 2019
Extracellular Vesicles Secreted by Acanthamoeba culbertsoni Have COX and Proteolytic Activity and Induce Hemolysis Sierra-López, Francisco; Castelan-Ramírez, Ismael; Hernández-Martínez, Dolores Microorganisms, Vol. 11, Issue 11 https://doi.org/10.3390/microorganisms11112762	journal	November 2023
Extracellular Vesicles from Naegleria fowleri Induce IL-8 Response in THP-1 Macrophage Lertjuthaporn, Sakaorat; Somkird, Jinjuta; Lekmanee, Kittima Pathogens, Vol. 11, Issue 6 https://doi.org/10.3390/pathogens11060632	journal	May 2022
In Vitro Evaluation of Combined Commercialized Ophthalmic Solutions Against Acanthamoeba Strains Reyes-Batlle, María; Mura-Escorche, Glorian; Sifaoui, Ines Pathogens, Vol. 8, Issue 3 https://doi.org/10.3390/pathogens8030109	journal	July 2019
Isolation of Acanthamoeba T5 from Water: Characterization of Its Pathogenic Potential, Including the Production of Extracellular Vesicles Retana Moreira, Lissette; Vargas Ramírez, Daniel; Linares, Fátima Pathogens, Vol. 9, Issue 2 https://doi.org/10.3390/pathogens9020144	journal	February 2020
Acanthamoeba encephalitis: A Case Report and Review of Therapy Swiatlo, E.; Zamora, A.; Henderson, H. Surgical Neurology International, Vol. 5, Issue 1 https://doi.org/10.4103/2152-7806.132239	journal	January 2014
The role of free-living pathogenic amoeba in the transmission of leprosy: a proof of principle Lahiri, Ramanuj; Krahenbuhl, James L. Leprosy Review, Vol. 79, Issue 4 https://doi.org/10.47276/lr.79.4.401	journal	December 2008

Similar Records

Gene discovery in the Acanthamoeba castellanii genome

Journal Article · 2005 · Protist · OSTI ID:888974

Anderson, Iain J; Watkins, Russell F; Samuelson, John; +4 more

Francisella tularensis type A Strains Cause the Rapid Encystment of Acanthamoeba castellanii and Survive in Amoebal Cysts for Three Weeks post Infection

Journal Article · 2009 · Applied Environmental Microbiology, vol. 75, no. 23, December 15, 2009, pp. 5488 · OSTI ID:972428

El-Etr, S H; Margolis, J; Monack, D; +4 more

Identification of Potent and Selective Inhibitors of Acanthamoeba: Structural Insights into Sterol 14α-Demethylase as a Key Drug Target

Journal Article · 2024 · Journal of Medicinal Chemistry · OSTI ID:2470115

Hargrove, Tatiana Y.; Lamb, David C.; Wawrzak, Zdzislaw; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Acanthamoeba castellanii
Neff
T4
extracellular vesicles
mPLEX
microbiology

Title: Comprehensive characterization of extracellular vesicles produced by environmental (Neff) and clinical (T4) strains of Acanthamoeba castellanii

Citation Formats

References (101)

Similar Records

Related Subjects