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Fungal and Parasitic Infections

Characterization of Extracellular Vesicles from Entamoeba histolytica Identifies Roles in Intercellular Communication That Regulates Parasite Growth and Development

Manu Sharma, Pedro Morgado, Hanbang Zhang, Gretchen Ehrenkaufer, Dipak Manna, Upinder Singh
Jeroen P. J. Saeij, Editor
Manu Sharma
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
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Pedro Morgado
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
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Hanbang Zhang
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
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Gretchen Ehrenkaufer
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
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Dipak Manna
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
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Upinder Singh
aDivision of Infectious Diseases, Stanford University School of Medicine, Stanford, California, USA
bDepartment of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, USA
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  • ORCID record for Upinder Singh
Jeroen P. J. Saeij
UC Davis School of Veterinary Medicine
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DOI: 10.1128/IAI.00349-20
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ABSTRACT

Extracellular vesicles (EVs) secreted by eukaryotic and prokaryotic cells to transport lipids, proteins, and nucleic acids to the external environment have important roles in cell-cell communication through cargo transfer. We identified and characterized EVs from Entamoeba histolytica, a protozoan parasite and a human pathogen. Conditioned medium from amebic parasites contained particles consistent with the expected size and morphology of EVs. Mass spectrometry was used to characterize the EV proteome and showed that it was enriched in common exosome marker proteins, including proteins associated with vesicle formation, cell signaling, and metabolism, as well as cytoskeletal proteins. Additionally, the EVs were found to selectively package small RNAs (sRNA), which were protected within the vesicles against RNase treatment. Sequencing analysis of the sRNA contained in EVs revealed that the majority were 27 nucleotides (nt) in size and represented a subset of the cellular antisense small RNA population that has previously been characterized in Entamoeba. RNA interference (RNAi) pathway proteins, including Argonaute, were also present in amebic EVs. Interestingly, we found that the amebic EVs impacted intercellular communication between parasites and altered encystation efficiency. EVs isolated from encysting parasites promoted encystation in other parasites, whereas EVs from metabolically active trophozoites impeded encystation. Overall, the data reveal that Entamoeba secrete EVs that are similar in size and shape to previously characterized exosomes from other organisms and that these EVs contain a defined protein and small RNA cargo and have roles in intercellular communication among parasites and influence growth kinetics.

FOOTNOTES

    • Received 16 June 2020.
    • Accepted 20 July 2020.
    • Accepted manuscript posted online 27 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Characterization of Extracellular Vesicles from Entamoeba histolytica Identifies Roles in Intercellular Communication That Regulates Parasite Growth and Development
Manu Sharma, Pedro Morgado, Hanbang Zhang, Gretchen Ehrenkaufer, Dipak Manna, Upinder Singh
Infection and Immunity Sep 2020, 88 (10) e00349-20; DOI: 10.1128/IAI.00349-20

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Characterization of Extracellular Vesicles from Entamoeba histolytica Identifies Roles in Intercellular Communication That Regulates Parasite Growth and Development
Manu Sharma, Pedro Morgado, Hanbang Zhang, Gretchen Ehrenkaufer, Dipak Manna, Upinder Singh
Infection and Immunity Sep 2020, 88 (10) e00349-20; DOI: 10.1128/IAI.00349-20
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KEYWORDS

Entamoeba
extracellular vesicles
encystation
RNA Interference
intercellular communication
proteomics
sRNA sequencing
exosomes
proteome
small RNAs

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