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Long non-coding RNAs as possible therapeutic targets in protozoa, and in Schistosoma and other helminths

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Abstract

Long non-coding RNAs (lncRNAs) emerged in the past 20 years due to massive amounts of scientific data regarding transcriptomic analyses. They have been implicated in a plethora of cellular processes in higher eukaryotes. However, little is known about lncRNA possible involvement in parasitic diseases, with most studies only detecting their presence in parasites of human medical importance. Here, we review the progress on lncRNA studies and their functions in protozoans and helminths. In addition, we show an example of knockdown of one lncRNA in Schistosoma mansoni, SmLINC156349, which led to in vitro parasite adhesion, motility, and pairing impairment, with a 20% decrease in parasite viability and 33% reduction in female oviposition. Other observed phenotypes were a decrease in the proliferation rate of both male and female worms and their gonads, and reduced female lipid and vitelline droplets that are markers for well-developed vitellaria. Impairment of female worms’ vitellaria in SmLINC156349-silenced worms led to egg development deficiency. All those results demonstrate the great potential of the tools and methods to characterize lncRNAs as potential new therapeutic targets. Further, we discuss the challenges and limitations of current methods for studying lncRNAs in parasites and possible solutions to overcome them, and we highlight the future directions of this exciting field.

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Acknowledgements

We acknowledge Patricia Aoki Miyasato and Dr. Eliana Nakano, Laboratorio de Malacologia, Instituto Butantan, for maintaining the S. mansoni life cycle and providing the infected hamsters. We would like to thank the Laboratório de Biologia Celular from Instituto Butantan and the Confocal Lab Technician Alexsander Seixas de Souza for the services provided on the Confocal Microscope Leica TCS SP8, purchased through Projeto 175 FINEP—IBUINFRA grant 01.12.0175.00 to Dr. Carlos Jared.

Funding

This work was supported by a grant from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Thematic grant number 2018/23693–5 to SV-A). G.O.S. received a fellowship from FAPESP (18/24015–0); H.S.C. received a fellowship from Conselho Nacional do Desenvolvimento Científico e Tecnológico (CNPq) (116733/2019–5); S.V-A laboratory was also supported by institutional funds from Fundação Butantan and S.V-A received an established investigator fellowship award from CNPq, Brasil.

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Authors and Affiliations

Authors

Contributions

Conceived the review: S.V.-A. and M.S.A.; literature search: G.O.S. and M.S.A; data analysis: G.O.S.; performed the in vitro experiments: G.O.S and H.S.C.; wrote the manuscript: G.O.S.; revised the manuscript: G.O.S., M.S.A., S.V.-A.; all authors reviewed the manuscript and approved the submitted version.

Corresponding authors

Correspondence to Murilo S. Amaral or Sergio Verjovski-Almeida.

Ethics declarations

Ethics approval

Housing conditions of the hamsters and experimental procedures used in this study were in strict accordance with the Ethical Principles in Animal Research adopted by the CONCEA and the experimental protocol was approved by the Ethics Committee for Animal Experimentation of Butantan Institute (CEUAIB n˚ 8859090919).

Conflict of interest

The authors declare no competing interests.

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Guest Editor: Anja Taubert

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

5-AzaC

5-azacytidine

alncRNAs

antisense lncRNAs

ASO

antisense oligonucleotides

AUF

autofluorescence

blncRNAs

bidirectional lncRNAs

ChAR-Seq

chromatin-associated RNA sequencing

CHART

capture hybridization analysis of RNA targets

ChIRP

chromatin isolation by RNA purification.

circRNAs

circular RNAs

CLASH

crosslinking, ligation, and sequencing of hybrids

CLIP

UV cross-linking and immunoprecipitation.

crasiRNAs

centromere repeat-associated short interacting RNAs

CRISPR-Cas

clustered regularly interspaced short palindromic repeats – CRISPR associated protein

dsRNA

double-stranded RNA

EdU

5-ethynyl-2′-deoxyuridine

ELVs

exosome-like vesicles

ESTs

expressed sequence tags

FISH

fluorescence in situ hybridization.

GO

gene ontology

GPCR

G-protein coupled receptor

GRID-Seq

global RNA interactions with DNA identified by deep sequencing

HF

hydatid fluid

ilncRNAs

intronic lncRNAs

ISH

in situ hybridization

LC-MS

liquid chromatography–mass spectrometry

LIGR-Seq

ligation of interacting RNA followed by deep sequencing

lincRNAs

intergenic lncRNAs

lncRNAs

long non-coding RNAs

MARGI

mapping RNA-genome interactions

MARIO

mapping RNA interactome in vivo

miRNAs

micro-RNAs

MTZ

metronidazole

ncRNA

non-coding RNA

NTDs

neglected tropical diseases

ORF

open reading frame

PAP

RNA poly (A) polymerases

PARIS

psoralen analysis of RNA interactions and structures

piRNAs

piwi-interacting RNAs

PSCs

protoscoleces

RADICL-Seq

RNA and DNA-interacting complexes ligated identified by deep sequencing

RAP

RNA antisense purification

RBP

RNA binding protein

RIP

RNA immunoprecipitation

RNAi

RNA interference

RNA-Seq

RNA-sequencing

rRNAs

ribosomal RNAs

RT-qPCR

reverse transcription quantitative PCR

scRNAs

small conditional RNAs

scRNA-Seq

single-cell RNA-Seq

SHAPE

selective 2′-hydroxyl acylation analyzed by primer extension

SIF

stumpy induction factor

siRNAs

small interfering RNAs

slncRNAs

sense lncRNAs

snoRNAs

small nucleolar RNAs

SNPs

single nucleotide polymorphisms

snRNAs

small nuclear RNAs

SPLASH

sequencing of psoralen-crosslinked, ligated, and selected hybrids

SRA

sequence read archive

telsRNAs

telomere-specific small RNAs

tiRNAs

tRNA‐derived stress‐induced RNAs

tRNAs

transfer RNAs

TSS

transcription start site

WISH

whole-mount in situ hybridization

Xist

X-inactive specific transcript

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Silveira, G.O., Coelho, H.S., Amaral, M.S. et al. Long non-coding RNAs as possible therapeutic targets in protozoa, and in Schistosoma and other helminths. Parasitol Res 121, 1091–1115 (2022). https://doi.org/10.1007/s00436-021-07384-5

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  • DOI: https://doi.org/10.1007/s00436-021-07384-5

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