Elsevier

Virus Research

Volume 257, 15 September 2018, Pages 25-32
Virus Research

Review
LncRNA, miRNA and lncRNA-miRNA interaction in viral infection

https://doi.org/10.1016/j.virusres.2018.08.018Get rights and content

Highlights

  • LncRNAs with different subcellular localization, are involved in different regulatory mechanisms, especially in viral infection.

  • MiRNAs can manipulate host antiviral immune response and virus replication by targeting both viral and cellular genes.

  • LncRNAs can act as miRNAs “sponges” or precursors while miRNAs can regulate lncRNAs and compete for mRNAs in viral infection.

Abstract

Noncoding RNAs (ncRNAs) are key components of the transcriptome and play an important role in both normal biological activity and pathological processes such as viral infection and tumorigenesis. LncRNAs and miRNAs are the most important elements of ncRNAs and function as vital regulatory elements. Their complex regulatory relationship has therefore attracted a lot of attention. In this review, we address the generation, classification, and regulatory mechanisms of lncRNAs and miRNAs in the interaction between virus and host, focusing on their mutual regulation in viral replication and pathogenesis. In-depth analysis of the underlying mechanisms will provide new information for the prevention of viral infections and development of antiviral drugs.

Introduction

Approximately 75% of the human genome is transcribed, but less than 3% encodes proteins. These noncoding RNAs (ncRNAs) were previously regarded as the “genomic noise’ of the coding regions (Chen and Wang, 2013). However, many studies have discovered that ncRNAs play a key role in numerous physiological processes, including cell proliferation and development, differentiation and apoptosis, as well as pathological conditions like disease manifestation, tumorigenesis, and viral infection (Sullivan, 2008). NcRNAs can be classified into housekeeping RNAs and regulatory RNAs. The former, including tRNAs and rRNAs, are ubiquitous in eukaryotic cells while the regulatory RNAs can be divided into small RNAs and long noncoding RNAs (lncRNAs) based on the transcript length. Small RNAs are shorter than 200 nt and include piwiRNAs (piRNAs), small interfering RNAs (siRNAs), small nucleolar RNAs (snoRNAs) and microRNAs (miRNAs). Those longer than 200 nt are known as lncRNAs (Esteller, 2011; Katsarou and Rao, 2015). Here we mainly discuss the roles of miRNA and lncRNA in diverse biological processes according to their function in many emerging fields, especially the interaction with viruses.

Section snippets

Concept and classification

LncRNAs refer to ncRNAs with transcripts greater than 200 nt and lack apparent open-reading frames (ORFs). Over the past few years, lncRNAs have garnered considerable attention due to their roles in transcription, post-transcription and epigenetics networks (Tang and He, 2018; Liu and Mao, 2018; Liu and Ding, 2017; Huang and Wang, 2018), as well as their abundance, diverse classes, and additional functions (Morris and Mattick, 2014). LncRNAs are mainly transcribed by RNA polymerase II (RNA pol

Role of miRNAs in viral replication

MicroRNA (miRNA) is a class of small ncRNAs containing about 22 nt, which modulate many diverse biological processes through post-transcriptional gene regulation (Bartel, 2004). Studies found that some primary transcripts like pri-miR171b and pri-miR165a, which were transcribed by polII in the nucleus and cut into pre-miRNAs by Drosha in the cytoplasm, could translate peptides and promote the accumulation of the corresponding miRNAs (Lauressergues and Couzigou, 2015). Furthermore, studies have

LncRNA-miRNA interaction in viral infection

In virus-infected cells, a variety of ncRNAs encoded by host and viral genes respectively form a regulatory network in the interaction between host and virus. Consequently, the interaction between lncRNAs and miRNAs has continued to provoke great research interest. Many studies have also found a variety of mutual regulatory mechanisms for lncRNAs and miRNAs at the posttranscriptional level (Table 1, Fig. 1).

Discussion and prospects

LncRNAs and miRNAs are vital epigenetic and subcellular regulatory factors that can be included in multilayered cellular biological reactions. In this review, we have summarized the common features and mechanisms of these noncoding transcripts based on three aspects: lncRNAs, miRNAs and the regulatory paradigms between them in viral infection. Furthermore, both lncRNAs and miRNAs have complex and independent regulatory networks, which are often interactional and interoperable within

Author contributions

L.C. and Y.Z. contributed equally to this work.

Conflicts of interest

The authors declare that they have no competing interests.

Acknowledgments

This work was supported by CAMS Initiative for Innovative Medicine (Grant number: 2016-I2M-1-019); National Natural Science Foundation of China (Grant number: 31700154); Science and Technology Project of Yunnan Province—general program(Grant number: 2016FB034); Major Science and Technology Special Project of Yunnan Province (Biomedicine) (Grant number: 2018ZF006).

References (136)

  • K. Katsarou et al.

    Infectious long non-coding RNAs

    Biochimie

    (2015)
  • C.C. Lau et al.

    Viral-human chimeric transcript predisposes risk to liver cancer development and progression

    Cancer Cell

    (2014)
  • H.W. Liang et al.

    Hepatitis B virus-human chimeric transcript HBx-LINE1 promotes hepatic injury via sequestering cellular microRNA-122

    J. Hepatol.

    (2016)
  • A.R. Marquitz et al.

    The Epstein-Barr virus BART microRNAs target the pro-apoptotic protein Bim

    Virology

    (2011)
  • C.P. Ponting et al.

    Evolution and functions of long noncoding RNAs

    Cell

    (2009)
  • L. Salmena et al.

    A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language?

    Cell

    (2011)
  • C.D. Sedano et al.

    Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2

    Cell Host Microbe

    (2014)
  • H. Seitz

    Redefining microRNA targets

    Curr. Biol.

    (2009)
  • C.F. Althaus et al.

    Tailored enrichment strategy detects low abundant small noncoding RNAs in HIV-1 infected cells

    Retrovirology

    (2012)
  • M.G. Andersson et al.

    Suppression of RNA interference by adenovirus virus-associated RNA

    J. Virol.

    (2005)
  • O. Aparicio et al.

    Adenovirus VA RNA-derived miRNAs target cellular genes involved in cell growth, gene expression and DNA repair

    Nucleic Acids Res.

    (2010)
  • C. Arias et al.

    KSHV 2.0: a comprehensive annotation of the Kaposi’s sarcoma-associated herpesvirus genome using next-generation sequencing reveals novel genomic and functional features

    PLoS Pathog.

    (2014)
  • A. Arvey et al.

    Target mRNA abundance dilutes microRNA and siRNA activity

    Mol. Syst. Biol.

    (2010)
  • M.D. Ballantyne et al.

    lncRNA/MicroRNA interactions in the vasculature

    Clin. Pharmacol. Ther.

    (2016)
  • M.A. Bernard et al.

    Novel HIV-1 miRNAs stimulate TNFα release in human macrophages via TLR8 signaling pathway

    PLoS ONE

    (2014)
  • K. Bidet et al.

    G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA

    PLoS Pathog.

    (2014)
  • H.P. Bogerd et al.

    Replication of many human viruses is refractory to inhibition by endogenous cellular microRNAs

    J. Virol.

    (2014)
  • J.C. Burnett et al.

    Control of stochastic gene expression by host factors at the HIV promoter

    PLoS Pathog.

    (2009)
  • M.N. Cabili et al.

    Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses

    Genes Dev.

    (2011)
  • X. Cai et al.

    The imprinted H19 noncoding RNA is a primary microRNA precursor

    RNA

    (2007)
  • X. Cai et al.

    Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed

    PLoS Pathog.

    (2006)
  • D.P. Caley et al.

    Long noncoding RNAs, chromatin, and development

    Sci. World J.

    (2010)
  • W. Cao et al.

    Functional characterization of the bovine foamy virus miRNA expression cassette and its dumbbell-shaped pri-miRNA

    Virus Genes

    (2018)
  • J. Carlevaro-Fita et al.

    Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells

    RNA.

    (2016)
  • D. Cazalla et al.

    Down-regulation of a host microRNA by a viral noncoding RNA

    Cold Spring Harb. Symp. Quant. Biol.

    (2010)
  • D. Cazalla et al.

    A.Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA

    Science

    (2010)
  • J. Chang et al.

    miR-122, a mammalian liver-specifc microRNA, is processed from hcr mRNA and may downregulate the high afnity cationic amino acid transporter CAT-1

    RNA Biol.

    (2004)
  • Z. Chang et al.

    Enterovirus 71 antagonizes the antiviral activity of host STAT3 and IL-6R with partial dependence on virus-induced miR-124

    J. Gen. Virol.

    (2017)
  • G. Chen et al.

    LncRNA Disease:a database for long-non-coding RNA-associated diseases

    Nucleic Acids Res.

    (2013)
  • E.J. Choi et al.

    Differential microRNA expression following infection with a mouse-adapted, highly virulent avian H5N2 virus

    BMC Microbiol.

    (2014)
  • N.K. Conrad et al.

    A Kaposi’s sarcoma virus RNA element that increases the nuclear abundance of intronless transcripts

    EMBO J.

    (2005)
  • H.L. Cook et al.

    The Herpesvirus saimiri small nuclear RNAs recruit AU-rich element-binding proteins but do not alter host AU-rich element-containing mRNA levels in virally transformed T cells

    Mol. Cell. Biol.

    (2004)
  • B.R. Cullen

    Viruses and microRNAs: RISCy interactionswith serious consequences

    Genes Dev.

    (2011)
  • T. Derrien et al.

    The long non-coding RNAs: a new (P)layer in the "Dark matter"

    Front. Genet.

    (2012)
  • T. Derrien et al.

    The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression

    Genome Res.

    (2012)
  • M.S. Ebert et al.

    Emerging roles for natural microRNA sponges

    Curr. Biol.

    (2010)
  • M.S. Ebert et al.

    MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells

    Nat. Methods

    (2007)
  • M. Esteller

    Non-coding RNAs in human disease

    Nat. Rev. Genet.

    (2011)
  • M.A. Faghihi et al.

    Evidence for natural antisense transcript-mediated inhibition of microRNA function

    Genome Biol.

    (2010)
  • R. Gernapudi et al.

    MicroRNA 140 promotes expression of long noncoding RNA NEAT1 in Adipogenesis

    Mol. Cell. Biol.

    (2015)
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