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Published in: Virology Journal 1/2020

Open Access 01-12-2020 | Human Cytomegalovirus | Review

MicroRNAs expressed by human cytomegalovirus

Authors: Lichen Zhang, Jiaqi Yu, Zhijun Liu

Published in: Virology Journal | Issue 1/2020

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Abstract

Background

MicroRNAs (miRNAs) are small non-coding RNAs about 22 nucleotides in length, which play an important role in gene regulation of both eukaryotes and viruses. They can promote RNA cleavage and repress translation via base-pairing with complementary sequences within mRNA molecules.

Main body

Human cytomegalovirus (HCMV) encodes a large number of miRNAs that regulate transcriptions of both host cells and themselves to favor viral infection and inhibit the host’s immune response. To date, ~ 26 mature HCMV miRNAs have been identified. Nevertheless, their roles in viral infection are ambiguous, and the mechanisms have not been fully revealed. Therefore, we discuss the methods used in HCMV miRNA research and summarize the important roles of HCMV miRNAs and their potential mechanisms in infection.

Conclusions

To study the miRNAs encoded by viruses and their roles in viral replication, expression, and infection will not only contribute to the planning of effective antiviral therapies, but also provide new molecular targets for the development of antiviral drugs.
Literature
1.
go back to reference Van Damme E, Van Loock M. Functional annotation of human cytomegalovirus gene products: an update. Front Microbiol. 2014;5:218.PubMedPubMedCentral Van Damme E, Van Loock M. Functional annotation of human cytomegalovirus gene products: an update. Front Microbiol. 2014;5:218.PubMedPubMedCentral
2.
go back to reference Fattuoni C, Palmas F, Noto A, Barberini L, Mussap M, Grapov D, Dessi A, Casu M, Casanova A, Furione M, et al. Primary HCMV infection in pregnancy from classic data towards metabolomics: An exploratory analysis. Clin Chim Acta. 2016;460:23–32.PubMedCrossRef Fattuoni C, Palmas F, Noto A, Barberini L, Mussap M, Grapov D, Dessi A, Casu M, Casanova A, Furione M, et al. Primary HCMV infection in pregnancy from classic data towards metabolomics: An exploratory analysis. Clin Chim Acta. 2016;460:23–32.PubMedCrossRef
3.
go back to reference Griffiths P, Baraniak I, Reeves M. The pathogenesis of human cytomegalovirus. J Pathol. 2015;235:288–97.PubMedCrossRef Griffiths P, Baraniak I, Reeves M. The pathogenesis of human cytomegalovirus. J Pathol. 2015;235:288–97.PubMedCrossRef
4.
go back to reference Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.PubMedCrossRef Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.PubMedCrossRef
5.
go back to reference Kozomara A, Birgaoanu M. Griffiths-Jones S: miRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47:D155–62.PubMedCrossRef Kozomara A, Birgaoanu M. Griffiths-Jones S: miRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47:D155–62.PubMedCrossRef
7.
go back to reference Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294:853–8.PubMedCrossRef Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294:853–8.PubMedCrossRef
9.
go back to reference Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, et al. Identification of microRNAs of the herpesvirus family. Nat Methods. 2005;2:269–76.PubMedCrossRef Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, et al. Identification of microRNAs of the herpesvirus family. Nat Methods. 2005;2:269–76.PubMedCrossRef
10.
go back to reference Fruci D, Rota R, Gallo A. The Role of HCMV and HIV-1 MicroRNAs: Processing, and Mechanisms of Action during Viral Infection. Front Microbiol. 2017;8:689.PubMedPubMedCentralCrossRef Fruci D, Rota R, Gallo A. The Role of HCMV and HIV-1 MicroRNAs: Processing, and Mechanisms of Action during Viral Infection. Front Microbiol. 2017;8:689.PubMedPubMedCentralCrossRef
11.
go back to reference Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. Identification of virus-encoded microRNAs. Science. 2004;304:734–6.PubMedCrossRef Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. Identification of virus-encoded microRNAs. Science. 2004;304:734–6.PubMedCrossRef
14.
go back to reference Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, Mandelboim O. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J Virol. 2009;83:10684–93.PubMedPubMedCentralCrossRef Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, Mandelboim O. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J Virol. 2009;83:10684–93.PubMedPubMedCentralCrossRef
15.
go back to reference Lee SH, Kalejta RF, Kerry J, Semmes OJ, O'Connor CM, Khan Z, Garcia BA, Shenk T, Murphy E. BclAF1 restriction factor is neutralized by proteasomal degradation and microRNA repression during human cytomegalovirus infection. Proc Natl Acad Sci U S A. 2012;109:9575–80.PubMedPubMedCentralCrossRef Lee SH, Kalejta RF, Kerry J, Semmes OJ, O'Connor CM, Khan Z, Garcia BA, Shenk T, Murphy E. BclAF1 restriction factor is neutralized by proteasomal degradation and microRNA repression during human cytomegalovirus infection. Proc Natl Acad Sci U S A. 2012;109:9575–80.PubMedPubMedCentralCrossRef
16.
go back to reference Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe. 2009;5:376–85.PubMedCrossRef Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe. 2009;5:376–85.PubMedCrossRef
17.
go back to reference Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, Horwitz E, Prokocimer Z, Prichard M, Hahn G, et al. Host immune system gene targeting by a viral miRNA. Science. 2007;317:376–81.PubMedPubMedCentralCrossRef Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, Horwitz E, Prokocimer Z, Prichard M, Hahn G, et al. Host immune system gene targeting by a viral miRNA. Science. 2007;317:376–81.PubMedPubMedCentralCrossRef
18.
go back to reference Grey F, Meyers H, White EA, Spector DH, Nelson J. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 2007;3:e163.PubMedPubMedCentralCrossRef Grey F, Meyers H, White EA, Spector DH, Nelson J. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 2007;3:e163.PubMedPubMedCentralCrossRef
20.
go back to reference Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, Ma X, Lau WB, Rong R, Yu X, et al. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011;124:175–84.PubMedCrossRef Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, Ma X, Lau WB, Rong R, Yu X, et al. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011;124:175–84.PubMedCrossRef
21.
go back to reference Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M, Landais I, Jeng S, McWeeney S, Britt W, Nelson JA. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe. 2014;15:363–73.PubMedPubMedCentralCrossRef Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M, Landais I, Jeng S, McWeeney S, Britt W, Nelson JA. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe. 2014;15:363–73.PubMedPubMedCentralCrossRef
22.
go back to reference Kim S, Seo D, Kim D, Hong Y, Chang H, Baek D, Kim VN, Lee S, Ahn K. Temporal Landscape of MicroRNA-Mediated Host-Virus Crosstalk during Productive Human Cytomegalovirus Infection. Cell Host Microbe. 2015;17:838–51.PubMedCrossRef Kim S, Seo D, Kim D, Hong Y, Chang H, Baek D, Kim VN, Lee S, Ahn K. Temporal Landscape of MicroRNA-Mediated Host-Virus Crosstalk during Productive Human Cytomegalovirus Infection. Cell Host Microbe. 2015;17:838–51.PubMedCrossRef
23.
go back to reference Hancock MH, Hook LM, Mitchell J, Nelson JA. Human Cytomegalovirus MicroRNAs miR-US5-1 and miR-UL112-3p Block Proinflammatory Cytokine Production in Response to NF-kappaB-Activating Factors through Direct Downregulation of IKKalpha and IKKbeta. mBio. 2017;8. Hancock MH, Hook LM, Mitchell J, Nelson JA. Human Cytomegalovirus MicroRNAs miR-US5-1 and miR-UL112-3p Block Proinflammatory Cytokine Production in Response to NF-kappaB-Activating Factors through Direct Downregulation of IKKalpha and IKKbeta. mBio. 2017;8.
24.
go back to reference Huang Y, Qi Y, Ma Y, He R, Ji Y, Sun Z, Ruan Q. Down-regulation of human cytomegalovirus UL138, a novel latency-associated determinant, by hcmv-miR-UL36. J Biosci. 2013;38:479–85.PubMedCrossRef Huang Y, Qi Y, Ma Y, He R, Ji Y, Sun Z, Ruan Q. Down-regulation of human cytomegalovirus UL138, a novel latency-associated determinant, by hcmv-miR-UL36. J Biosci. 2013;38:479–85.PubMedCrossRef
25.
go back to reference Landais I, Pelton C, Streblow D, DeFilippis V, McWeeney S, Nelson JA. Human Cytomegalovirus miR-UL112-3p Targets TLR2 and Modulates the TLR2/IRAK1/NFkappaB Signaling Pathway. PLoS Pathog. 2015;11:e1004881.PubMedPubMedCentralCrossRef Landais I, Pelton C, Streblow D, DeFilippis V, McWeeney S, Nelson JA. Human Cytomegalovirus miR-UL112-3p Targets TLR2 and Modulates the TLR2/IRAK1/NFkappaB Signaling Pathway. PLoS Pathog. 2015;11:e1004881.PubMedPubMedCentralCrossRef
26.
go back to reference Romania P, Cifaldi L, Pignoloni B, Starc N, D'Alicandro V, Melaiu O, Li Pira G, Giorda E, Carrozzo R, Bergvall M, et al. Identification of a Genetic Variation in ERAP1 Aminopeptidase that Prevents Human Cytomegalovirus miR-UL112-5p-Mediated Immunoevasion. Cell Rep. 2017;20:846–53.PubMedCrossRef Romania P, Cifaldi L, Pignoloni B, Starc N, D'Alicandro V, Melaiu O, Li Pira G, Giorda E, Carrozzo R, Bergvall M, et al. Identification of a Genetic Variation in ERAP1 Aminopeptidase that Prevents Human Cytomegalovirus miR-UL112-5p-Mediated Immunoevasion. Cell Rep. 2017;20:846–53.PubMedCrossRef
27.
go back to reference Kim Y, Lee S, Kim S, Kim D, Ahn JH, Ahn K. Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog. 2012;8:e1002577.PubMedPubMedCentralCrossRef Kim Y, Lee S, Kim S, Kim D, Ahn JH, Ahn K. Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog. 2012;8:e1002577.PubMedPubMedCentralCrossRef
28.
go back to reference Wang YP, Qi Y, Huang YJ, Qi ML, Ma YP, He R, Ji YH, Sun ZR, Ruan Q. Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int J Mol Med. 2013;31:959–66.PubMedCrossRef Wang YP, Qi Y, Huang YJ, Qi ML, Ma YP, He R, Ji YH, Sun ZR, Ruan Q. Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int J Mol Med. 2013;31:959–66.PubMedCrossRef
29.
go back to reference Babu SG, Pandeya A, Verma N, Shukla N, Kumar RV, Saxena S. Role of HCMV miR-UL70-3p and miR-UL148D in overcoming the cellular apoptosis. Mol Cell Biochem. 2014;393:89–98.PubMedCrossRef Babu SG, Pandeya A, Verma N, Shukla N, Kumar RV, Saxena S. Role of HCMV miR-UL70-3p and miR-UL148D in overcoming the cellular apoptosis. Mol Cell Biochem. 2014;393:89–98.PubMedCrossRef
30.
go back to reference Lau B, Poole E, Krishna B, Sellart I, Wills MR, Murphy E, Sinclair J. The Expression of Human Cytomegalovirus MicroRNA MiR-UL148D during Latent Infection in Primary Myeloid Cells Inhibits Activin A-triggered Secretion of IL-6. Sci Rep. 2016;6:31205.PubMedPubMedCentralCrossRef Lau B, Poole E, Krishna B, Sellart I, Wills MR, Murphy E, Sinclair J. The Expression of Human Cytomegalovirus MicroRNA MiR-UL148D during Latent Infection in Primary Myeloid Cells Inhibits Activin A-triggered Secretion of IL-6. Sci Rep. 2016;6:31205.PubMedPubMedCentralCrossRef
31.
go back to reference Hancock MH, Crawford LB, Pham AH, Mitchell J, Struthers HM, Yurochko AD, Caposio P, Nelson JA. Human Cytomegalovirus miRNAs Regulate TGF-beta to Mediate Myelosuppression while Maintaining Viral Latency in CD34(+) Hematopoietic Progenitor Cells. Cell Host Microbe. 2020;27:104–114.e104.PubMedCrossRef Hancock MH, Crawford LB, Pham AH, Mitchell J, Struthers HM, Yurochko AD, Caposio P, Nelson JA. Human Cytomegalovirus miRNAs Regulate TGF-beta to Mediate Myelosuppression while Maintaining Viral Latency in CD34(+) Hematopoietic Progenitor Cells. Cell Host Microbe. 2020;27:104–114.e104.PubMedCrossRef
32.
go back to reference Lisboa LF, Egli A, O'Shea D, Asberg A, Hartmann A, Rollag H, Pang XL, Tyrrell DL, Kumar D, Humar A. Hcmv-miR-UL22A-5p: A Biomarker in Transplantation With Broad Impact on Host Gene Expression and Potential Immunological Implications. Am J Transplant. 2015;15:1893–902.PubMedCrossRef Lisboa LF, Egli A, O'Shea D, Asberg A, Hartmann A, Rollag H, Pang XL, Tyrrell DL, Kumar D, Humar A. Hcmv-miR-UL22A-5p: A Biomarker in Transplantation With Broad Impact on Host Gene Expression and Potential Immunological Implications. Am J Transplant. 2015;15:1893–902.PubMedCrossRef
33.
go back to reference Petrucelli A, Rak M, Grainger L, Goodrum F. Characterization of a novel Golgi apparatus-localized latency determinant encoded by human cytomegalovirus. J Virol. 2009;83:5615–29.PubMedPubMedCentralCrossRef Petrucelli A, Rak M, Grainger L, Goodrum F. Characterization of a novel Golgi apparatus-localized latency determinant encoded by human cytomegalovirus. J Virol. 2009;83:5615–29.PubMedPubMedCentralCrossRef
34.
go back to reference Guo X, Huang Y, Qi Y, Liu Z, Ma Y, Shao Y, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-UL36-5p inhibits apoptosis via downregulation of adenine nucleotide translocator 3 in cultured cells. Arch Virol. 2015;160:2483–90.PubMedCrossRef Guo X, Huang Y, Qi Y, Liu Z, Ma Y, Shao Y, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-UL36-5p inhibits apoptosis via downregulation of adenine nucleotide translocator 3 in cultured cells. Arch Virol. 2015;160:2483–90.PubMedCrossRef
35.
go back to reference Ding M, Wang X, Wang C, Liu X, Zen K, Wang W, Zhang CY, Zhang C. Distinct expression profile of HCMV encoded miRNAs in plasma from oral lichen planus patients. J Transl Med. 2017;15:133.PubMedPubMedCentralCrossRef Ding M, Wang X, Wang C, Liu X, Zen K, Wang W, Zhang CY, Zhang C. Distinct expression profile of HCMV encoded miRNAs in plasma from oral lichen planus patients. J Transl Med. 2017;15:133.PubMedPubMedCentralCrossRef
36.
go back to reference Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 2011;12:984–91.PubMedPubMedCentralCrossRef Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 2011;12:984–91.PubMedPubMedCentralCrossRef
37.
go back to reference Shao Y, Qi Y, Huang Y, Liu Z, Ma Y, Guo X, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-US4-5p promotes apoptosis via downregulation of p21-activated kinase 2 in cultured cells. Mol Med Rep. 2017;16:4171–8.PubMedCrossRef Shao Y, Qi Y, Huang Y, Liu Z, Ma Y, Guo X, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-US4-5p promotes apoptosis via downregulation of p21-activated kinase 2 in cultured cells. Mol Med Rep. 2017;16:4171–8.PubMedCrossRef
38.
go back to reference Tirabassi R, Hook L, Landais I, Grey F, Meyers H, Hewitt H, Nelson J. Human cytomegalovirus US7 is regulated synergistically by two virally encoded microRNAs and by two distinct mechanisms. J Virol. 2011;85:11938–44.PubMedPubMedCentralCrossRef Tirabassi R, Hook L, Landais I, Grey F, Meyers H, Hewitt H, Nelson J. Human cytomegalovirus US7 is regulated synergistically by two virally encoded microRNAs and by two distinct mechanisms. J Virol. 2011;85:11938–44.PubMedPubMedCentralCrossRef
39.
go back to reference Jiang S, Huang Y, Qi Y, He R, Liu Z, Ma Y, Guo X, Shao Y, Sun Z, Ruan Q. Human cytomegalovirus miR-US5-1 inhibits viral replication by targeting Geminin mRNA. Virol Sin. 2017;32:431–9.PubMedPubMedCentralCrossRef Jiang S, Huang Y, Qi Y, He R, Liu Z, Ma Y, Guo X, Shao Y, Sun Z, Ruan Q. Human cytomegalovirus miR-US5-1 inhibits viral replication by targeting Geminin mRNA. Virol Sin. 2017;32:431–9.PubMedPubMedCentralCrossRef
40.
go back to reference Stark TJ, Arnold JD, Spector DH, Yeo GW. High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol. 2012;86:226–35.PubMedPubMedCentralCrossRef Stark TJ, Arnold JD, Spector DH, Yeo GW. High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol. 2012;86:226–35.PubMedPubMedCentralCrossRef
41.
go back to reference Mikell I, Crawford LB, Hancock MH, Mitchell J, Buehler J, Goodrum F, Nelson JA. HCMV miR-US22 down-regulation of EGR-1 regulates CD34+ hematopoietic progenitor cell proliferation and viral reactivation. PLoS Pathog. 2019;15:e1007854.PubMedPubMedCentralCrossRef Mikell I, Crawford LB, Hancock MH, Mitchell J, Buehler J, Goodrum F, Nelson JA. HCMV miR-US22 down-regulation of EGR-1 regulates CD34+ hematopoietic progenitor cell proliferation and viral reactivation. PLoS Pathog. 2019;15:e1007854.PubMedPubMedCentralCrossRef
42.
go back to reference Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog. 2010;6:e1000967.PubMedPubMedCentralCrossRef Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog. 2010;6:e1000967.PubMedPubMedCentralCrossRef
43.
go back to reference Qi M, Qi Y, Ma Y, He R, Ji Y, Sun Z, Ruan Q. Over-expression of human cytomegalovirus miR-US25-2-3p downregulates eIF4A1 and inhibits HCMV replication. FEBS Lett. 2013;587:2266–71.PubMedCrossRef Qi M, Qi Y, Ma Y, He R, Ji Y, Sun Z, Ruan Q. Over-expression of human cytomegalovirus miR-US25-2-3p downregulates eIF4A1 and inhibits HCMV replication. FEBS Lett. 2013;587:2266–71.PubMedCrossRef
44.
go back to reference Shen ZZ, Pan X, Miao LF, Ye HQ, Chavanas S, Davrinche C, McVoy M, Luo MH. Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One. 2014;9:e88531.PubMedPubMedCentralCrossRef Shen ZZ, Pan X, Miao LF, Ye HQ, Chavanas S, Davrinche C, McVoy M, Luo MH. Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One. 2014;9:e88531.PubMedPubMedCentralCrossRef
45.
go back to reference Guo X, Qi Y, Huang Y, Liu Z, Ma Y, Shao Y, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-US33-5p inhibits viral DNA synthesis and viral replication by down-regulating expression of the host Syntaxin3. FEBS Lett. 2015;589:440–6.PubMedCrossRef Guo X, Qi Y, Huang Y, Liu Z, Ma Y, Shao Y, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus miR-US33-5p inhibits viral DNA synthesis and viral replication by down-regulating expression of the host Syntaxin3. FEBS Lett. 2015;589:440–6.PubMedCrossRef
46.
go back to reference Mendelson M, Monard S, Sissons P, Sinclair J. Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol. 1996;77(Pt 12):3099–102.PubMedCrossRef Mendelson M, Monard S, Sissons P, Sinclair J. Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol. 1996;77(Pt 12):3099–102.PubMedCrossRef
47.
go back to reference Li G, Kamil JP. Viral Regulation of Cell Tropism in Human Cytomegalovirus. J Virol. 2016;90:626–9.PubMedCrossRef Li G, Kamil JP. Viral Regulation of Cell Tropism in Human Cytomegalovirus. J Virol. 2016;90:626–9.PubMedCrossRef
48.
go back to reference Meshesha MK, Bentwich Z, Solomon SA, Avni YS. In vivo expression of human cytomegalovirus (HCMV) microRNAs during latency. Gene. 2016;575:101–7.PubMedCrossRef Meshesha MK, Bentwich Z, Solomon SA, Avni YS. In vivo expression of human cytomegalovirus (HCMV) microRNAs during latency. Gene. 2016;575:101–7.PubMedCrossRef
49.
go back to reference Pan C, Zhu D, Wang Y, Li L, Li D, Liu F, Zhang CY, Zen K. Human Cytomegalovirus miR-UL148D Facilitates Latent Viral Infection by Targeting Host Cell Immediate Early Response Gene 5. PLoS Pathog. 2016;12:e1006007.PubMedPubMedCentralCrossRef Pan C, Zhu D, Wang Y, Li L, Li D, Liu F, Zhang CY, Zen K. Human Cytomegalovirus miR-UL148D Facilitates Latent Viral Infection by Targeting Host Cell Immediate Early Response Gene 5. PLoS Pathog. 2016;12:e1006007.PubMedPubMedCentralCrossRef
51.
go back to reference Iwuchukwu OC, Harvey JR, Dordea M, Critchley AC, Drew PJ. The role of oncoplastic therapeutic mammoplasty in breast cancer surgery--a review. Surg Oncol. 2012;21:133–41.PubMedCrossRef Iwuchukwu OC, Harvey JR, Dordea M, Critchley AC, Drew PJ. The role of oncoplastic therapeutic mammoplasty in breast cancer surgery--a review. Surg Oncol. 2012;21:133–41.PubMedCrossRef
52.
go back to reference Chen J, Xia S, Yang X, Chen H, Li F, Liu F, Chen Z. Human Cytomegalovirus Encoded miR-US25-1-5p Attenuates CD147/EMMPRIN-Mediated Early Antiviral Response. Viruses. 2017;9. Chen J, Xia S, Yang X, Chen H, Li F, Liu F, Chen Z. Human Cytomegalovirus Encoded miR-US25-1-5p Attenuates CD147/EMMPRIN-Mediated Early Antiviral Response. Viruses. 2017;9.
53.
go back to reference Fu M, Gao Y, Zhou Q, Zhang Q, Peng Y, Tian K, Wang J, Zheng X. Human cytomegalovirus latent infection alters the expression of cellular and viral microRNA. Gene. 2014;536:272–8.PubMedCrossRef Fu M, Gao Y, Zhou Q, Zhang Q, Peng Y, Tian K, Wang J, Zheng X. Human cytomegalovirus latent infection alters the expression of cellular and viral microRNA. Gene. 2014;536:272–8.PubMedCrossRef
55.
go back to reference Dunn W, Trang P, Zhong Q, Yang E, van Belle C, Liu F. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell Microbiol. 2005;7:1684–95.PubMedCrossRef Dunn W, Trang P, Zhong Q, Yang E, van Belle C, Liu F. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell Microbiol. 2005;7:1684–95.PubMedCrossRef
56.
go back to reference Meshesha MK, Veksler-Lublinsky I, Isakov O, Reichenstein I, Shomron N, Kedem K, Ziv-Ukelson M, Bentwich Z, Avni YS. The microRNA Transcriptome of Human Cytomegalovirus (HCMV). Open Virol J. 2012;6:38–48.PubMedPubMedCentralCrossRef Meshesha MK, Veksler-Lublinsky I, Isakov O, Reichenstein I, Shomron N, Kedem K, Ziv-Ukelson M, Bentwich Z, Avni YS. The microRNA Transcriptome of Human Cytomegalovirus (HCMV). Open Virol J. 2012;6:38–48.PubMedPubMedCentralCrossRef
57.
go back to reference Hancock MH, Tirabassi RS, Nelson JA. Rhesus cytomegalovirus encodes seventeen microRNAs that are differentially expressed in vitro and in vivo. Virology. 2012;425:133–42.PubMedCrossRef Hancock MH, Tirabassi RS, Nelson JA. Rhesus cytomegalovirus encodes seventeen microRNAs that are differentially expressed in vitro and in vivo. Virology. 2012;425:133–42.PubMedCrossRef
58.
go back to reference Buck AH, Santoyo-Lopez J, Robertson KA, Kumar DS, Reczko M, Ghazal P. Discrete clusters of virus-encoded micrornas are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J Virol. 2007;81:13761–70.PubMedPubMedCentralCrossRef Buck AH, Santoyo-Lopez J, Robertson KA, Kumar DS, Reczko M, Ghazal P. Discrete clusters of virus-encoded micrornas are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J Virol. 2007;81:13761–70.PubMedPubMedCentralCrossRef
59.
go back to reference Grey F, Antoniewicz A, Allen E, Saugstad J, McShea A, Carrington JC, Nelson J. Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol. 2005;79:12095–9.PubMedPubMedCentralCrossRef Grey F, Antoniewicz A, Allen E, Saugstad J, McShea A, Carrington JC, Nelson J. Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol. 2005;79:12095–9.PubMedPubMedCentralCrossRef
60.
go back to reference Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, Mandelboim M, Mandelboim O. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol. 2008;9:1065–73.PubMedCrossRef Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, Mandelboim M, Mandelboim O. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol. 2008;9:1065–73.PubMedCrossRef
61.
go back to reference Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806–13.PubMedCrossRef Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806–13.PubMedCrossRef
62.
go back to reference Yu LP, Shi LY, Zhang MM, Wang SY, Cai J, Gao MM, Xiong W. Yang XC: [MicroRNA expression profile and pathogenetic initial study in essential hypertension]. Zhonghua Xin Xue Guan Bing Za Zhi. 2011;39:488–93.PubMed Yu LP, Shi LY, Zhang MM, Wang SY, Cai J, Gao MM, Xiong W. Yang XC: [MicroRNA expression profile and pathogenetic initial study in essential hypertension]. Zhonghua Xin Xue Guan Bing Za Zhi. 2011;39:488–93.PubMed
63.
go back to reference Huang Y, Chen D, He J, Cai J, Shen K, Liu X, Yang X, Xu L. Hcmv-miR-UL112 attenuates NK cell activity by inhibition type I interferon secretion. Immunol Lett. 2015;163:151–6.PubMedCrossRef Huang Y, Chen D, He J, Cai J, Shen K, Liu X, Yang X, Xu L. Hcmv-miR-UL112 attenuates NK cell activity by inhibition type I interferon secretion. Immunol Lett. 2015;163:151–6.PubMedCrossRef
64.
go back to reference Shen K, Xu L, Chen D, Tang W, Huang Y. Human cytomegalovirus-encoded miR-UL112 contributes to HCMV-mediated vascular diseases by inducing vascular endothelial cell dysfunction. Virus Genes. 2018;54:172–81.PubMedCrossRef Shen K, Xu L, Chen D, Tang W, Huang Y. Human cytomegalovirus-encoded miR-UL112 contributes to HCMV-mediated vascular diseases by inducing vascular endothelial cell dysfunction. Virus Genes. 2018;54:172–81.PubMedCrossRef
65.
go back to reference Murphy E, Vanicek J, Robins H, Shenk T, Levine AJ. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A. 2008;105:5453–8.PubMedPubMedCentralCrossRef Murphy E, Vanicek J, Robins H, Shenk T, Levine AJ. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A. 2008;105:5453–8.PubMedPubMedCentralCrossRef
66.
go back to reference Lau B, Poole E, Van Damme E, Bunkens L, Sowash M, King H, Murphy E, Wills M, Van Loock M, Sinclair J. Human cytomegalovirus miR-UL112-1 promotes the down-regulation of viral immediate early-gene expression during latency to prevent T-cell recognition of latently infected cells. J Gen Virol. 2016;97:2387–98.PubMedPubMedCentralCrossRef Lau B, Poole E, Van Damme E, Bunkens L, Sowash M, King H, Murphy E, Wills M, Van Loock M, Sinclair J. Human cytomegalovirus miR-UL112-1 promotes the down-regulation of viral immediate early-gene expression during latency to prevent T-cell recognition of latently infected cells. J Gen Virol. 2016;97:2387–98.PubMedPubMedCentralCrossRef
67.
go back to reference Donlon TA, Krensky AM, Wallace MR, Collins FS, Lovett M, Clayberger C. Localization of a human T-cell-specific gene, RANTES (D17S136E), to chromosome 17q11.2-q12. Genomics. 1990;6:548–53.PubMedCrossRef Donlon TA, Krensky AM, Wallace MR, Collins FS, Lovett M, Clayberger C. Localization of a human T-cell-specific gene, RANTES (D17S136E), to chromosome 17q11.2-q12. Genomics. 1990;6:548–53.PubMedCrossRef
68.
go back to reference Maghazachi AA, Al-Aoukaty A, Schall TJ. CC chemokines induce the generation of killer cells from CD56+ cells. Eur J Immunol. 1996;26:315–9.PubMedCrossRef Maghazachi AA, Al-Aoukaty A, Schall TJ. CC chemokines induce the generation of killer cells from CD56+ cells. Eur J Immunol. 1996;26:315–9.PubMedCrossRef
69.
go back to reference Goodrum F, Reeves M, Sinclair J, High K, Shenk T. Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro. Blood. 2007;110:937–45.PubMedPubMedCentralCrossRef Goodrum F, Reeves M, Sinclair J, High K, Shenk T. Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro. Blood. 2007;110:937–45.PubMedPubMedCentralCrossRef
70.
go back to reference Naqvi AR, Shango J, Seal A, Shukla D, Nares S. Viral miRNAs Alter Host Cell miRNA Profiles and Modulate Innate Immune Responses. Front Immunol. 2018;9:433.PubMedPubMedCentralCrossRef Naqvi AR, Shango J, Seal A, Shukla D, Nares S. Viral miRNAs Alter Host Cell miRNA Profiles and Modulate Innate Immune Responses. Front Immunol. 2018;9:433.PubMedPubMedCentralCrossRef
71.
go back to reference Mohammad AA, Costa H, Landazuri N, Lui WO, Hultenby K, Rahbar A, Yaiw KC, Soderberg-Naucler C. Human cytomegalovirus microRNAs are carried by virions and dense bodies and are delivered to target cells. J Gen Virol. 2017;98:1058–72.PubMedPubMedCentralCrossRef Mohammad AA, Costa H, Landazuri N, Lui WO, Hultenby K, Rahbar A, Yaiw KC, Soderberg-Naucler C. Human cytomegalovirus microRNAs are carried by virions and dense bodies and are delivered to target cells. J Gen Virol. 2017;98:1058–72.PubMedPubMedCentralCrossRef
72.
go back to reference Shao Y, Qi Y, Huang Y, Liu Z, Ma Y, Guo X, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus-encoded miR-US4-1 promotes cell apoptosis and benefits discharge of infectious virus particles by targeting QARS. J Biosci. 2016;41:183–92.PubMedCrossRef Shao Y, Qi Y, Huang Y, Liu Z, Ma Y, Guo X, Jiang S, Sun Z, Ruan Q. Human cytomegalovirus-encoded miR-US4-1 promotes cell apoptosis and benefits discharge of infectious virus particles by targeting QARS. J Biosci. 2016;41:183–92.PubMedCrossRef
73.
go back to reference Caputo TM, Cummaro A, Lettera V, Mazzarotta A, Battista E, Netti PA, Causa F. One-step scalable fluorescent microgel bioassay for the ultrasensitive detection of endogenous viral miR-US4-5p. Analyst. 2019;144:1369–78.PubMedCrossRef Caputo TM, Cummaro A, Lettera V, Mazzarotta A, Battista E, Netti PA, Causa F. One-step scalable fluorescent microgel bioassay for the ultrasensitive detection of endogenous viral miR-US4-5p. Analyst. 2019;144:1369–78.PubMedCrossRef
74.
go back to reference Bokoch GM. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction? Cell Death Differ. 1998;5:637–45.PubMedCrossRef Bokoch GM. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction? Cell Death Differ. 1998;5:637–45.PubMedCrossRef
75.
go back to reference Yurochko AD. New Mechanism by Which Human Cytomegalovirus MicroRNAs Negate the Proinflammatory Response to Infection. mBio. 2017;8. Yurochko AD. New Mechanism by Which Human Cytomegalovirus MicroRNAs Negate the Proinflammatory Response to Infection. mBio. 2017;8.
76.
go back to reference Liu Y, Pan J, Liu L, Li W, Tao R, Chen Y, Li H, Shang S. The influence of HCMV infection on autophagy in THP-1 cells. Medicine (Baltimore). 2017;96:e8298.CrossRef Liu Y, Pan J, Liu L, Li W, Tao R, Chen Y, Li H, Shang S. The influence of HCMV infection on autophagy in THP-1 cells. Medicine (Baltimore). 2017;96:e8298.CrossRef
77.
go back to reference Buehler J, Carpenter E, Zeltzer S, Igarashi S, Rak M, Mikell I, Nelson JA, Goodrum F. Host signaling and EGR1 transcriptional control of human cytomegalovirus replication and latency. PLoS Pathog. 2019;15:e1008037.PubMedPubMedCentralCrossRef Buehler J, Carpenter E, Zeltzer S, Igarashi S, Rak M, Mikell I, Nelson JA, Goodrum F. Host signaling and EGR1 transcriptional control of human cytomegalovirus replication and latency. PLoS Pathog. 2019;15:e1008037.PubMedPubMedCentralCrossRef
78.
go back to reference Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.PubMedPubMedCentralCrossRef Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.PubMedPubMedCentralCrossRef
79.
go back to reference Fan J, Zhang W, Liu Q. Human cytomegalovirus-encoded miR-US25-1 aggravates the oxidised low density lipoprotein-induced apoptosis of endothelial cells. Biomed Res Int. 2014;2014:531979.PubMedPubMedCentral Fan J, Zhang W, Liu Q. Human cytomegalovirus-encoded miR-US25-1 aggravates the oxidised low density lipoprotein-induced apoptosis of endothelial cells. Biomed Res Int. 2014;2014:531979.PubMedPubMedCentral
80.
go back to reference Zhang Z, Kang Y, Zhang Z, Zhang H, Duan X, Liu J, Li X, Liao W. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells. Osteoarthritis Cartilage. 2012;20:1638–46.PubMedCrossRef Zhang Z, Kang Y, Zhang Z, Zhang H, Duan X, Liu J, Li X, Liao W. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells. Osteoarthritis Cartilage. 2012;20:1638–46.PubMedCrossRef
81.
go back to reference Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438:685–9.PubMedCrossRef Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438:685–9.PubMedCrossRef
Metadata
Title
MicroRNAs expressed by human cytomegalovirus
Authors
Lichen Zhang
Jiaqi Yu
Zhijun Liu
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2020
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-020-1296-4

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