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Critical Reviews™ in Eukaryotic Gene Expression
インパクトファクター: 2.156 5年インパクトファクター: 2.255 SJR: 0.649 SNIP: 0.599 CiteScore™: 3

ISSN 印刷: 1045-4403
ISSN オンライン: 2162-6502

Critical Reviews™ in Eukaryotic Gene Expression

DOI: 10.1615/CritRevEukaryotGeneExpr.2020034571
pages 337-348

Role of MicroRNAs in Establishing Latency of Human Immunodeficiency Virus

Muhammad Munam Mustafa Bukhari
Division of Molecular Virology, National Centre of Excellence in Molecular Biology (CEMB), University of the Punjab, Lahore, Pakistan
Iqra Mir
Division of Molecular Virology, National Centre of Excellence in Molecular Biology (CEMB), University of the Punjab, Lahore, Pakistan
Muhammad Idrees
Division of Molecular Virology and Infectious Diseases, Centre of Excellence in Molecular Biology (CEMB), University of the Punjab, Lahore-Pakistan; Hazara University, Khyber Pakhtunkhwa, Pakistan
Samia Afzal
Division of Molecular Virology & Molecular Diagnostics, National Centre of Excellence in Molecular Biology (CEMB), University of the Punjab, Lahore, Pakistan
Muhammad Shahid
Division of Molecular Virology, National Centre of Excellence in Molecular Biology (CEMB), University of the Punjab, Lahore, Pakistan

要約

Acquired immunodeficiency syndrome (AIDS) emerged as an epidemic in Africa in 1981, and now it has become a most destructive global pandemic. Human immunodeficiency virus (HIV) is responsible for the pathogenesis of AIDS, and it is usually transmitted through unsafe sexual activities. HIV is a lentivirus that can remain latent in the host cells for a long period, and it has various mechanisms to establish latency. The HIV genome encodes several microRNAs (miRNA-TAR, miRNA-H1, miRNA-H3, and miRNA-Nef-367) that act as posttranscriptional control by targeting mRNA sequences. The miRNA-TAR, miRNA-Nef-367, and miRNA-H1 have established roles in HIV latency, whereas miRNA-H3 can activate the latent reservoirs of HIV. The human genome also encodes several miRNAs that have defensive roles against infections. Cellular miRNAs (miRNA-29a, miRNA-146a, miRNA-34c-5'p, miRNA-186, miRNA-210 and miRNA-222) also contribute to viral latency. The most challenging hurdle in the development of effective HIV therapeutics is viral latency. A complete understanding of latency will enable us to develop efficient therapeutics and to eradicate HIV from the globe.

参考

  1. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W, Montagnier L. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983;220(4599):868-71. PubMed PMID: 6189183. Epub 1983/05/20.eng.

  2. Wain-Hobson S, Alizon M, Montagnier L. Relationship of AIDS to other retroviruses. Nature. 1985;313(6005):743. PubMed PMID: 2983221. Epub 1985/02/06.eng.

  3. Case K. Nomenclature: Human immunodeficiency virus. Ann Intern Med. 1986;105(1):133. PubMed PMID: 3013059. Epub 1986/07/01.eng.

  4. Siliciano RF, Greene WC. HIV latency. Cold Spring Harb Perspect Med. 2011;1(1):a007096. PubMed PMID: 22229121. PMCID: 3234450. Epub 2012/01/10.eng.

  5. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, Saksela K, Markowitz M, Ho DD. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature. 1997;387(6629):188-91. PubMed PMID: 9144290. Epub 1997/05/08.eng.

  6. Davey RT Jr, Bhat N, Yoder C, Chun TW, Metcalf JA, Dewar R, Natarajan V, Lempicki RA, Adelsberger JW, Miller KD, Kovacs JA, Polis MA, Walker RE, Falloon J, Masur H, Gee D, Baseler M, Dimitrov DS, Fauci AS, Lane HC. HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proc Natl Acad Sci U S A. 1999;96(26):15109-14. PubMed PMID: 10611346. PMCID: 24781. Epub 1999/12/28.eng.

  7. Chun TW, Davey RT Jr, Engel D, Lane HC, Fauci AS. Re-emergence of HIV after stopping therapy. Nature. 1999;401(6756):874-5. PubMed PMID: 10553903. Epub 1999/11/30.eng.

  8. Hill AL, Rosenbloom DI, Fu F, Nowak MA, Siliciano RF. Predicting the outcomes of treatment to eradicate the latent reservoir for HIV-1. Proc Natl Acad Sci U S A. 2014;111(37):13475-80. PubMed PMID: 25097264. PM-CID: 4169952. Epub 2014/08/07.eng.

  9. Chun TW, Finzi D, Margolick J, Chadwick K, Schwartz D, Siliciano RF. In vivo fate of HIV-1-infected T cells: Quantitative analysis of the transition to stable latency. Nat Med. 1995;1(12):1284-90. PubMed PMID: 7489410. Epub 1995/12/01.eng.

  10. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, Taylor H, Hermankova M, Chadwick K, Margolick J, Quinn TC, Kuo YH, Brookmeyer R, Zeiger MA, Barditch-Crovo P, Siliciano RF. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature. 1997;387(6629):183-8. PubMed PMID: 9144289. Epub 1997/05/08.eng.

  11. Huang Q, Chen L, Luo M, Lv H, Luo D, Li T, Huang S, Xie L, Teng Y, Liu Z, Luo F, Xiong H, Zeng Y, Hou W, Feng Y. HIV-1-induced miR-146a attenuates monocyte migration by targeting CCL5 in human primary macrophages. AIDS Res Hum Retroviruses. 2018;34(7):580-9. PubMed PMID: 29717615. Epub 2018/05/03.eng.

  12. Siliciano JD, Lai J, Callender M, Pitt E, Zhang H, Margolick JB, Gallant JE, Cofrancesco J Jr, Moore RD, Gange SJ, Siliciano RF. Stability of the latent reservoir for HIV-1 in patients receiving valproic acid. J Infect Dis. 2007;195(6):833-6. PubMed PMID: 17299713. Epub 2007/02/15.eng.

  13. Sengupta S, Siliciano RF. Targeting the latent reservoir for HIV-1. Immunity. 2018;48(5):872-95. PubMed PMID: 29768175. PMCID: 6196732. Epub 2018/05/17.eng.

  14. Zhang Y, Fan M, Geng G, Liu B, Huang Z, Luo H, Zhou J, Guo X, Cai W, Zhang H. A novel HIV-1-encoded microRNA enhances its viral replication by targeting the TATA box region. Retrovirology. 2014;11:23. PubMed PMID: 24620741. PMCID: 4007588. Epub 2014/03/14. eng.

  15. Brahic M, Stowring L, Ventura P, Haase AT. Gene expression in visna virus infection in sheep. Nature. 1981;292(5820):240-2. PubMed PMID: 6265786. Epub 1981/07/16.eng.

  16. Folks T, Powell DM, Lightfoote MM, Benn S, Martin MA, Fauci AS. Induction of HTLV-III/LAV from a non-virus-producing T-cell line: Implications for latency. Science. 1986;231(4738):600-2. PubMed PMID: 3003906. Epub 1986/02/07.eng.

  17. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, Meese E, Wain-Hobson S, Meyerhans A. Recombination: Multiply infected spleen cells in HIV patients. Nature. 2002;418(6894):144. PubMed PMID: 12110879. Epub 2002/07/12.eng.

  18. Emiliani S, Van Lint C, Fischle W, Paras P Jr, Ott M, Brady J, Verdin E. A point mutation in the HIV-1 Tat responsive element is associated with postintegration latency. Proc Natl Acad Sci US A. 1996;93(13):6377-81. PubMed PMID: 8692823. PMCID: 39030. Epub 1996/06/25.eng.

  19. Emiliani S, Fischle W, Ott M, Van Lint C, Amella CA, Verdin E. Mutations in the tat gene are responsible for human immunodeficiency virus type 1 postintegration latency in the U1 cell line. J Virol. 1998;72(2):1666-70. PubMed PMID: 9445075. PMCID: 124653. Epub 1998/01/28.eng.

  20. Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe. 2008;4(2):123-33. PubMed PMID: 18692772. PMCID: 4217705. Epub 2008/08/12.eng.

  21. Greger IH, Demarchi F, Giacca M, Proudfoot NJ. Transcriptional interference perturbs the binding of Sp1 to the HIV-1 promoter. Nucleic Acids Res. 1998;26(5):1294-301. PubMed PMID: 9469840. PMCID: 147389. Epub 1998/04/04.eng.

  22. Han Y, Lassen K, Monie D, Sedaghat AR, Shimoji S, Liu X, Pierson TC, Margolick JB, Siliciano RF, Siliciano JD. Resting CD4+ T cells from human immunodeficiency virus type 1 (HIV-1)-infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J Virol. 2004;78(12):6122-33. PubMed PMID: 15163705. PMCID: 416493. Epub 2004/05/28.eng.

  23. Jordan A, Defechereux P, Verdin E. The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J. 2001;20(7):1726-38. PubMed PMID: 11285236. PM-CID: 145503. Epub 2001/04/04.eng.

  24. Kauder SE, Bosque A, Lindqvist A, Planelles V, Verdin E. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog. 2009;5(6):e1000495. PubMed PMID: 19557157. PMCID: 2695767. Epub 2009/06/27. eng.

  25. Mbonye U, Karn J. Transcriptional control ofHIV latency: Cellular signaling pathways, epigenetics, happenstance and the hope for a cure. Virology. 2014;454-455:328-39. PubMed PMID: 24565118. PMCID: 4010583. Epub 2014/02/26.eng.

  26. Zhang Z, Klatt A, Gilmour DS, Henderson AJ. Negative elongation factor NELF represses human immunodeficiency virus transcription by pausing the RNA polymerase II complex. J Biol Chem. 2007;282(23):16981-8. PubMed PMID: 17442680. Epub 2007/04/20.eng.

  27. Jadlowsky JK, Wong JY, Graham AC, Dobrowolski C, Devor RL, Adams MD, Fujinaga K, Karn J. Negative elongation factor is required for the maintenance of proviral latency but does not induce promoter-proximal pausing of RNA polymerase II on the HIV long terminal repeat. Mol Cell Biol. 2014;34(11):1911-28. PubMed PMID: 24636995. PMCID: 4019061. Epub 2014/03/19.eng.

  28. Rice AP, Herrmann CH. Regulation of TAK/P-TEFb in CD4+ T lymphocytes and macrophages. Curr HIV Res. 2003;1(4):395-404. PubMed PMID: 15049426. Epub 2004/03/31.eng.

  29. Yang X, Gold MO, Tang DN, Lewis DE, Aguilar-Cordova E, Rice AP, Herrmann CH. TAK, an HIV Tat-associated kinase, is a member of the cyclin-dependent family of protein kinases and is induced by activation of peripheral blood lymphocytes and differentiation of promonocytic cell lines. Proc Natl Acad Sci U S A. 1997;94(23):12331-6. PubMed PMID: 9356449. PMCID: 24930. Epub 1997/11/14.eng.

  30. Bernier A, Sagan SM. The diverse roles of microRNAs at the host-virus interface. Viruses. 2018;10(8):440. PubMed PMID: 30126238. PMCID: 6116274. Epub 2018/08/22.eng.

  31. Lee RC, Feinbaum RL, Ambros V. The C. elegans heter-ochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75(5):843-54. PubMed PMID: 8252621. Epub 1993/12/03.eng.

  32. Kim VN. MicroRNA biogenesis: Coordinated cropping and dicing. Nat Rev Mol Cell Biol. 2005;6(5):376-85. PubMed PMID: 15852042. Epub 2005/04/27.eng.

  33. Zamore PD, Haley B. Ribo-gnome: The big world of small RNAs. Science. 2005;309(5740):1519-24. PubMed PMID: 16141061. Epub 2005/09/06.eng.

  34. 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(3):363-73. PubMed PMID: 24629342. PMCID: 4029511. Epub 2014/03/19.eng.

  35. Eisenberg I, Eran A, Nishino I, Moggio M, Lamperti C, Amato AA, Lidov HG, Kang PB, North KN, Mitrani-Rosenbaum S, Flanigan KM, Neely LA, Whitney D, Beggs AH, Kohane IS, Kunkel LM. Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A. 2007;104(43):17016-21. PubMed PMID: 17942673. PMCID: 2040449. Epub 2007/10/19. eng.

  36. Kloosterman WP, Plasterk RHA. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006;11(4):441-50. PubMed PMID: 17011485. Epub 2006/10/03.eng.

  37. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834-8. PubMed PMID: 15944708. Epub 2005/06/10.eng.

  38. Wang X, Ye L, Hou W, Zhou Y, Wang YJ, Metzger DS, Ho WZ. Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood. 2009;113(3):671-4. PubMed PMID: 19015395. PMCID: 2628373. Epub 2008/11/19.eng.

  39. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: MicroRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009;11(3):228-34. PubMed PMID: 19255566. Epub 2009/03/04.eng.

  40. Feng Y, Zhang X, Song Q, Li T, Zeng Y. Drosha processing controls the specificity and efficiency of global microRNA expression. Biochim Biophys Acta. 2011;1809(11-12):700-7. PubMed PMID: 21683814. PMCID: 3210421. Epub 2011/06/21.eng.

  41. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17(24):3011-6. PubMed PMID: 14681208. PMCID: 305252. Epub 2003/12/19.eng.

  42. Feng Y, Zhang X, Graves P, Zeng Y. A comprehensive analysis of precursor microRNA cleavage by human Dicer. RNA. 2012;18(11):2083-92. PubMed PMID: 22984192. PMCID: 3479397. Epub 2012/09/18.eng.

  43. Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G. miRNPs: A novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 2002;16(6):720-8. PubMed PMID: 11914277.eng.

  44. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97. PubMed PMID: 14744438. Epub 2004/01/28.eng.

  45. Klase Z, Kale P, Winograd R, Gupta MV, Heydarian M, Berro R, McCaffrey T, Kashanchi F. HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol Biol. 2007;8:63. PubMed PMID: 17663774. PMCID: 1955452. Epub 2007/08/01.eng.

  46. Ouellet DL, Plante I, Landry P, Barat C, Janelle ME, Flamand L, Tremblay MJ, Provost P. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res. 2008;36(7):2353-65. PubMed PMID: 18299284. PM-CID: 2367715. Epub 2008/02/27.eng.

  47. Klase Z, Winograd R, Davis J, Carpio L, Hildreth R, Heydarian M, Fu S, McCaffrey T, Meiri E, Ayash-Rashkovsky M, Gilad S, Bentwich Z, Kashanchi F. HIV-1 TAR miRNA protects against apoptosis by altering cellular gene expression. Retrovirology. 2009;6:18. PubMed PMID: 19220914. PMCID: 2654423. Epub 2009/02/18.eng.

  48. Omoto S, Ito M, Tsutsumi Y, Ichikawa Y, Okuyama H, Brisibe EA, Saksena NK, Fujii YR. HIV-1 nef suppression by virally encoded microRNA. Retrovirology. 2004;1:44. PubMed PMID: 15601474. PMCID: 544868. Epub 2004/12/17.eng.

  49. Zhou Y, Sun L, Wang X, Liang H, Ye L, Zhou L, Liang BY, Li JL, Liu MQ, Peng JS, Zhou DJ, Gui XE, Ho WZ. Short communication: HIV-1 infection suppresses circulating viral restriction microRNAs. AIDS Res Hum Retroviruses. 2016;32(4):386-9. PubMed PMID: 26607272. PMCID: 4817567. Epub 2015/11/27.eng.

  50. Ouellet DL, Vigneault-Edwards J, Letourneau K, Gobeil LA, Plante I, Burnett JC, Rossi JJ, Provost P. Regulation of host gene expression by HIV-1 TAR microRNAs. Retrovirology. 2013;10:86. PubMed PMID: 23938024. PM-CID: 3751525. Epub 2013/08/14.eng.

  51. Kaul D, Khanna A, Suman. Evidence and nature of a novel miRNA encoded by HIV-1. Proc Indian Natl Sci Acad. 2006;72(2):91-5.

  52. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97.

  53. Kaul D, Ahlawat A, Gupta SD. HIV-1 genome-encoded hiv1-mir-H1 impairs cellular responses to infection. Mol Cell Biochem. 2009;323(1-2):143-8. PubMed PMID: 19082544. Epub 2008/12/17.eng.

  54. Hariharan M, Scaria V, Pillai B, Brahmachari SK. Targets for human encoded microRNAs in HIV genes. Biochem Biophys Res Commun. 2005;337(4):1214-8. PubMed PMID: 16236258. Epub 2005/10/21.eng.

  55. Zhao RY, Bukrinsky M, Elder RT. HIV-1 viral protein R (Vpr) & host cellular responses. Indian J Med Res. 2005;121(4):270-86. PubMed PMID: 15817944. Epub 2005/04/09.eng.

  56. Kino T, Gragerov A, Slobodskaya O, Tsopanomichalou M, Chrousos GP, Pavlakis GN. Human immunodeficiency virus type 1 (HIV-1) accessory protein Vpr induces transcription of the HIV-1 and glucocorticoid-responsive promoters by binding directly to p300/CBP coactivators. J Virol. 2002;76(19):9724-34. PubMed PMID: 12208951. PMCID: 136530. Epub 2002/09/05.eng.

  57. Yeung ML, Bennasser Y, Watashi K, Le SY, Houzet L, Jeang KT. Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: Evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res. 2009;37(19):6575-86. PubMed PMID: 19729508. PMCID: 2770672. Epub 2009/09/05.eng.

  58. Li L, Feng H, Da Q, Jiang H, Chen L, Xie L, Huang Q, Xiong H, Luo F, Kang L, Zeng Y, Hu H, Hou W, Feng Y. Expression of HIV-encoded microRNA-TAR and its inhibitory effect on viral replication in human primary macrophages. Arch Virol. 2016;161(5):1115-23. PubMed PMID: 26831929. Epub 2016/02/03.eng.

  59. Kestler HW 3rd, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell. 1991;65(4):651-62. PubMed PMID: 2032289. Epub 1991/05/17.eng.

  60. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, McPhee DA, Greenway AL, Ellett A, Chatfield C, Lawson VA, Crowe S, Maerz A, Sonza S, Learmont J, Sullivan JS, Cunningham A, Dwyer D, Dowton D, Mills J. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 1995;270(5238):988-91. PubMed PMID: 7481804. Epub 1995/11/10.eng.

  61. Mariani R, Kirchhoff F, Greenough TC, Sullivan JL, Desrosiers RC, Skowronski J. High frequency of defective nef alleles in a long-term survivor with nonprogressive human immunodeficiency virus type 1 infection. J Virol. 1996;70(11):7752-64. PubMed PMID: 8892896. PMCID: 190845. Epub 1996/11/01.eng.

  62. Michael NL, Chang G, d'Arcy LA, Ehrenberg PK, Mariani R, Busch MP, Birx DL, Schwartz DH. Defective accessory genes in a human immunodeficiency virus type 1-infected long-term survivor lacking recoverable virus. J Virol. 1995;69(7):4228-36. PubMed PMID: 7769682. PMCID: 189160. Epub 1995/07/01.eng.

  63. D'Aloja P, Olivetta E, Bona R, Nappi F, Pedacchia D, Pugliese K, Ferrari G, Verani P, Federico M. gag, vif, and nef genes contribute to the homologous viral interference induced by a nonproducer human immunodeficiency virus type 1 (HIV-1) variant: Identification of novel HIV-1-inhibiting viral protein mutants. J Virol. 1998;72(5):4308-19. PubMed PMID: 9557721. PMCID: 109661. Epub 1998/04/29.eng.

  64. D'Aloja P, Santarcangelo AC, Arold S, Baur A, Federico M. Genetic and functional analysis of the human immunodeficiency virus (HIV) type 1-inhibiting F12-HIVnef allele. J Gen Virol. 2001;82(Pt 11):2735-45. PubMed PMID: 11602785. Epub 2001/10/17.eng.

  65. Omoto S, Fujii YR. Regulation of human immunodeficiency virus 1 transcription by nef microRNA. J Gen Virol. 2005;86(Pt 3):751-5. PubMed PMID: 15722536. Epub 2005/02/22.eng.

  66. Buonaguro L, Buonaguro FM, Giraldo G, Ensoli B. The human immunodeficiency virus type 1 Tat protein trans-activates tumor necrosis factor beta gene expression through a TAR-like structure. J Virol. 1994;68(4):2677- 82. PubMed PMID: 8139045. PMCID: 236745. Epub 1994/04/01.eng.

  67. Dingwall C, Ernberg I, Gait MJ, Green SM, Heaphy S, Karn J, Lowe AD, Singh M, Skinner MA, Valerio R. Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc Natl Acad Sci U S A. 1989;86(18):6925-9. PubMed PMID: 2476805. PMCID: 297963. Epub 1989/09/01.eng.

  68. Alles J, Fehlmann T, Fischer U, Backes C, Galata V, Minet M, Hart M, Abu-Halima M, Grasser FA, Lenhof H-P, Keller A, Meese E. An estimate of the total number of true human miRNAs. Nucleic Acids Res. 2019;47(7):3353-64.

  69. Callis TE, Chen JF, Wang DZ. MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol. 2007;26(4):219-25. PubMed PMID: 17465888. Epub 2007/05/01.eng.

  70. Fabbri M, Ivan M, Cimmino A, Negrini M, Calin GA. Regulatory mechanisms of microRNAs involvement in cancer. Expert Opin Biol Ther. 2007;7(7):1009-19. PubMed PMID: 17665990. Epub 2007/08/02.eng.

  71. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007;5(8):e203. PubMed PMID: 17676975. PMCID: 1925136. Epub 2007/08/07. eng.

  72. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell. 2007;27(3):435-48. PubMed PMID: 17679093. PMCID: 3139456. Epub 2007/08/07.eng.

  73. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell. 2003 Feb;4(2):205-17. PubMed PMID: 12586064. Epub 2003/02/15.eng.

  74. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell. 2004;16(5):1235-50. PubMed PMID: 15084715. PMCID: 423212. Epub 2004/04/16.eng.

  75. Lecellier CH, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S, Himber C, Saib A, Voinnet O. A cellular microRNA mediates antiviral defense in human cells. Science. 2005;308(5721):557-60. PubMed PMID: 15845854. Epub 2005/04/23.eng.

  76. Qu N, Ma Z, Zhang M, Rushdi MN, Krueger CJ, Chen AK. Inhibition of retroviral Gag assembly by non-silencing miRNAs promotes autophagic viral degradation. Protein Cell. 2018;9(7):640-51. PubMed PMID: 28884441. PMCID: 6019656. Epub 2017/09/09.eng.

  77. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science. 2005;309(5740):1577-81. PubMed PMID: 16141076. Epub 2005/09/06.eng.

  78. Jopling CL, Norman KL, Sarnow P. Positive and negative modulation of viral and cellular mRNAs by liver-specific microRNA miR-122. Cold Spring Harb Symp Quant Biol. 2006;71:369-76. PubMed PMID: 17381319. Epub 2007/03/27.eng.

  79. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007;449(7164):919-22. PubMed PMID: 17943132. PM-CID: 2748825. Epub 2007/10/19.eng.

  80. Liston A, Papadopoulou AS, Danso-Abeam D, Dooley J. MicroRNA-29 in the adaptive immune system: Setting the threshold. Cell Mol Life Sci. 2012;69(21):3533-41. PubMed PMID: 22971773. Epub 2012/09/14.eng.

  81. Nathans R, Chu CY, Serquina AK, Lu CC, Cao H, Rana TM. Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol Cell. 2009;34(6):696-709. PubMed PMID: 19560422. PMCID: 2763548. Epub 2009/06/30.eng.

  82. Ahluwalia JK, Khan SZ, Soni K, Rawat P, Gupta A, Hariharan M, Scaria V, Lalwani M, Pillai B, Mitra D, Brahmachari SK. Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology. 2008;5:117. PubMed PMID: 19102781.eng.

  83. Hou J, Wang P, Lin L, Liu X, Ma F, An H, Wang Z, Cao X. MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J Immunol. 2009;183(3):2150-8. PubMed PMID: 19596990. Epub 2009/07/15.eng.

  84. Teng Y, Luo M, Yu T, Chen L, Huang Q, Chen S, Xie L, Zeng Y, Luo F, Xiong H, Liu Y, Hou W, Feng Y. CRISPR/Cas9-mediated deletion of miR-146a enhances antiviral response in HIV-1 infected cells. Genes Immun. 2019;20(4):327-37.

  85. Rokavec M, Li H, Jiang L, Hermeking H. The p53/miR-34 axis in development and disease. J Mol Cell Biol. 2014;6(3):214-30. PubMed PMID: 24815299. Epub 2014/05/13.eng.

  86. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ. A microRNA component of the p53 tumour suppressor network. Nature. 2007;447(7148):1130-4. PubMed PMID: 17554337. PMCID: 4590999. Epub 2007/06/08.eng.

  87. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, Tokino T. Epigenetic silencing of microR-NA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 2008;68(11):4123-32. PubMed PMID: 18519671. Epub 2008/06/04.eng.

  88. Amaral AJ, Andrade J, Foxall RB, Matoso P, Matos AM, Soares RS, Rocha C, Ramos CG, Tendeiro R, Serra-Caetano A, Guerra-Assunjao JA, Santa-Marta M, Gonjalves J, Gama-Carvalho M, Sousa AE. miRNA profiling of human naive CD4 T cells links miR-34c-5p to cell activation and HIV replication. EMBO J. 2017;36(3):346-60. PubMed PMID: 27993935. PMCID: 5286376. Epub 2016/12/21.eng.

  89. Modai S, Farberov L, Herzig E, Isakov O, Hizi A, Shomron N. HIV-1 infection increases microRNAs that inhibit Dicer1, HRB and HIV-EP2, thereby reducing viral replication. PLoS One. 2019;14(1):e0211111. PubMed PMID: 30682089. PMCID: 6347224. Epub 2019/01/27.eng.

  90. Saleh S, Wightman F, Ramanayake S, Alexander M, Kumar N, Khoury G, Pereira C, Purcell D, Cameron PU, Lewin SR. Expression and reactivation of HIV in a chemokine induced model of HIV latency in primary resting CD4+ T cells. Retrovirology. 2011;8:80. PubMed PMID: 21992606. PMCID: 3215964. Epub 2011/10/14. eng.

  91. Saleh S, Lu HK, Evans V, Harisson D, Zhou J, Jaworowski A, Sallmann G, Cheong KY, Mota TM, Tennakoon S, Angelovich TA, Anderson J, Harman A, Cunningham A, Gray L, Churchill M, Mak J, Drummer H, Vatakis DN, Lewin SR, Cameron PU. HIV integration and the establishment of latency in CCL19-treated resting CD4+ T cells require activation of NF-KB. Retrovirology. 2016;13(1):49. PubMed PMID: 27459960. PMCID: 4962537. Epub 2016/07/28.eng.

  92. Han Y, Lin YB, An W, Xu J, Yang HC, O'Connell K, Dordai D, Boeke JD, Siliciano JD, Siliciano RF. Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell Host Microbe. 2008;4(2):134-46. PubMed PMID: 18692773. PMCID: 2604135. Epub 2008/08/12.eng.

  93. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, Van Lint C, Aunis D, Rohr O. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J. 2007;26(2):412-23. PubMed PMID: 17245431. PMCID: 1783449. Epub 2007/01/25.eng.

  94. du Chene I, Basyuk E, Lin YL, Triboulet R, Knezevich A, Chable-Bessia C, Mettling C, Baillat V, Reynes J, Corbeau P, Bertrand E, Marcello A, Emiliani S, Kiernan R, Benkirane M. Suv39H1 and HP1y are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J. 2007;26(2):424-35. PubMed PMID: 17245432.eng.

  95. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, Boucher G, Boulassel MR, Ghattas G, Brenchley JM, Schacker TW, Hill BJ, Douek DC, Routy JP, Haddad EK, Sekaly RP. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med. 2009;15(8):893-900. PubMed PMID: 19543283. PMCID: 2859814. Epub 2009/06/23. eng.

  96. Van Lint C, Emiliani S, Ott M, Verdin E. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 1996;15(5):1112-20. PubMed PMID: 8605881. PMCID: 450009. Epub 1996/03/01.eng.

  97. Bednarik DP, Duckett C, Kim SU, Perez VL, Griffis K, Guenthner PC, Folks TM. DNA CpG methylation inhibits binding of NF-KB proteins to the HIV-1 long terminal repeat cognate DNA motifs. New Biol. 1991;3(10):969-76. PubMed PMID: 1768651. Epub 1991/10/01.eng.

  98. Blazkova J, Murray D, Justement JS, Funk EK, Nelson AK, Moir S, Chun TW, Fauci AS. Paucity of HIV DNA methylation in latently infected, resting CD4+ T cells from infected individuals receiving antiretroviral therapy. J Virol. 2012;86(9):5390-2. PubMed PMID: 22345448. PM-CID: 3347337. Epub 2012/02/22.eng.

  99. Duverger A, Jones J, May J, Bibollet-Ruche F, Wagner FA, Cron RQ, Kutsch O. Determinants of the establishment of human immunodeficiency virus type 1 latency. J Virol. 2009;83(7):3078-93. PubMed PMID: 19144703. PMCID: 2655589. Epub 2009/01/16.eng.

  100. Burnett JC, Miller-Jensen K, Shah PS, Arkin AP, Schaffer DV. Control of stochastic gene expression by host factors at the HIV promoter. PLoS Pathog. 2009;5(1):e1000260. PubMed PMID: 19132086. PMCID: 2607019. Epub 2009/01/10.eng.

  101. Duverger A, Wolschendorf F, Zhang M, Wagner F, Hatcher B, Jones J, Cron RQ, van der Sluis RM, Jeeninga RE, Berkhout B, Kutsch O. An AP-1 binding site in the enhancer/core element of the HIV-1 promoter controls the ability of HIV-1 to establish latent infection. J Virol. 2013;87(4):2264-77. PubMed PMID: 23236059. PM.

  102. Donahue DA, Kuhl BD, Sloan RD, Wainberg MA. The viral protein Tat can inhibit the establishment of HIV-1 latency. J Virol. 2012;86(6):3253-63. PubMed PMID: 22238306. PMCID: 3302319. Epub 2012/01/13.eng.

  103. Weinberger LS, Burnett JC, Toettcher JE, Arkin AP, Schaffer DV. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell. 2005;122(2):169-82. PubMed PMID: 16051143. Epub 2005/07/30.eng.

  104. Tyagi M, Karn J. CBF-1 promotes transcriptional silencing during the establishment of HIV-1 latency. EMBO J. 2007;26(24):4985-95. PubMed PMID: 18007589. PM-CID: 2140115. Epub 2007/11/17.eng.

  105. Pearson R, Kim YK, Hokello J, Lassen K, Friedman J, Tyagi M, Karn J. Epigenetic silencing of human immunodeficiency virus (HIV) transcription by formation of restrictive chromatin structures at the viral long terminal repeat drives the progressive entry of HIV into latency. J Virol. 2008;82(24):12291-303. PubMed PMID: 18829756. PMCID: 2593349. Epub 2008/10/03.eng.

  106. Riou C, Yassine-Diab B, van Grevenynghe J, Somogyi R, Greller LD, Gagnon D, Gimmig S, Wilkinson P, Shi Y, Cameron MJ, Campos-Gonzalez R, Balderas RS, Kelvin D, Sekaly RP, Haddad EK. Convergence of TCR and cytokine signaling leads to FOXO3a phosphorylation and drives the survival of CD4+ central memory T cells. J Exp Med. 2007;204(1):79-91. PubMed PMID: 17190839. PMCID: 2118424. Epub 2006/12/28.eng.

  107. Tzachanis D, Lafuente EM, Li L, Boussiotis VA. Intrinsic and extrinsic regulation of T lymphocyte quiescence. Leuk Lymphoma. 2004;45(10):1959-67. PubMed PMID: 15370239. Epub 2004/09/17.eng.

  108. Van Der Heide LP, Hoekman MFM, Smidt MP. The ins and outs of FoxO shuttling: Mechanisms of FoxO translocation and transcriptional regulation. Biochem J. 2004;380(Pt 2):297-309. PubMed PMID: 15005655. PM-CID: 1224192. Epub 2004/03/10.eng.

  109. Wang X, Diao C, Yang X, Yang Z, Liu M, Li X, Tang H. ICP4-induced miR-101 attenuates HSV-1 replication. Sci Rep. 2016;6:23205. PubMed PMID: 26984403. PMCID: 4794718. Epub 2016/03/18.eng.

  110. Zheng SQ, Li YX, Zhang Y, Li X, Tang H. MiR-101 regulates HSV-1 replication by targeting ATP5B. Antiviral Res. 2011;89(3):219-26. PubMed PMID: 21291913. Epub 2011/02/05.eng.

  111. Pan D, Flores O, Umbach JL, Pesola JM, Bentley P, Rosato PC, Leib DA, Cullen BR, Coen DM. A neuron-specific host microRNA targets herpes simplex virus-1 ICP0 expression and promotes latency. Cell Host Microbe. 2014;15(4):446-56. PubMed PMID: 24721573. PMCID: 4142646. Epub 2014/04/12.eng.

  112. Wang Q, Li DC, Li ZF, Liu CX, Xiao YM, Zhang B, Li XD, Zhao J, Chen LP, Xing XM, Tang SF, Lin YC, Lai YD, Yang P, Zeng JL, Xiao Q, Zeng XW, Lin ZN, Zhuang ZX, Zhuang SM, Chen W. Upregulation of miR-27a contributes to the malignant transformation of human bronchial epithelial cells induced by SV40 small T antigen. Oncogene. 2011;30(36):3875-86. PubMed PMID: 21460851. Epub 2011/04/05.eng.

  113. Lerner M, Lundgren J, Akhoondi S, Jahn A, Ng HF, Ak- bari Moqadam F, Oude Vrielink JAF, Agami R, Den Boer ML, Grander D, Sangfelt O. MiRNA-27a controls FBW7/hCDC4-dependent cyclin E degradation and cell cycle progression. Cell Cycle. 2011;10(13):2172-83. PubMed PMID: 21597324. Epub 2011/05/21.eng.

  114. Xie N, Cui H, Banerjee S, Tan Z, Salomao R, Fu M, Abraham E, Thannickal VJ, Liu G. miR-27a regulates inflammatory response of macrophages by targeting IL-10. J Immunol. 2014;193(1):327-34. PubMed PMID: 24835395. PMCID: 4065847. Epub 2014/05/20.eng.

  115. Park JL, Kim M, Song KS, Kim SY, Kim YS. Cell-free miR-27a, a potential diagnostic and prognostic biomarker for gastric cancer. Genomics Inform. 2015;13(3):70-5. PubMed PMID: 26523130. PMCID: 4623443. Epub 2015/11/03.eng.

  116. Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci. 2007;10(12):1513-4. PubMed PMID: 17994015. Epub 2007/11/13.eng.

  117. Alvarez-Saavedra M, Antoun G, Yanagiya A, Oliva-Hernandez R, Cornejo-Palma D, Perez-Iratxeta C, Sonenberg N, Cheng HY. miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum Mol Genet. 2011;20(4):731-51. PubMed PMID: 21118894. PMCID: 3115667. Epub 2010/12/02.eng.

  118. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S, 0rum H. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science. 2010;327(5962):198-201. PubMed PMID: 19965718. PMCID: 3436126. Epub 2009/12/08.eng.

  119. Norman KL, Sarnow P. Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J Virol. 2010;84(1):666-70. PubMed PMID: 19846523. PMCID: 2798415. Epub 2009/10/23.eng.


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