How HTLV-1 may subvert miRNAs for persistence and transformation.

[en] Distinct mechanisms are used by viruses to interact with cellular miRNAs. The role of microRNAs in viral replication and persistence ranges from viral-encoded microRNAs to suppressors of RNA interference. Viruses can also exploit cellular miRNAs for influencing cellular metabolism to ensure efficient replication or latency. In particular, two recent studies provide examples of how HTLV-1 may co-opt or subvert cellular miRNAs for persistent replication and oncogenic purposes. The pathways modulated by these described miRNAs are critically involved in apoptosis, proliferation and innate immune response.

Disciplines :

Oncology

Author, co-author :

Bouzar, Amel ; Université de Liège - ULiège > Chimie et bio-industries > Centre de Bio. Fond. - Section de Biologie cell. et moléc.

Willems, Luc ; Université de Liège - ULiège > GIGA-Research

Language :

English

Title :

How HTLV-1 may subvert miRNAs for persistence and transformation.

Publication date :

2008

Journal title :

Retrovirology

eISSN :

1742-4690

Publisher :

BioMed Central, London, United Kingdom

Volume :

Pages :

101

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 07 April 2009

Statistics

Number of views

115 (23 by ULiège)

Number of downloads

1 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Gironella M Seux M Xie MJ Cano C Tomasini R Gommeaux J Garcia S Nowak J Yeung ML Jeang KT Chaix A Fazli L Motoo Y Wang Q Rocchi P Russo A Gleave M Dagorn JC Iovanna JL Carrier A Pébusque MJ Dusetti NJ Tumor protein 53-induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development Proc Natl Acad Sci USA 2007, 104:16170-16175. 2042180 17911264 10.1073/pnas.0703942104
Scaria V Jadhav V microRNAs in viral oncogenesis Retrovirology 2007, 4:82. 2217556 18036240 10.1186/1742-4690-4-82
Yeung ML Benkirane M Jeang KT Small non-coding RNAs, mammalian cells, and viruses: Regulatory interactions? Retrovirology 2007, 4:74. 2164956 17937800 10.1186/1742-4690-4-74
Baltimore D Boldin MP O'Connell RM Rao DS Taganov KD MicroRNAs: New regulators of immune cell development and function Nat Immunol 2008, 9:839-845. 10.1038/ni.f.209 18645592
Voinnet O Pinto YM Baulcombe DC Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants Proc Natl Acad Sci USA 1999, 96:14147-14152. 24205 10570213 10.1073/pnas.96.24.14147
Roth BM Pruss GJ Vance VB Plant viral suppressors of RNA silencing Virus Res 2004, 102:97-108. 10.1016/j.virusres.2004.01.020 15068885
Grassmann R Jeang K The roles of microRNAs in mammalian virus infection Biochim Biophys Acta 2008, 1779:706-711. 18549828
Pfeffer S Zavolan M Grässer FA Chien M Russo JJ Ju J John B Enright AJ Marks D Sander C Tuschl T Identification of virus-encoded microRNAs Science 2004, 304:734-736. 10.1126/science.1096781 15118162
Pfeffer S Sewer A Lagos-Quintana M Sheridan R Sander C Grässer FA van Dyk LF Ho CK Shuman S Chien M Russo JJ Ju J Randall G Lindenbach BD Rice CM Simon V Ho DD Zavolan M Tuschl T Identification of microRNAs of the herpesvirus family Nat Methods 2005, 2:269-276. 10.1038/nmeth746 15782219
Tang S Bertke AS Patel A Wang K Cohen JI Krause PR An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor Proc Natl Acad Sci USA 2008, 105:10931-10936. 10.1073/pnas.0801845105 18678906
Cai X Lu S Zhang Z Gonzalez CM Damania B Cullen BR Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells Proc Natl Acad Sci USA 2005, 102:5570-5575. 556237 15800047 10.1073/pnas.0408192102
Sullivan CS Grundhoff AT Tevethia S Pipas JM Ganem D SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells Nature 2005, 435:682-686. 10.1038/nature03576 15931223
Lu S Cullen BR Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis J Virol 2004, 78:12868-12876. 524998 15542639 10.1128/JVI.78.23.12868-12876.2004
Watanabe Y Kishi A Yachie N Kanai A Tomita M Computational analysis of microRNA-mediated antiviral defense in humans FEBS Lett 2007, 581:4603-4610. 10.1016/j.febslet.2007.08.049 17825824
Lecellier CH Dunoyer P Arar K Lehmann-Che J Eyquem S Himber C Saïb A Voinnet O A cellular microRNA mediates antiviral defense in human cells Science 2005, 308:557-560. 10.1126/science.1108784 15845854
Jopling CL Yi M Lancaster AM Lemon SM Sarnow P Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA Science 2005, 309:1577-1581. 10.1126/science.1113329 16141076
Jopling CL Schutz S Sarnow P Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome Cell Host Microbe 2008, 4:77-85. 10.1016/j.chom.2008.05.013 18621012
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, 449:919-922. 10.1038/nature06205 17943132
Kapadia SB Chisari FV Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids Proc Natl Acad Sci USA 2005, 102:2561-2566. 549027 15699349 10.1073/pnas.0409834102
Ye J Wang C Sumpter R Jr Brown MS Goldstein JL Gale M Jr Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation Proc Natl Acad Sci USA 2003, 100:15865-15870. 307659 14668447 10.1073/pnas.2237238100
Cullen BR Is RNA interference involved in intrinsic antiviral immunity in mammals? Nat Immunol 2006, 7:563-567. 10.1038/ni1352 16715068
Triboulet R Mari B Lin YL Chable-Bessia C Bennasser Y Lebrigand K Cardinaud B Maurin T Barbry P Baillat V Reynes J Corbeau P Jeang KT Benkirane M Suppression of microRNA-silencing pathway by HIV-1 during virus replication Science 2007, 315:1579-1582. 10.1126/science.1136319 17322031
Huang J Wang F Argyris E Chen K Liang Z Tian H Huang W Squires K Verlinghieri G Zhang H Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes Nat Med 2007, 13:1241-1247. 10.1038/ nm1639 17906637
Han Y Siliciano RF Keeping quiet: MicroRNAs in HIV-1 latency Nat Med 2007, 13:1138-1140. 10.1038/nm1007-1138 17917655
Lu F Weidmer A Liu CG Volinia S Croce CM Lieberman PM Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence J Virol 2008, 82:10436-10443. 10.1128/ JVI.00752-08 18753206
Motsch N Pfuhl T Mrazek J Barth S Grasser FA Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a RNA Biol 2007, 4:131-137. 18347435
Tam W Identification and characterization of human BIC, a gene on chromosome 21 that encodes a noncoding RNA Gene 2001, 274:157-167. 10.1016/S0378-1119(01)00612-6 11675008
Lum AM Wang BB Li L Channa N Bartha G Wabl M Retroviral activation of the mir-106a microRNA cistron in T lymphoma Retrovirology 2007, 4:5. 1794537 17442096 10.1186/1742-4690-4-5
Beck-Engeser GB Lum AM Huppi K Caplen NJ Wang BB Wabl M Pvt1-encoded microRNAs in oncogenesis Retrovirology 2008, 5:4. 2257975 18194563 10.1186/1742-4690-5-4
Pichler K Schneider G Grassmann R MicroRNA miR-146a and further oncogenesis-related cellular microRNAs are dysregulated in HTLV-1 transformed T lymphocytes Retrovirology 2008, 5:100. 10.1186/ 1742-4690-5-100 19014482
Yeung ML Yasunaga J Bennasser Y Dusetti N Harris D Ahmad N Matsuoka M Jeang KT Roles for MicroRNAs, miR-93 and miR-130b, and Tumor Protein 53-Induced Nuclear Protein 1 Tumor Suppressor in Cell Growth Dysregulation by Human T-Cell Lymphotrophic Virus 1 Cancer Res 2008, 68:8976-8985. 10.1158/0008-5472.CAN-08-0769 18974142
Hanon E Stinchcombe JC Saito M Asquith BE Taylor GP Tanaka Y Weber JN Griffiths GM Bangham CR Fratricide among CD8(+) T lymphocytes naturally infected with human T cell lymphotropic virus type I Immunity 2000, 13:657-664. 10.1016/S1074-7613(00)00065-0 11114378
Jones KS Petrow-Sadowski C Huang YK Bertolette DC Ruscetti FW Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(+) T cells Nat Med 2008, 14:429-436. 10.1038/ nm1745 18376405
Twizere JC Kruys V Lefèbvre L Vanderplasschen A Collete D Debacq C Lai WS Jauniaux JC Bernstein LR Semmes OJ Burny A Blackshear PJ Kettmann R Willems L Interaction of retroviral Tax oncoproteins with tristetraprolin and regulation of tumor necrosis factor-alpha expression J Natl Cancer Inst 2003, 95:1846-1859. 14679154
Matsuoka M Jeang KT Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation Nat Rev Cancer 2007, 7:270-280. 10.1038/nrc2111 17384582
Boxus M Twizere JC Legros S Dewulf JF Kettmann R Willems L The HTLV-1 Tax interactome Retrovirology 2008, 5:76. 2533353 18702816 10.1186/ 1742-4690-5-76
Tomasini R Seux M Nowak J Bontemps C Carrier A Dagorn JC Pébusque MJ Iovanna JL Dusetti NJ TP53INP1 is a novel p73 target gene that induces cell cycle arrest and cell death by modulating p73 transcriptional activity Oncogene 2005, 24:8093-8104. 16044147
Gommeaux J Cano C Garcia S Gironella M Pietri S Culcasi M Pébusque MJ Malissen B Dusetti N Iovanna J Carrier A Colitis and colitis-associated cancer are exacerbated in mice deficient for tumor protein 53-induced nuclear protein 1 Mol Cell Biol 2007, 27:2215-2228. 1820489 17242209 10.1128/MCB.01454-06
Ito Y Motoo Y Yoshida H Iovanna JL Takamura Y Miya A Kuma K Miyauchi A Decreased expression of tumor protein p53-induced nuclear protein 1 (TP53INP1) in breast carcinoma Anticancer Res 2006, 26:4391-4395. 17201159
Jiang PH Motoo Y Garcia S Iovanna JL Pebusque MJ Sawabu N Down-expression of tumor protein p53-induced nuclear protein 1 in human gastric cancer World J Gastroenterol 2006, 12:691-696. 16521180
Bonazzi VF Irwin D Hayward NK Identification of candidate tumor suppressor genes inactivated by promoter methylation in melanoma Genes Chromosomes Cancer 2009, 48:1-10. 21 10.1002/gcc.20615 18803327
Ito Y Motoo Y Yoshida H Iovanna JL Nakamura Y Kuma K Miyauchi A High level of tumour protein p53-induced nuclear protein 1 (TP53INP1) expression in anaplastic carcinoma of the thyroid Pathology 2006, 38:545-547. 10.1080/00313020601024094 17393983
Eis PS Tam W Sun L Chadburn A Li Z Gomez MF Lund E Dahlberg JE Accumulation of miR-155 and BIC RNA in human B cell lymphomas Proc Natl Acad Sci USA 2005, 102:3627-3632. 552785 15738415 10.1073/pnas.0500613102
Kluiver J Poppema S de Jong D Blokzijl T Harms G Jacobs S Kroesen BJ Berg van den A BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas J Pathol 2005, 207:243-249. 10.1002/path.1825 16041695
Rodriguez A Vigorito E Clare S Warren MV Couttet P Soond DR van Dongen S Grocock RJ Das PP Miska EA Vetrie D Okkenhaug K Enright AJ Dougan G Turner M Bradley A Requirement of bic/microRNA-155 for normal immune function Science 2007, 316:608-611. 10.1126/science.1139253 17463290
Thai TH Calado DP Casola S Ansel KM Xiao C Xue Y Murphy A Frendewey D Valenzuela D Kutok JL Schmidt-Supprian M Rajewsky N Yancopoulos G Rao A Rajewsky K Regulation of the germinal center response by microRNA-155 Science 2007, 316:604-608. 10.1126/science.1141229 17463289
Yin Q McBride J Fewell C Lacey M Wang X Lin Z Cameron J Flemington EK MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways J Virol 2008, 82:5295-5306. 2395216 18367535 10.1128/JVI.02380-07
Kong W Yang H He L Zhao JJ Coppola D Dalton WS et al MicroRNA-155 Is Regulated by TGF{beta}/Smad Pathway and Contributes to Epithelial Cell Plasticity by Targeting RhoA Mol Cell Biol 2008, 28:6773-6784. 10.1128/ MCB.00941-08 18794355
Daly AC Randall RA Hill CS TGF-{beta}-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth Mol Cell Biol 2008, 28:6889-6902. 10.1128/MCB.01192-08 18794361
Arnulf B Villemain A Nicot C Mordelet E Charneau P Kersual J Zermati Y Mauviel A Bazarbachi A Hermine O Human T-cell lymphotropic virus oncoprotein Tax represses TGF-beta 1 signaling in human T cells via c-Jun activation: A potential mechanism of HTLV-I leukemogenesis Blood 2002, 100:4129-4138. 10.1182/blood-2001-12-0372 12393612
Mori N Morishita M Tsukazaki T Giam CZ Kumatori A Tanaka Y Yamamoto N Human T-cell leukemia virus type I oncoprotein Tax represses Smad-dependent transforming growth factor beta signaling through interaction with CREB-binding protein/p300 Blood 2001, 97:2137-2144. 10.1182/blood.V97.7.2137 11264182
Lee DK Kim BC Brady JN Jeang KT Kim SJ Human T-cell lymphotropic virus type 1 tax inhibits transforming growth factor-beta signaling by blocking the association of Smad proteins with Smad-binding element J Biol Chem 2002, 277:33766-33775. 10.1074/jbc.M200150200 12097320
Taganov KD Boldin MP Chang KJ Baltimore D NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses Proc Natl Acad Sci USA 2006, 103:12481-12486. 1567904 16885212 10.1073/pnas.0605298103
Dai R Phillips RA Zhang Y Khan D Crasta O Ahmed SA Suppression of LPS-induced IFN{gamma} and nitric oxide in splenic lymphocytes by select estrogen-regulated miRNA: A novel mechanism of immune modulation Blood 2008.
Kawai T Akira S Signaling to NF-kappaB by Toll-like receptors Trends Mol Med 2007, 13:460-469. 10.1016/j.molmed.2007.09.002 18029230
Jazdzewski K Murray EL Franssila K Jarzab B Schoenberg DR Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma Proc Natl Acad Sci USA 2008, 105:7269-7274. 10.1073/pnas.0802682105 18474871 2438239
Cavanagh MH Landry S Audet B Arpin-André C Hivin P Paré ME Thête J Wattel E Marriott SJ Mesnard JM Barbeau B HTLV-I antisense transcripts initiating in the 3′LTR are alternatively spliced and polyadenylated Retrovirology 2006, 3:15. 1459196 16512901 10.1186/ 1742-4690-3-15
Usui T Yanagihara K Tsukasaki K Murata K Hasegawa H Yamada Y Kamihira S Characteristic expression of HTLV-1 basic zipper factor (HBZ) transcripts in HTLV-1 provirus-positive cells Retrovirology 2008, 5:34. 2386809 18426605 10.1186/1742-4690-5-34
Satou Y Yasunaga J Yoshida M Matsuoka M HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells Proc Natl Acad Sci USA 2006, 103:720-725. 1334651 16407133 10.1073/ pnas.0507631103