The m6A epitranscriptome opens a new charter in immune system logic

References

• Delaunay S, Frye M. RNA modifications regulating cell fate in cancer. Nat Cell Biol. 2019;21(5):552–559.
   Google Scholar
• Desrosiers R, Friderici K, Rottman F. Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells. Proc Natl Acad Sci U S A. 1974;71(10):3971–3975.
   Google Scholar
• Chen Z, Zhao P, Li F, et al. Comprehensive review and assessment of computational methods for predicting RNA post-transcriptional modification sites from RNA sequences. Brief Bioinform. 2019. DOI:10.1093/bib/bbz112
   Google Scholar
• Meyer KD. DART-seq: an antibody-free method for global m(6)A detection. Nat Methods. 2019;16(12):1275–1280.
   Google Scholar
• Liu J, Li K, Cai J, et al. Landscape and regulation of m(6)A and m(6)am methylome across human and mouse tissues. Mol Cell. 2020;77(2):426–440.
   Google Scholar
• Yang Y, Hsu PJ, Chen YS, et al. Dynamic transcriptomic m(6)A decoration: writers, erasers, readers and functions in RNA metabolism. Cell Res. 2018;28(6):616–624.
   Google Scholar
• Zheng Q, Hou J, Zhou Y, et al. The RNA helicase DDX46 inhibits innate immunity by entrapping m(6)A-demethylated antiviral transcripts in the nucleus. Nat Immunol. 2017;18(10):1094–1103.
   Google Scholar
• Liu Y, Liu Z, Tang H, et al. The N(6)-methyladenosine (m(6)A)-forming enzyme METTL3 facilitates M1 macrophage polarization through the methylation of STAT1 mRNA. Am J Physiol Cell Physiol. 2019;317(4):C762–C775.
   Google Scholar
• Wang H, Hu X, Huang M, et al. Mettl3-mediated mRNA m(6)A methylation promotes dendritic cell activation. Nat Commun. 2019;10(1):1898.
   Google Scholar
• Gokhale NS, McIntyre A, Mattocks MD, et al. Altered m(6)A modification of specific cellular transcripts affects flaviviridae infection. Mol Cell. 2020;77(3):542–555.
   Google Scholar
• Han D, Liu J, Chen C, et al. Anti-tumour immunity controlled through mRNA m(6)A methylation and YTHDF1 in dendritic cells. Nature. 2019;566(7743):270–274.
   Google Scholar
• Sledz P, Jinek M. Structural insights into the molecular mechanism of the m(6)A writer complex. Elife. 2016;5. DOI:10.7554/eLife.18434.
   Google Scholar
• Liu J, Yue Y, Han D, et al. A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat Chem Biol. 2014;10(2):93–95.
   Google Scholar
• Zhang S. Mechanism of N(6)-methyladenosine modification and its emerging role in cancer. Pharmacol Ther. 2018;189(173–183). DOI:10.1016/j.pharmthera.2018.04.011
   Google Scholar
• Hu Y, Wang S, Liu J, et al. New sights in cancer: component and function of N6-methyladenosine modification. Biomed Pharmacother. 2020;122(109694). DOI:10.1016/j.biopha.2019.109694
   Google Scholar
• Lan Q, Liu PY, Haase J, et al. The critical role of RNA m(6)A methylation in cancer. Cancer Res. 2019;79(7):1285–1292.
   Google Scholar
• Mendel M, Chen KM, Homolka D, et al. Methylation of structured RNA by the m(6)A writer METTL16 is essential for mouse embryonic development. Mol Cell. 2018;71(6):986–1000.
   Google Scholar
• Wang X, Feng J, Xue Y, et al. Structural basis of N(6)-adenosine methylation by the METTL3-METTL14 complex. Nature. 2016;534(7608):575–578.
   Google Scholar
• Ping XL, Sun BF, Wang L, et al. Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 2014;24(2):177–189.
   Google Scholar
• Lan T, Li H, Zhang D, et al. KIAA1429 contributes to liver cancer progression through N6-methyladenosine-dependent post-transcriptional modification of GATA3. Mol Cancer. 2019;18(1):186.
   Google Scholar
• Knuckles P, Lence T, Haussmann IU, et al. Zc3h13/Flacc is required for adenosine methylation by bridging the mRNA-binding factor Rbm15/Spenito to the m(6)A machinery component Wtap/Fl(2)d. Genes Dev. 2018;32(5–6):415–429.
   Google Scholar
• Wang Y, Li Y, Toth JI, et al. N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat Cell Biol. 2014;16(2):191–198.
   Google Scholar
• Zhou KI, Pan T. Structures of the m(6)A methyltransferase complex: two subunits with distinct but coordinated roles. Mol Cell. 2016;63(2):183–185.
   Google Scholar
• Yao QJ, Sang L, Lin M, et al. Mettl3-Mettl14 methyltransferase complex regulates the quiescence of adult hematopoietic stem cells. Cell Res. 2018;28(9):952–954.
   Google Scholar
• Pendleton KE, Chen B, Liu K, et al. The U6 snRNA m(6)A methyltransferase METTL16 regulates SAM synthetase intron retention. Cell. 2017;169(5):824–835.
   Google Scholar
• Frayling TM, Timpson NJ, Weedon MN, et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science. 2007;316(5826):889–894.
   Google Scholar
• Jia G, Fu Y, Zhao X, et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol. 2011;7(12):885–887.
   Google Scholar
• Huang Y, Su R, Sheng Y, et al. Small-molecule targeting of oncogenic FTO demethylase in acute myeloid leukemia. Cancer Cell. 2019;35(4):677–691.
   Google Scholar
• Li Z, Weng H, Su R, et al. FTO plays an oncogenic role in acute myeloid leukemia as a N(6)-methyladenosine RNA demethylase. Cancer Cell. 2017;31(1):127–141.
   Google Scholar
• Wu R, Liu Y, Yao Y, et al. FTO regulates adipogenesis by controlling cell cycle progression via m(6)A-YTHDF2 dependent mechanism. Biochim Biophys Acta Mol Cell Biol Lipids. 2018;1863(10):1323–1330.
   Google Scholar
• Yang S, Wei J, Cui YH, et al. m(6)A mRNA demethylase FTO regulates melanoma tumorigenicity and response to anti-PD-1 blockade. Nat Commun. 2019;10(1):2782.
   Google Scholar
• Tang C, Klukovich R, Peng H, et al. ALKBH5-dependent m6A demethylation controls splicing and stability of long 3ʹ-UTR mRNAs in male germ cells. Proc Natl Acad Sci U S A. 2018;115(2):E325–E333.
   Google Scholar
• Patil DP, Pickering BF, Jaffrey SR. Reading m(6)A in the transcriptome: m(6)A-binding proteins. Trends Cell Biol. 2018;28(2):113–127.
   Google Scholar
• Wang X, Zhao BS, Roundtree IA, et al. N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell. 2015;161(6):1388–1399.
   Google Scholar
• Shi H, Wang X, Lu Z, et al. YTHDF3 facilitates translation and decay of N(6)-methyladenosine-modified RNA. Cell Res. 2017;27(3):315–328.
   Google Scholar
• Jin D, Guo J, Wu Y, et al. m(6)A mRNA methylation initiated by METTL3 directly promotes YAP translation and increases YAP activity by regulating the MALAT1-miR-1914-3p-YAP axis to induce NSCLC drug resistance and metastasis. J Hematol Oncol. 2019;12(1):135.
   Google Scholar
• Roundtree IA, Luo GZ, Zhang Z, et al. YTHDC1 mediates nuclear export of N(6)-methyladenosine methylated mRNAs. Elife. 2017;6. DOI:10.7554/eLife.31311.
   Google Scholar
• Liu J, Dou X, Chen C, et al. N (6)-methyladenosine of chromosome-associated regulatory RNA regulates chromatin state and transcription. Science. 2020;367(6477):580–586.
   Google Scholar
• Wu R, Jiang D, Wang Y, et al. N (6)-methyladenosine (m(6)A) methylation in mRNA with a dynamic and reversible epigenetic modification. Mol Biotechnol. 2016;58(7):450–459.
   Google Scholar
• Ma C, Liao S, Zhu Z. Crystal structure of human YTHDC2 YTH domain. Biochem Biophys Res Commun. 2019;518(4):678–684.
   Google Scholar
• Bailey AS, Batista PJ, Gold RS, et al. The conserved RNA helicase YTHDC2 regulates the transition from proliferation to differentiation in the germline. Elife. 2017;6. DOI:10.7554/eLife.26116.
   Google Scholar
• Soh Y, Mikedis MM, Kojima M, et al.:Meioc maintains an extended meiotic prophase I in mice. Plos Genet. 2017;13(4):e1006704.
   Google Scholar
• Huang H, Weng H, Sun W, et al. Author correction: recognition of RNA N(6)-methyladenosine by IGF2BP proteins enhances mRNA stability and translation. Nat Cell Biol. 2018;20(9):1098.
   Google Scholar
• Samuels TJ, Jarvelin AI, Ish-Horowicz D, et al. Imp/IGF2BP levels modulate individual neural stem cell growth and division through myc mRNA stability. Elife. 2020;9. DOI:10.7554/eLife.51529.
   Google Scholar
• Hutt DM, Loguercio S, Roth DM, et al. Correcting the F508del-CFTR variant by modulating eukaryotic translation initiation factor 3-mediated translation initiation. J Biol Chem. 2018;293(35):13477–13495.
   Google Scholar
• Alarcon CR, Goodarzi H, Lee H, et al. HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA processing events. Cell. 2015;162(6):1299–1308.
   Google Scholar
• Liu N, Dai Q, Zheng G, et al. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature. 2015;518(7540):560–564.
   Google Scholar
• Laslo P, Pongubala JM, Lancki DW, et al. Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin Immunol. 2008;20(4):228–235.
   Google Scholar
• Ziauddin J, Schneider DS. Where does innate immunity stop and adaptive immunity begin? Cell Host Microbe. 2012;12(4):394–395.
   Google Scholar
• Parkin J, Cohen B. An overview of the immune system. Lancet. 2001;357(9270):1777–1789.
   Google Scholar
• Tomar N. De RK A brief outline of the immune system. Methods Mol Biol. 2014;1184(3–12). DOI:10.1007/978-1-4939-1115-8_1
   Google Scholar
• Raggi F, Pelassa S, Pierobon D, et al. Regulation of human macrophage M1-M2 polarization balance by hypoxia and the triggering receptor expressed on myeloid cells-1. Front Immunol. 2017;8(1097). DOI:10.3389/fimmu.2017.01097
   Google Scholar
• Gu X, Zhang Y, Li D, et al. N6-methyladenosine demethylase FTO promotes M1 and M2 macrophage activation. Cell Signal. 2020;69(109553). DOI:10.1016/j.cellsig.2020.109553
   Google Scholar
• Ait-Oufella H, Sage AP, Mallat Z, et al. Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ Res. 2014;114(10):1640–1660.
   Google Scholar
• Granot T, Senda T, Carpenter DJ, et al. Dendritic cells display subset and tissue-specific maturation dynamics over human life. Immunity. 2017;46(3):504–515.
   Google Scholar
• Palomino-Segura M, Perez L, Farsakoglu Y, et al. Protection against influenza infection requires early recognition by inflammatory dendritic cells through C-type lectin receptor SIGN-R1. Nat Microbiol. 2019;4(11):1930–1940.
   Google Scholar
• Saadeh D, Kurban M, Abbas O. Update on the role of plasmacytoid dendritic cells in inflammatory/ autoimmune skin diseases. Exp Dermatol. 2016;25(6):415–421.
   Google Scholar
• Liu J, Zhang X, Chen K, et al. CCR7 chemokine receptor-inducible lnc-Dpf3 restrains dendritic cell migration by inhibiting HIF-1alpha-mediated glycolysis. Immunity. 2019;50(3):600–615.
   Google Scholar
• Poli A, Michel T, Patil N, et al. Revisiting the functional impact of NK cells. Trends Immunol. 2018;39(6):460–472.
   Google Scholar
• Penaloza HF, Alvarez D, Munoz-Durango N, et al. The role of myeloid-derived suppressor cells in chronic infectious diseases and the current methodology available for their study. J Leukoc Biol. 2019;105(5):857–872.
   Google Scholar
• Ko HJ, Lee JM, Kim YJ, et al. Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J Immunol. 2009;182(4):1818–1828.
   Google Scholar
• Hoffman W, Lakkis FG, Chalasani G, et al. Antibodies, and more. Clin J Am Soc Nephrol. 2016;11(1):137–154.
   Google Scholar
• Zheng Z, Zhang L, Cui XL, et al. Control of early B cell development by the RNA N(6)-methyladenosine methylation. Cell Rep. 2020;31(13):107819.
   Google Scholar
• Zhang W, He X, Hu J, et al. Dysregulation of N(6)-methyladenosine regulators predicts poor patient survival in mantle cell lymphoma. Oncol Lett. 2019;18(4):3682–3690.
   Google Scholar
• Takaba H, Takayanagi H. The mechanisms of T cell selection in the thymus. Trends Immunol. 2017;38(11):805–816.
   Google Scholar
• Scully C, Georgakopoulou EA, Hassona Y. The immune system: basis of so much health and disease: 4. immunocytes. Dent Update. 2017;44(5):436–438, 441–442.
   Google Scholar
• Li HB, Tong J, Zhu S, et al. m(6)A mRNA methylation controls T cell homeostasis by targeting the IL-7/STAT5/SOCS pathways. Nature. 2017;548(7667):338–342.
   Google Scholar
• Furlan M, Galeota E, de Pretis S, et al. m6A-dependent RNA dynamics in T cell differentiation. Genes (Basel). 2019;10(1). DOI:10.3390/genes10010028
   Google Scholar
• Gerritsen B, Pandit A. The memory of a killer T cell: models of CD8(+) T cell differentiation. Immunol Cell Biol. 2016;94(3):236–241.
   Google Scholar
• Jurczyszak D, Zhang W, Terry SN, et al. HIV protease cleaves the antiviral m6A reader protein YTHDF3 in the viral particle. Plos Pathog. 2020;16(2):e1008305.
   Google Scholar
• Lu W, Tirumuru N, St GC, et al. N(6)-methyladenosine-binding proteins suppress HIV-1 infectivity and viral production. J Biol Chem. 2018;293(34):12992–13005.
   Google Scholar
• Tong J, Cao G, Zhang T, et al. m(6)A mRNA methylation sustains Treg suppressive functions. Cell Res. 2018;28(2):253–256.
   Google Scholar
• Yu R, Li Q, Feng Z, et al. m6A reader YTHDF2 regulates LPS-induced inflammatory response. Int J Mol Sci. 2019;20(6). DOI:10.3390/ijms20061323
   Google Scholar
• Gokhale NS, McIntyre A, McFadden MJ, et al. N6-methyladenosine in flaviviridae viral RNA genomes regulates infection. Cell Host Microbe. 2016;20(5):654–665.
   Google Scholar
• Cohen J. HIV/AIDS. Dreams meet realities at AIDS conference. Science. 2012;337(6094):509–510.
   Google Scholar
• Lichinchi G, Gao S, Saletore Y, et al. Dynamics of the human and viral m(6)A RNA methylomes during HIV-1 infection of T cells. Nat Microbiol. 2016;1(16011). DOI:10.1038/nmicrobiol.2016.11
   Google Scholar
• Tirumuru N, Zhao BS, Lu W, et al. N(6)-methyladenosine of HIV-1 RNA regulates viral infection and HIV-1 Gag protein expression. Elife. 2016;5. DOI:10.7554/eLife.15528.
   Google Scholar
• Kennedy EM, Bogerd HP, Kornepati A, et al. Posttranscriptional m(6)A editing of HIV-1 mRNAs enhances viral gene expression. Cell Host Microbe. 2017;22(6):830.
   Google Scholar
• Kariko K, Buckstein M, Ni H, et al. Suppression of RNA recognition by toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity. 2005;23(2):165–175.
   Google Scholar
• Repunte-Canonigo V, Lefebvre C, George O, et al. Gene expression changes consistent with neuroAIDS and impaired working memory in HIV-1 transgenic rats. Mol Neurodegener. 2014;9(26). DOI:10.1186/1750-1326-9-26
   Google Scholar
• Sanna PP, Repunte-Canonigo V, Masliah E, et al. Gene expression patterns associated with neurological disease in human HIV infection. Plos One. 2017;12(4):e175316.
   Google Scholar
• Fleming AM, Nguyen N, Burrows CJ. Colocalization of m(6)A and G-quadruplex-forming sequences in viral RNA (HIV, Zika, Hepatitis B, and SV40) suggests topological control of adenosine N (6)-methylation. ACS Cent Sci. 2019;5(2):218–228.
   Google Scholar
• Krug RM, Morgan MA, Shatkin AJ. Influenza viral mRNA contains internal N6-methyladenosine and 5ʹ-terminal 7-methylguanosine in cap structures. J Virol. 1976;20(1):45–53.
   Google Scholar
• Narayan P, Ayers DF, Rottman FM, et al. Unequal distribution of N6-methyladenosine in influenza virus mRNAs. Mol Cell Biol. 1987;7(4):1572–1575.
   Google Scholar
• Courtney DG, Kennedy EM, Dumm RE, et al. Epitranscriptomic enhancement of influenza a virus gene expression and replication. Cell Host Microbe. 2017;22(3):377–386.
   Google Scholar
• Winkler R, Gillis E, Lasman L, et al. m(6)A modification controls the innate immune response to infection by targeting type I interferons. Nat Immunol. 2019;20(2):173–182.
   Google Scholar
• Durbin AF, Wang C, Marcotrigiano J, et al. RNAs containing modified nucleotides fail to trigger RIG-I conformational changes for innate immune signaling. Mbio. 2016;7(5). DOI:10.1128/mBio.00833-16
   Google Scholar
• Horner SM, Gale MJ. Regulation of hepatic innate immunity by hepatitis C virus. Nat Med. 2013;19(7):879–888.
   Google Scholar
• Villordo SM, Filomatori CV, Sanchez-Vargas I, et al. Dengue virus RNA structure specialization facilitates host adaptation. Plos Pathog. 2015;11(1):e1004604.
   Google Scholar
• Lichinchi G, Zhao BS, Wu Y, et al. Dynamics of human and viral RNA methylation during zika virus infection. Cell Host Microbe. 2016;20(5):666–673.
   Google Scholar
• Purushothaman P, Uppal T, Verma SC. Molecular biology of KSHV lytic reactivation. Viruses. 2015;7(1):116–153.
   Google Scholar
• Aneja KK, Yuan Y. Reactivation and lytic replication of Kaposi’s sarcoma-associated herpesvirus: an update. Front Microbiol. 2017;8(613). DOI:10.3389/fmicb.2017.00613
   Google Scholar
• Tan B, Gao SJ. The RNA Epitranscriptome of DNA Viruses. J Virol. 2018;92(22). DOI:10.1128/JVI.00696-18
   Google Scholar
• Hesser CR, Karijolich J, Dominissini D, et al. N6-methyladenosine modification and the YTHDF2 reader protein play cell type specific roles in lytic viral gene expression during Kaposi’s sarcoma-associated herpesvirus infection. Plos Pathog. 2018;14(4):e1006995.
   Google Scholar
• Ye F. RNA N(6)-adenosine methylation (m(6)A) steers epitranscriptomic control of herpesvirus replication. Inflamm Cell Signal. 2017;4:3.
   Google Scholar
• Baquero-Perez B, Antanaviciute A, Yonchev ID, et al. The Tudor SND1 protein is an m(6)A RNA reader essential for replication of Kaposi’s sarcoma-associated herpesvirus. Elife. 2019;8. DOI:10.7554/eLife.47261.
   Google Scholar
• Canaani D, Kahana C, Lavi S, et al. Identification and mapping of N6-methyladenosine containing sequences in simian virus 40 RNA. Nucleic Acids Res. 1979;6(8):2879–2899.
   Google Scholar
• Kahana C, Gidoni D, Canaani D, et al. Simian virus 40 early mRNA’s in lytically infected and transformed cells contain six 5ʹ-terminal caps. J Virol. 1981;37(1):7–16.
   Google Scholar
• Finkel D, Groner Y. Methylations of adenosine residues (m6A) in pre-mRNA are important for formation of late simian virus 40 mRNAs. Virol. 1983;131(2):409–425.
   Google Scholar
• Tsai K, Courtney DG, Cullen BR. Addition of m6A to SV40 late mRNAs enhances viral structural gene expression and replication. Plos Pathog. 2018;14(2):e1006919.
   Google Scholar
• Chen XP, Long X, Jia WL, et al. Viral integration drives multifocal HCC during the occult HBV infection. J Exp Clin Cancer Res. 2019;38(1):261.
   Google Scholar
• Imam H, Khan M, Gokhale NS, et al. N6-methyladenosine modification of hepatitis B virus RNA differentially regulates the viral life cycle. Proc Natl Acad Sci U S A. 2018;115(35):8829–8834.
   Google Scholar
• Imam H, Kim GW, Mir SA, et al. Interferon-stimulated gene 20 (ISG20) selectively degrades N6-methyladenosine modified hepatitis B virus transcripts. Plos Pathog. 2020;16(2):e1008338.
   Google Scholar
• Liu J, Eckert MA, Harada BT, et al. m(6)A mRNA methylation regulates AKT activity to promote the proliferation and tumorigenicity of endometrial cancer. Nat Cell Biol. 2018;20(9):1074–1083.
   Google Scholar
• Wang Q, Chen C, Ding Q, et al. METTL3-mediated m(6)A modification of HDGF mRNA promotes gastric cancer progression and has prognostic significance. Gut. 2019. DOI:10.1136/gutjnl-2019-319639
   Google Scholar
• Huang H, Weng H, Chen J. m(6)a modification in coding and non-coding RNAs: roles and therapeutic implications in cancer. Cancer Cell. 2020;37(3):270–288.
   Google Scholar
• Su R, Dong L, Li C, et al. R-2HG exhibits anti-tumor activity by targeting FTO/m(6)A/MYC/CEBPA signaling. Cell. 2018;172(90–105):1–2.
   Google Scholar
• Su R, Dong L, Li Y, et al. Targeting FTO suppresses cancer stem cell maintenance and immune evasion. Cancer Cell. 2020;38(1):79–96.
   Google Scholar
• Chen YG, Chen R, Ahmad S, et al. N6-methyladenosine modification controls circular RNA immunity. Mol Cell. 2019;76(1):96–109.
   Google Scholar
• Gubin MM, Artyomov MN, Mardis ER, et al. Tumor neoantigens: building a framework for personalized cancer immunotherapy. J Clin Invest. 2015;125(9):3413–3421.
   Google Scholar
• Li N, Kang Y, Wang L, et al. ALKBH5 regulates anti-PD-1 therapy response by modulating lactate and suppressive immune cell accumulation in tumor microenvironment. Proc Natl Acad Sci U S A. 2020;117(33):20159–20170.
   Google Scholar
• Shen C, Sheng Y, Zhu AC, et al. RNA demethylase ALKBH5 selectively promotes tumorigenesis and cancer stem cell self-renewal in acute myeloid leukemia. Cell Stem Cell. 2020;27(1):64–80.
   Google Scholar
• Xu F, Zhang H, Chen J, et al. Immune signature of T follicular helper cells predicts clinical prognostic and therapeutic impact in lung squamous cell carcinoma. Int Immunopharmacol. 2020;81(105932). DOI:10.1016/j.intimp.2019.105932
   Google Scholar
• Motorin Y, Helm M. Methods for RNA modification mapping using deep sequencing: established and new emerging technologies. Genes (Basel). 2019;10(1). DOI:10.3390/genes10010035
   Google Scholar
• Bader JP, Brown NR, Chiang PK, et al. 3-Deazaadenosine, an inhibitor of adenosylhomocysteine hydrolase, inhibits reproduction of Rous sarcoma virus and transformation of chick embryo cells. Virol. 1978;89(2):494–505.
   Google Scholar