Title: Cytosine drives evolution of <scp>SARS‐CoV‐2</scp>
Abstract: Environmental MicrobiologyVolume 22, Issue 6 p. 1977-1985 Hypothesis Cytosine drives evolution of SARS-CoV-2 Antoine Danchin, Corresponding Author Antoine Danchin [email protected] orcid.org/0000-0002-6350-5001 Kodikos Labs, 24 rue Jean Baldassini, 69007 Lyon/Institut Cochin, 75013 Paris, FranceFor correspondence. E-mail [email protected], Tel. +331 4441 2551, Fax +331 4441 2559Search for more papers by this authorPhilippe Marlière, Philippe Marlière TESSSI, The European Syndicate of Synthetic Scientists and Industrialists, 81 rue Réaumur, 75002, Paris, FranceSearch for more papers by this author Antoine Danchin, Corresponding Author Antoine Danchin [email protected] orcid.org/0000-0002-6350-5001 Kodikos Labs, 24 rue Jean Baldassini, 69007 Lyon/Institut Cochin, 75013 Paris, FranceFor correspondence. E-mail [email protected], Tel. +331 4441 2551, Fax +331 4441 2559Search for more papers by this authorPhilippe Marlière, Philippe Marlière TESSSI, The European Syndicate of Synthetic Scientists and Industrialists, 81 rue Réaumur, 75002, Paris, FranceSearch for more papers by this author First published: 14 April 2020 https://doi.org/10.1111/1462-2920.15025Citations: 26Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References Arribas, M., Aguirre, J., Manrubia, S., and Lázaro, E. (2018) Differences in adaptive dynamics determine the success of virus variants that propagate together. Virus Evol 4: vex043. 10.1093/ve/vex043 PubMedWeb of Science®Google Scholar Aurrecoechea, C., Brestelli, J., Brunk, B.P., Carlton, J.M., Dommer, J., Fischer, S., et al. (2009) GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res 37: D526–D530. 10.1093/nar/gkn631 CASPubMedWeb of Science®Google Scholar Balendiran, G.K., Molina, J.A., Xu, Y., Torres-Martinez, J., Stevens, R., Focia, P.J., et al. (1999) Ternary complex structure of human HGPRTase, pRpp, Mg2+, and the inhibitor HPP reveals the involvement of the flexible loop in substrate binding. Protein Sci 8: 1023–1031. 10.1110/ps.8.5.1023 CASPubMedWeb of Science®Google Scholar Bermingham, A., Chand, M.A., Brown, C.S., Aarons, E., Tong, C., Langrish, C., et al. (2012) Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill 17: 20290. 10.2807/ese.17.40.20290-en CASPubMedWeb of Science®Google Scholar Bohnsack, K.E., Höbartner, C., and Bohnsack, M.T. (2019) Eukaryotic 5-methylcytosine (m5C) RNA methyltransferases: mechanisms, cellular functions, and links to disease. Genes (Basel) 10: E102. 10.3390/genes10020102 CASPubMedWeb of Science®Google Scholar Chauhan, N., Farine, L., Pandey, K., Menon, A.K., and Bütikofer, P. (2016) Lipid topogenesis—35 years on. Biochim Biophys Acta 1861: 757–766. 10.1016/j.bbalip.2016.02.025 CASPubMedWeb of Science®Google Scholar Chen, S.-C., and Olsthoorn, R.C.L. (2010) Group-specific structural features of the 5′-proximal sequences of coronavirus genomic RNAs. Virology 401: 29–41. 10.1016/j.virol.2010.02.007 CASPubMedWeb of Science®Google Scholar Chen, Y., Liu, Q., and Guo, D. (2020) Emerging coronaviruses: genome structure, replication, and pathogenesis. J Med Virol 92: 418–423. 10.1002/jmv.25681 CASPubMedWeb of Science®Google Scholar Cheng, M.-L., Chien, K.-Y., Lai, C.-H., Li, G.-J., Lin, J.-F., and Ho, H.-Y. (2020) Metabolic reprogramming of host cells in response to enteroviral infection. Cell 9: E473. 10.3390/cells9020473 CASPubMedWeb of Science®Google Scholar Chin, K.C., and Cresswell, P. (2001) Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci U S A 98: 15125–15130. 10.1073/pnas.011593298 CASPubMedWeb of Science®Google Scholar Choy, P.C., Paddon, H.B., and Vance, D.E. (1980) An increase in cytoplasmic CTP accelerates the reaction catalyzed by CTP:phosphocholine cytidylyltransferase in poliovirus-infected HeLa cells. J Biol Chem 255: 1070–1073. CASPubMedWeb of Science®Google Scholar Cornell, R.B., and Ridgway, N.D. (2015) CTP:phosphocholine cytidylyltransferase: function, regulation, and structure of an amphitropic enzyme required for membrane biogenesis. Prog Lipid Res 59: 147–171. 10.1016/j.plipres.2015.07.001 CASPubMedWeb of Science®Google Scholar Del Caño-Ochoa, F., and Ramón-Maiques, S. (2020) The multienzymatic protein CAD leading the de novo biosynthesis of pyrimidines localizes exclusively in the cytoplasm and does not translocate to the nucleus. Nucleosides Nucleotides Nucleic Acids. https://doi.org/10.1080/15257770.2019.1706743. PubMedWeb of Science®Google Scholar Dev, R.R., Ganji, R., Singh, S.P., Mahalingam, S., Banerjee, S., and Khosla, S. (2017) Cytosine methylation by DNMT2 facilitates stability and survival of HIV-1 RNA in the host cell during infection. Biochem J 474: 2009–2026. 10.1042/BCJ20170258 CASPubMedWeb of Science®Google Scholar Di Conza, G., and Ho, P.-C. (2020) ER stress responses: an emerging modulator for innate immunity. Cell 9: E695. 10.3390/cells9030695 CASPubMedWeb of Science®Google Scholar Du, Y.-X., and Chen, X.-P. (2020) Favipiravir: pharmacokinetics and concerns about clinical trials for 2019-nCoV infection. Clin Pharmacol Ther (in press). https://doi.org/10.1002/cpt.1844. 10.1002/cpt.1844 PubMedWeb of Science®Google Scholar Dukhovny, A., Shlomai, A., and Sklan, E.H. (2018) The antiviral protein Viperin suppresses T7 promoter dependent RNA synthesis-possible implications for its antiviral activity. Sci Rep 8: 8100. 10.1038/s41598-018-26516-z PubMedWeb of Science®Google Scholar Durdevic, Z., Hanna, K., Gold, B., Pollex, T., Cherry, S., Lyko, F., and Schaefer, M. (2013) Efficient RNA virus control in drosophila requires the RNA methyltransferase Dnmt2. EMBO Rep 14: 269–275. 10.1038/embor.2013.3 CASPubMedWeb of Science®Google Scholar Duschene, K.S., and Broderick, J.B. (2010) The antiviral protein viperin is a radical SAM enzyme. FEBS Lett 584: 1263–1267. 10.1016/j.febslet.2010.02.041 CASPubMedWeb of Science®Google Scholar Ebrahimi, K.H., Howie, D., Rowbotham, J., McCullagh, J., Armstrong, F., and James, W.S. (2020) Viperin, through its radical-SAM activity, depletes cellular nucleotide pools and interferes with mitochondrial metabolism to inhibit viral replication. FEBS Lett (in press). https://doi.org/10.1002/1873-3468.13761. 10.1002/1873-3468.13761 PubMedWeb of Science®Google Scholar Fang, J., Wang, H., Bai, J., Zhang, Q., Li, Y., Liu, F., and Jiang, P. (2016) Monkey viperin restricts porcine reproductive and respiratory syndrome virus replication. PLoS One 11: e0156513. 10.1371/journal.pone.0156513 PubMedWeb of Science®Google Scholar Ficarelli, M., Antzin-Anduetza, I., Hugh-White, R., Firth, A.E., Sertkaya, H., Wilson, H., et al. (2020) CpG dinucleotides inhibit HIV-1 replication through zinc finger antiviral protein (ZAP)-dependent and -independent mechanisms. J Virol 94: e01337-19. 10.1128/JVI.01337-19 PubMedWeb of Science®Google Scholar Forsdyke, D.R., and Mortimer, J.R. (2000) Chargaff's legacy. Gene 261: 127–137. 10.1016/S0378-1119(00)00472-8 CASPubMedWeb of Science®Google Scholar Furusho, K., Shibata, T., Sato, R., Fukui, R., Motoi, Y., Zhang, Y., et al. (2019) Cytidine deaminase enables toll-like receptor 8 activation by cytidine or its analogs. Int Immunol 31: 167–173. 10.1093/intimm/dxy075 CASPubMedWeb of Science®Google Scholar Furuta, Y., Komeno, T., and Nakamura, T. (2017) Favipiravir (T-705), a broad spectrum inhibitor of viral RNA polymerase. Proc Jpn Acad Ser B Phys Biol Sci 93: 449–463. 10.2183/pjab.93.027 CASPubMedWeb of Science®Google Scholar Gizzi, A.S., Grove, T.L., Arnold, J.J., Jose, J., Jangra, R.K., Garforth, S.J., et al. (2018) A naturally occurring antiviral ribonucleotide encoded by the human genome. Nature 558: 610–614. 10.1038/s41586-018-0238-4 CASPubMedWeb of Science®Google Scholar Green, T.J., Benkendorff, K., Robinson, N., Raftos, D., and Speck, P. (2014) Anti-viral gene induction is absent upon secondary challenge with double-stranded RNA in the Pacific oyster, Crassostrea gigas. Fish Shellfish Immunol 39: 492–497. 10.1016/j.fsi.2014.06.010 CASPubMedWeb of Science®Google Scholar Huang, M., Kozlowski, P., Collins, M., Wang, Y., Haystead, T.A., and Graves, L.M. (2002) Caspase-dependent cleavage of carbamoyl phosphate synthetase II during apoptosis. Mol Pharmacol 61: 569–577. 10.1124/mol.61.3.569 CASPubMedWeb of Science®Google Scholar Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., et al. (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395: 497–506. 10.1016/S0140-6736(20)30183-5 CASPubMedWeb of Science®Google Scholar Hutchison, C.A., Chuang, R.-Y., Noskov, V.N., Assad-Garcia, N., Deerinck, T.J., Ellisman, M.H., et al. (2016) Design and synthesis of a minimal bacterial genome. Science 351: aad6253. 10.1126/science.aad6253 CASPubMedWeb of Science®Google Scholar Jee, Y. (2020) WHO international health regulations emergency committee for the COVID-19 outbreak. Epidemiol Health 42: e2020013. 10.4178/epih.e2020013 CASPubMedWeb of Science®Google Scholar Kaiser, S., Jurkowski, T.P., Kellner, S., Schneider, D., Jeltsch, A., and Helm, M. (2017) The RNA methyltransferase Dnmt2 methylates DNA in the structural context of a tRNA. RNA Biol 14: 1241–1251. 10.1080/15476286.2016.1236170 PubMedWeb of Science®Google Scholar Kuo, L., Koetzner, C.A., and Masters, P.S. (2016) A key role for the carboxy-terminal tail of the murine coronavirus nucleocapsid protein in coordination of genome packaging. Virology 494: 100–107. 10.1016/j.virol.2016.04.009 CASPubMedWeb of Science®Google Scholar Kutnjak, D., Elena, S.F., and Ravnikar, M. (2017) Time-sampled population sequencing reveals the interplay of selection and genetic drift in experimental evolution of potato virus Y. J Virol 91: e00690-17. 10.1128/JVI.00690-17 PubMedWeb of Science®Google Scholar Lagace, T.A., and Ridgway, N.D. (2013) The role of phospholipids in the biological activity and structure of the endoplasmic reticulum. Biochim Biophys Acta 1833: 2499–2510. 10.1016/j.bbamcr.2013.05.018 CASPubMedWeb of Science®Google Scholar Lee, J., and Ridgway, N.D. (2020) Substrate channeling in the glycerol-3-phosphate pathway regulates the synthesis, storage and secretion of glycerolipids. Biochim Biophys Acta Mol Cell Biol Lipids 1865: 158438. 10.1016/j.bbalip.2019.03.010 CASPubMedWeb of Science®Google Scholar Li, J., Huang, S., Chen, J., Yang, Z., Fei, X., Zheng, M., et al. (2007) Identification and characterization of human uracil phosphoribosyltransferase (UPRTase). J Hum Genet 52: 415–422. 10.1007/s10038-007-0129-2 CASPubMedWeb of Science®Google Scholar Li, Y., Surya, W., Claudine, S., and Torres, J. (2014) Structure of a conserved Golgi complex-targeting signal in coronavirus envelope proteins. J Biol Chem 289: 12535–12549. 10.1074/jbc.M114.560094 CASPubMedWeb of Science®Google Scholar Li, H., Ye, F., Ren, J.-Y., Wang, P.-Y., Du, L.-L., and Liu, J.-L. (2018) Active transport of cytoophidia in Schizosaccharomyces pombe. FASEB J 32: 5891–5898. 10.1096/fj.201800045RR CASPubMedWeb of Science®Google Scholar Li, X., Zai, J., Zhao, Q., Nie, Q., Li, Y., Foley, B.T., and Chaillon, A. (2020) Evolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2. J Med Virol (in press). https://doi.org/10.1002/jmv.25731 10.1002/jmv.25731 Web of Science®Google Scholar Liu, J.-L. (2010) Intracellular compartmentation of CTP synthase in drosophila. J Genet Genomics 37: 281–296. 10.1016/S1673-8527(09)60046-1 CASPubMedWeb of Science®Google Scholar Luo, X., Wang, X., Gao, Y., Zhu, J., Liu, S., Gao, G., and Gao, P. (2020) Molecular mechanism of RNA recognition by zinc-finger antiviral protein. Cell Rep 30: 46–52 e4. 10.1016/j.celrep.2019.11.116 CASPubMedWeb of Science®Google Scholar Mayer, K.A., Stöckl, J., Zlabinger, G.J., and Gualdoni, G.A. (2019) Hijacking the supplies: metabolism as a novel facet of virus-host interaction. Front Immunol 10: 1533. 10.3389/fimmu.2019.01533 CASPubMedWeb of Science®Google Scholar McMaster, C.R. (2018) From yeast to humans - roles of the Kennedy pathway for phosphatidylcholine synthesis. FEBS Lett 592: 1256–1272. 10.1002/1873-3468.12919 CASPubMedWeb of Science®Google Scholar Orton, R.J., Wright, C.F., King, D.P., and Haydon, D.T. (2020) Estimating viral bottleneck sizes for FMDV transmission within and between hosts and implications for the rate of viral evolution. Interface Focus 10: 20190066. 10.1098/rsfs.2019.0066 PubMedWeb of Science®Google Scholar Park, M., Cook, A.R., Lim, J.T., Sun, Y., and Dickens, B.L. (2020) A systematic review of COVID-19 epidemiology based on current evidence. J Clin Med 9: E967. 10.3390/jcm9040967 CASPubMedWeb of Science®Google Scholar Sawicki, S.G., Sawicki, D.L., and Siddell, S.G. (2007) A contemporary view of coronavirus transcription. J Virol 81: 20–29. 10.1128/JVI.01358-06 CASPubMedWeb of Science®Google Scholar Schilling, C.H., Edwards, J.S., and Palsson, B.O. (1999) Toward metabolic phenomics: analysis of genomic data using flux balances. Biotechnol Prog 15: 288–295. 10.1021/bp9900357 CASPubMedWeb of Science®Google Scholar Seo, J.-Y., and Cresswell, P. (2013) Viperin regulates cellular lipid metabolism during human cytomegalovirus infection. PLoS Pathog 9: e1003497. 10.1371/journal.ppat.1003497 CASPubMedWeb of Science®Google Scholar Sexton, N.R., Smith, E.C., Blanc, H., Vignuzzi, M., Peersen, O.B., and Denison, M.R. (2016) Homology-based identification of a mutation in the coronavirus RNA-dependent RNA polymerase that confers resistance to multiple mutagens. J Virol 90: 7415–7428. 10.1128/JVI.00080-16 CASPubMedWeb of Science®Google Scholar Sheahan, T.P., Sims, A.C., Zhou, S., Graham, R.L., Pruijssers, A.J., Agostini, M.L., et al. (2020) An orally bioavailable broad-spectrum antiviral inhibits SARS-CoV-2 in human airway epithelial cell cultures and multiple coronaviruses in mice. Sci Transl Med 06 Apr 2020: eabb5883. Google Scholar Sledziewska, E., and Janion, C. (1980) Mutagenic specificity of N4-hydroxycytidine. Mutat Res 70: 11–16. 10.1016/0027-5107(80)90053-6 CASPubMedWeb of Science®Google Scholar Song, H.-D., Tu, C.-C., Zhang, G.-W., Wang, S.-Y., Zheng, K., Lei, L.-C., et al. (2005) Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci U S A 102: 2430–2435. 10.1073/pnas.0409608102 CASPubMedWeb of Science®Google Scholar Sun, Z., and Liu, J.-L. (2019) mTOR-S6K1 pathway mediates cytoophidium assembly. J Genet Genomics 46: 65–74. 10.1016/j.jgg.2018.11.006 PubMedWeb of Science®Google Scholar Tanaka, Y., Inoue, A., Mizunuma, T., Matsumura, H., Yokomori, H., Komiyama, T., and Otori, K. (2019) Tolerability of erythrocyte ribavirin triphosphate concentrations depends on the ITPA genotype. Ther Drug Monit 41: 497–502. 10.1097/FTD.0000000000000626 CASPubMedWeb of Science®Google Scholar Thiagarajan, D., Dev, R.R., and Khosla, S. (2011) The DNA methyltranferase Dnmt2 participates in RNA processing during cellular stress. Epigenetics 6: 103–113. 10.4161/epi.6.1.13418 CASPubMedWeb of Science®Google Scholar Traut, T.W. (1994) Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140: 1–22. 10.1007/BF00928361 CASPubMedWeb of Science®Google Scholar Turinici, G., and Danchin, A. (2007) The SARS case study: an alarm clock? In Encyclopedia of Infectious Diseases, M. Tibayrenc (ed). Hoboken, NJ: John Wiley & Sons, Inc., pp. 151–162. 10.1002/9780470114209.ch9 Google Scholar Udugama, B., Kadhiresan, P., Kozlowski, H.N., Malekjahani, A., Osborne, M., Li, V.Y.C., et al. (2020) Diagnosing COVID-19: the disease and tools for detection. ACS Nano (in press). https://doi.org/10.1021/acsnano.0c02624 10.1021/acsnano.0c02624 PubMedWeb of Science®Google Scholar Wei, C., Zheng, C., Sun, J., Luo, D., Tang, Y., Zhang, Y., et al. (2018) Viperin inhibits enterovirus A71 replication by interacting with viral 2C protein. Viruses 11: E13. 10.3390/v11010013 PubMedGoogle Scholar Wellen, K.E., and Thompson, C.B. (2012) A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol 13: 270–276. 10.1038/nrm3305 CASPubMedWeb of Science®Google Scholar Wilson, J.M., O'Toole, T.E., Argos, P., Shewach, D.S., Daddona, P.E., and Kelley, W.N. (1986) Human adenine phosphoribosyltransferase. Complete amino acid sequence of the erythrocyte enzyme. J Biol Chem 261: 13677–13683. CASPubMedWeb of Science®Google Scholar Woods, P.S., Doolittle, L.M., Rosas, L.E., Joseph, L.M., Calomeni, E.P., and Davis, I.C. (2016) Lethal H1N1 influenza a virus infection alters the murine alveolar type II cell surfactant lipidome. Am J Physiol Lung Cell Mol Physiol 311: L1160–L1169. 10.1152/ajplung.00339.2016 PubMedWeb of Science®Google Scholar Zhang, Y., Burke, C.W., Ryman, K.D., and Klimstra, W.B. (2007) Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J Virol 81: 11246–11255. 10.1128/JVI.01282-07 CASPubMedWeb of Science®Google Scholar Zhang, Y., Morar, M., and Ealick, S.E. (2008) Structural biology of the purine biosynthetic pathway. Cell Mol Life Sci 65: 3699–3724. 10.1007/s00018-008-8295-8 CASPubMedWeb of Science®Google Scholar Zhang, J., Zeng, H., Gu, J., Li, H., Zheng, L., and Zou, Q. (2020) Progress and prospects on vaccine development against SARS-CoV-2. Vaccines (Basel) 8: E153. 10.3390/vaccines8020153 CASPubMedWeb of Science®Google Scholar Zheng, Y., and Kielian, M. (2013) Imaging of the alphavirus capsid protein during virus replication. J Virol 87: 9579–9589. 10.1128/JVI.01299-13 CASPubMedWeb of Science®Google Scholar Zhu, Z., Chen, M., Abernathy, E., Icenogle, J., Zhou, S., Wang, C., et al. (2016) Analysis of complete genomes of the rubella virus genotypes 1E and 2B which circulated in China, 2000–2013. Sci Rep 6: 39025. 10.1038/srep39025 CASPubMedWeb of Science®Google Scholar Zhu, M., Zhou, J., Liang, Y., Nair, V., Yao, Y., and Cheng, Z. (2020) CCCH-type zinc finger antiviral protein mediates antiviral immune response by activating T cells. J Leukoc Biol 107: 299–307. 10.1002/JLB.1AB1119-314RRR CASPubMedWeb of Science®Google Scholar Citing Literature Volume22, Issue6June 2020Pages 1977-1985 ReferencesRelatedInformation