{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T07:18:14Z","timestamp":1789197494368,"version":"build-2803163510"},"reference-count":62,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2020,10,5]],"date-time":"2020-10-05T00:00:00Z","timestamp":1601856000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,10,5]],"date-time":"2020-10-05T00:00:00Z","timestamp":1601856000000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,10,5]],"date-time":"2020-10-05T00:00:00Z","timestamp":1601856000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01GM093278"],"award-info":[{"award-number":["R01GM093278"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01GM119386"],"award-info":[{"award-number":["R01GM119386"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["MCB-1915843"],"award-info":[{"award-number":["MCB-1915843"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>\n                    Modifications in the tRNA anticodon loop, adjacent to the three-nucleotide anticodon, influence translation fidelity by stabilizing the tRNA to allow for accurate reading of the mRNA genetic code. One example is the N1-methylguanosine modification at guanine nucleotide 37 (m\n                    <jats:sup>1<\/jats:sup>\n                    G37) located in the anticodon loop andimmediately adjacent to the anticodon nucleotides 34, 35, 36. The absence of m\n                    <jats:sup>1<\/jats:sup>\n                    G37 in tRNA\n                    <jats:sup>Pro<\/jats:sup>\n                    causes +1 frameshifting on polynucleotide, slippery codons. Here, we report structures of the bacterial ribosome containing tRNA\n                    <jats:sup>Pro<\/jats:sup>\n                    bound to either cognate or slippery codons to determine how the m\n                    <jats:sup>1<\/jats:sup>\n                    G37 modification prevents mRNA frameshifting. The structures reveal that certain codon\u2013anticodon contexts and the lack of m\n                    <jats:sup>1<\/jats:sup>\n                    G37 destabilize interactions of tRNA\n                    <jats:sup>Pro<\/jats:sup>\n                    with the P site of the ribosome, causing large conformational changes typically only seen during EF-G-mediated translocation of the mRNA-tRNA pairs. These studies provide molecular insights into how m\n                    <jats:sup>1<\/jats:sup>\n                    G37 stabilizes the interactions of tRNA\n                    <jats:sup>Pro<\/jats:sup>\n                    with the ribosome in the context of a slippery mRNA codon.\n                  <\/jats:p>","DOI":"10.7554\/elife.51898","type":"journal-article","created":{"date-parts":[[2020,10,5]],"date-time":"2020-10-05T08:00:48Z","timestamp":1601884848000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.51898","source":"Crossref","is-referenced-by-count":45,"title":["Structural insights into mRNA reading frame regulation by tRNA modification and slippery codon\u2013anticodon pairing"],"prefix":"10.7554","volume":"9","author":[{"given":"Eric D","family":"Hoffer","sequence":"first","affiliation":[{"name":"Department of Biochemistry, Emory University School of Medicine, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samuel","family":"Hong","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Emory University School of Medicine, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S","family":"Sunita","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Emory University School of Medicine, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tatsuya","family":"Maehigashi","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Emory University School of Medicine, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1344-5581","authenticated-orcid":true,"suffix":"Jnr","given":"Ruben L","family":"Gonzalez","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Columbia University, New York, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul C","family":"Whitford","sequence":"additional","affiliation":[{"name":"Department of Physics, Northeastern University, Boston, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8821-688X","authenticated-orcid":true,"given":"Christine M","family":"Dunham","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Emory University School of Medicine, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2020,10,5]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"1624","DOI":"10.1261\/rna.2118105","article-title":"Contribution of 16S rRNA nucleotides forming the 30S subunit A and P sites to translation in Escherichia coli","volume":"11","author":"Abdi","year":"2005","journal-title":"RNA"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1107\/S0907444909052925","article-title":"PHENIX : a comprehensive Python-based system for macromolecular structure solution","volume":"66","author":"Adams","year":"2010","journal-title":"Acta Crystallographica Section D Biological Crystallography"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/bs.enz.2017.03.005","article-title":"The importance of being modified: the role of RNA modifications in translational fidelity","volume":"41","author":"Agris","year":"2017","journal-title":"The Enzymes"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1080\/15476286.2017.1356562","article-title":"Celebrating wobble decoding: half a century and still much is new","volume":"15","author":"Agris","year":"2018","journal-title":"RNA Biology"},{"key":"bib5","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkw530","article-title":"Ribosomal frameshifting and transcriptional slippage: from genetic steganography and cryptography to adventitious use","volume":"243","author":"Atkins","year":"2016","journal-title":"Nucleic Acids Research"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1038\/nsmb.3193","article-title":"Choreography of molecular movements during ribosome progression along mRNA","volume":"23","author":"Belardinelli","year":"2016","journal-title":"Nature Structural & Molecular Biology"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1080\/15476286.2016.1240140","article-title":"Translocation as continuous movement through the ribosome","volume":"13","author":"Belardinelli","year":"2016","journal-title":"RNA Biology"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"986","DOI":"10.1126\/science.2471265","article-title":"Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine","volume":"244","author":"Bj\u00f6rk","year":"1989","journal-title":"Science"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"D303","DOI":"10.1093\/nar\/gkx1030","article-title":"MODOMICS: a database of RNA modification pathways. 2017 update","volume":"46","author":"Boccaletto","year":"2018","journal-title":"Nucleic Acids Research"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/B978-0-12-386497-0.00004-9","article-title":"Control of gene expression by translational recoding","volume":"86","author":"Dinman","year":"2012","journal-title":"Advances in Protein Chemistry and Structural Biology"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1126\/science.1202692","article-title":"Structures of the bacterial ribosome in classical and hybrid states of tRNA binding","volume":"332","author":"Dunkle","year":"2011","journal-title":"Science"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.biochi.2015.02.007","article-title":"Mechanisms of mRNA frame maintenance and its subversion during translation of the genetic code","volume":"114","author":"Dunkle","year":"2015","journal-title":"Biochimie"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1107\/S0907444910007493","article-title":"Features and development of coot","volume":"66","author":"Emsley","year":"2010","journal-title":"Acta Crystallographica"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1038\/nsmb.2011","article-title":"mRNA translocation occurs during the second step of ribosomal intersubunit rotation","volume":"18","author":"Ermolenko","year":"2011","journal-title":"Nature Structural & Molecular Biology"},{"key":"bib15","doi-asserted-by":"publisher","first-page":"1944","DOI":"10.1261\/rna.046953.114","article-title":"Structural insights into translational recoding by frameshift suppressor tRNASufJ","volume":"20","author":"Fagan","year":"2014","journal-title":"RNA"},{"key":"bib16","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms8226","article-title":"Maintenance of protein synthesis reading frame by EF-P and m(1)G37-tRNA","volume":"6","author":"Gamper","year":"2015","journal-title":"Nature Communications"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"14866","DOI":"10.3390\/ijms160714866","article-title":"The UGG isoacceptor of tRNAPro is naturally prone to frameshifts","volume":"16","author":"Gamper","year":"2015","journal-title":"International Journal of Molecular Sciences"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"694","DOI":"10.1126\/science.1179709","article-title":"The structure of the ribosome with elongation factor G trapped in the posttranslocational state","volume":"326","author":"Gao","year":"2009","journal-title":"Science"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/0022-2836(76)90214-x","article-title":"Studies of the complex between transfer RNAs with complementary anticodons. I. origins of enhanced affinity between complementary triplets","volume":"103","author":"Grosjean","year":"1976","journal-title":"Journal of Molecular Biology"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"20391","DOI":"10.1073\/pnas.1218999109","article-title":"Rotation of the head of the 30S ribosomal subunit during mRNA translocation","volume":"109","author":"Guo","year":"2012","journal-title":"PNAS"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.mib.2008.02.003","article-title":"tRNA's modifications bring order to gene expression","volume":"11","author":"Gustilo","year":"2008","journal-title":"Current Opinion in Microbiology"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"756","DOI":"10.1006\/jmbi.1993.1429","article-title":"Deficiency of 1-methylguanosine in tRNA from Salmonella typhimurium induces frameshifting by quadruplet translocation","volume":"232","author":"Hagervall","year":"1993","journal-title":"Journal of Molecular Biology"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"1073","DOI":"10.1002\/embj.201387465","article-title":"GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits","volume":"33","author":"Holtkamp","year":"2014","journal-title":"The EMBO Journal"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"11226","DOI":"10.1073\/pnas.1809319115","article-title":"Mechanism of tRNA-mediated +1 ribosomal frameshifting","volume":"115","author":"Hong","year":"2018","journal-title":"PNAS"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1016\/j.molcel.2017.10.014","article-title":"Structural basis for Polyproline-Mediated ribosome stalling and rescue by the translation elongation factor EF-P","volume":"68","author":"Huter","year":"2017","journal-title":"Molecular Cell"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1038\/nsmb.1790","article-title":"Structural aspects of messenger RNA reading frame maintenance by the ribosome","volume":"17","author":"Jenner","year":"2010","journal-title":"Nature Structural & Molecular Biology"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1107\/S0907444909047337","article-title":"Xds","volume":"66","author":"Kabsch","year":"2010","journal-title":"Acta Crystallographica"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"1468","DOI":"10.1002\/1873-3468.13478","article-title":"Mechanisms and biomedical implications of -1 programmed ribosome frameshifting on viral and bacterial mRNAs","volume":"593","author":"Korniy","year":"2019","journal-title":"FEBS Letters"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1006\/jmbi.1997.1176","article-title":"Three modified nucleosides present in the anticodon stem and loop influence the in vivo aa-tRNA selection in a tRNA-dependent manner","volume":"271","author":"Li","year":"1997","journal-title":"Journal of Molecular Biology"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"1619","DOI":"10.4161\/15476286.2014.992273","article-title":"Distribution and frequencies of post-transcriptional modifications in tRNAs","volume":"11","author":"Machnicka","year":"2014","journal-title":"RNA Biology"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"12740","DOI":"10.1073\/pnas.1409436111","article-title":"Structural insights into +1 frameshifting promoted by expanded or modification-deficient anticodon stem loops","volume":"111","author":"Maehigashi","year":"2014","journal-title":"PNAS"},{"key":"bib32","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gky013","article-title":"Selective terminal methylation of a tRNA wobble base","volume":"46","author":"Masuda","year":"2018","journal-title":"Nucleic Acids Research"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"13325","DOI":"10.1073\/pnas.1413731111","article-title":"Molecular mechanics of 30S subunit head rotation","volume":"111","author":"Mohan","year":"2014","journal-title":"PNAS"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"1186","DOI":"10.1038\/nsmb861","article-title":"The role of modifications in Codon discrimination by tRNALysUUU","volume":"11","author":"Murphy","year":"2004","journal-title":"Nature Structural & Molecular Biology"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"1662","DOI":"10.1261\/rna.7106404","article-title":"The modified wobble nucleoside uridine-5-oxyacetic acid in tRNAPro(cmo5UGG) promotes reading of all four proline codons in vivo","volume":"10","author":"Nasvall","year":"2004","journal-title":"RNA"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"5281","DOI":"10.1074\/jbc.RA119.007410","article-title":"Importance of a tRNA anticodon loop modification and a conserved, noncanonical anticodon stem pairing in tRNA CGGPro for decoding","volume":"294","author":"Nguyen","year":"2019","journal-title":"Journal of Biological Chemistry"},{"key":"bib37","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms10586","article-title":"Steric interactions lead to collective tilting motion in the ribosome during mRNA-tRNA translocation","volume":"7","author":"Nguyen","year":"2016","journal-title":"Nature Communications"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1093\/nar\/30.3.759","article-title":"Imbalance of tRNA(Pro) isoacceptors induces +1 frameshifting at near-cognate codons","volume":"30","author":"O'Connor","year":"2002","journal-title":"Nucleic Acids Research"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1016\/S0092-8674(02)01086-3","article-title":"Selection of tRNA by the ribosome requires a transition from an open to a closed form","volume":"111","author":"Ogle","year":"2002","journal-title":"Cell"},{"key":"bib40","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.aax8030","article-title":"Active role of elongation factor G in maintaining the mRNA reading frame during translation","volume":"5","author":"Peng","year":"2019","journal-title":"Science Advances"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1016\/j.jmb.2006.05.016","article-title":"Translocation of a tRNA with an extended anticodon through the ribosome","volume":"360","author":"Phelps","year":"2006","journal-title":"Journal of Molecular Biology"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/S1097-2765(00)80048-9","article-title":"A new model for phenotypic suppression of frameshift mutations by mutant tRNAs","volume":"1","author":"Qian","year":"1998","journal-title":"Molecular Cell"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1038\/nature09547","article-title":"Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites","volume":"468","author":"Ratje","year":"2010","journal-title":"Nature"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1038\/385037a0","article-title":"Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome","volume":"385","author":"Rodnina","year":"1997","journal-title":"Nature"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1006\/jmbi.2000.3886","article-title":"Role of domains 4 and 5 in elongation factor G functions on the ribosome","volume":"300","author":"Savelsbergh","year":"2000","journal-title":"Journal of Molecular Biology"},{"key":"bib46","article-title":"Schrodinger","author":"Schrodinger LLC","year":"2010","unstructured":"Schrodinger LLC. 2010. Schrodinger. LLC."},{"key":"bib47","doi-asserted-by":"publisher","first-page":"1935","DOI":"10.1126\/science.1131127","article-title":"Structure of the 70S ribosome complexed with mRNA and tRNA","volume":"313","author":"Selmer","year":"2006","journal-title":"Science"},{"key":"bib48","first-page":"1671","article-title":"Chemical and enzymatic synthesis of tRNAs for high-throughput crystallization","volume":"7","author":"Sherlin","year":"2001","journal-title":"RNA"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"3463","DOI":"10.1093\/nar\/20.13.3463","article-title":"Insertion (sufB) in the anticodon loop or base substitution (sufC) in the anticodon stem of tRNA(Pro)2 from Salmonella typhimurium induces suppression of frameshift mutations","volume":"20","author":"Sroga","year":"1992","journal-title":"Nucleic Acids Research"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/978-1-62703-980-2_10","article-title":"Efficient splinted ligation of synthetic RNA using RNA ligase","volume":"1126","author":"Stark","year":"2014","journal-title":"Methods in Molecular Biology"},{"key":"bib51","doi-asserted-by":"publisher","DOI":"10.1021\/bi005120y","article-title":"Hypermodified nucleosides in the anticodon of tRNA(Lys) stabilize a canonical U-turn structure","volume":"39","author":"Sundaram","year":"2000","journal-title":"Biochemistry"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1126\/science.1228985","article-title":"Translation elongation factor EF-P alleviates ribosome stalling at Polyproline stretches","volume":"339","author":"Ude","year":"2013","journal-title":"Science"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"4863","DOI":"10.1093\/emboj\/20.17.4863","article-title":"Improvement of reading frame maintenance is a common function for several tRNA modifications","volume":"20","author":"Urbonavicius","year":"2001","journal-title":"The EMBO Journal"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1016\/j.jmb.2006.05.006","article-title":"Recognition and positioning of mRNA in the ribosome by tRNAs with expanded anticodons","volume":"360","author":"Walker","year":"2006","journal-title":"Journal of Molecular Biology"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1038\/nsmb.3177","article-title":"Multiperspective smFRET reveals rate-determining late intermediates of ribosomal translocation","volume":"23","author":"Wasserman","year":"2016","journal-title":"Nature Structural & Molecular Biology"},{"key":"bib56","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1003003","article-title":"Connecting the kinetics and energy landscape of tRNA translocation on the ribosome","volume":"9","author":"Whitford","year":"2013","journal-title":"PLOS Computational Biology"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"16391","DOI":"10.1074\/jbc.M200253200","article-title":"Accurate translation of the genetic code depends on tRNA modified nucleosides","volume":"277","author":"Yarian","year":"2002","journal-title":"Journal of Biological Chemistry"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1038\/nature07582","article-title":"Quality control by the ribosome following peptide bond formation","volume":"457","author":"Zaher","year":"2009","journal-title":"Nature"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/j.str.2018.01.013","article-title":"Alternative mode of E-Site tRNA binding in the presence of a downstream mRNA stem loop at the entrance channel","volume":"26","author":"Zhang","year":"2018","journal-title":"Structure"},{"key":"bib60","doi-asserted-by":"publisher","DOI":"10.1126\/science.1236086","article-title":"Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation","volume":"340","author":"Zhou","year":"2013","journal-title":"Science"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1126\/science.1255030","article-title":"How the ribosome hands the A-site tRNA to the P site during EF-G-catalyzed translocation","volume":"345","author":"Zhou","year":"2014","journal-title":"Science"},{"key":"bib62","doi-asserted-by":"publisher","first-page":"7813","DOI":"10.1073\/pnas.1901310116","article-title":"Spontaneous ribosomal translocation of mRNA and tRNAs into a chimeric hybrid state","volume":"116","author":"Zhou","year":"2019","journal-title":"PNAS"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/51898\/elife-51898-v2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/51898\/elife-51898-v2.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/51898","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T20:58:26Z","timestamp":1697057906000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/51898"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,5]]},"references-count":62,"alternative-id":["10.7554\/eLife.51898"],"URL":"https:\/\/doi.org\/10.7554\/elife.51898","archive":["CLOCKSS"],"relation":{"is-supplemented-by":[{"id-type":"accession","id":"6NTA","asserted-by":"subject"},{"id-type":"accession","id":"6NSH","asserted-by":"subject"},{"id-type":"accession","id":"6NUO","asserted-by":"subject"},{"id-type":"accession","id":"6NWY","asserted-by":"subject"},{"id-type":"accession","id":"6O3M","asserted-by":"subject"},{"id-type":"accession","id":"6OSI","asserted-by":"subject"}],"has-review":[{"id-type":"doi","id":"10.7554\/eLife.51898.sa1","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.51898.sa2","asserted-by":"object"}],"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.09.01.277525","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,10,5]]},"article-number":"e51898"}}