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Main virulence factors in LIPI-1 include long 5\u2032 untranslated regions (5\u2032UTRs), among which is Rli51, a small RNA (sRNA) in the 5\u2032UTR of the Zn-metalloprotease-coding mpl. So far, Rli51 function and molecular mechanisms have remained obscure. Here, we show that Rli51 exhibits a dual mechanism of regulation, functioning as a cis- and as a trans-acting sRNA. Under nutrient-rich conditions, rli51-mpl transcription is prematurely terminated, releasing a short 121-nucleotide-long sRNA. Rli51 is predicted to function as a transcription attenuator that can fold into either a terminator or a thermodynamically more stable antiterminator. We show that the sRNA Rli21\/RliI binds to a single-stranded RNA loop in Rli51, which is essential to mediate premature transcription termination, suggesting that sRNA binding could stabilize the terminator fold. During intracellular infection, rli51 transcription is increased, which generates a higher abundance of the short Rli51 sRNA and allows for transcriptional read-through into mpl. Comparative intracellular bacterial transcriptomics in rli51-null mutants and the wild-type reference strain EGD-e suggests that Rli51 upregulates iron-scavenging proteins and downregulates virulence factors from LIPI-1. MS2 affinity purification confirmed that Rli51 binds transcripts of the heme-binding protein Lmo2186 and Lmo0937 in vivo. These results prove that Rli51 functions as a trans-acting sRNA in intracellular bacteria. Our research shows a growth condition-dependent mechanism of regulation for Rli51, preventing unintended mpl transcription in extracellular bacteria and regulating genes important for virulence in intracellular bacteria.<\/jats:p>","DOI":"10.3390\/ijms25179380","type":"journal-article","created":{"date-parts":[[2024,8,29]],"date-time":"2024-08-29T11:12:13Z","timestamp":1724929933000},"page":"9380","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Rli51 Attenuates Transcription of the Listeria Pathogenicity Island 1 Gene mpl and Functions as a Trans-Acting sRNA in Intracellular Bacteria"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7404-7122","authenticated-orcid":false,"given":"\u00c1lvaro","family":"Mor\u00f3n","sequence":"first","affiliation":[{"name":"Department of Cell Biology, Facultad de Ciencias Biol\u00f3gicas, Universidad Complutense de Madrid, 28040 Madrid, Spain"},{"name":"Laboratory of Intracellular Bacterial Pathogens, National Centre for Biotechnology (CNB)-CSIC, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-1354-0683","authenticated-orcid":false,"given":"Laura","family":"Ortiz-Miravalles","sequence":"additional","affiliation":[{"name":"Laboratory of Intracellular Bacterial Pathogens, National Centre for Biotechnology (CNB)-CSIC, 28049 Madrid, Spain"},{"name":"Department of Molecular Biology, Universidad Aut\u00f3noma de Madrid, Centro de Biologia Molecular Severo Ochoa (CBM) CSIC-UAM, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8454-3760","authenticated-orcid":false,"given":"Marcos","family":"Pe\u00f1alver","sequence":"additional","affiliation":[{"name":"Laboratory of Intracellular Bacterial Pathogens, National Centre for Biotechnology (CNB)-CSIC, 28049 Madrid, Spain"},{"name":"Department of Molecular Biology, Universidad Aut\u00f3noma de Madrid, Centro de Biologia Molecular Severo Ochoa (CBM) CSIC-UAM, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4120-0530","authenticated-orcid":false,"given":"Francisco","family":"Garc\u00eda-del Portillo","sequence":"additional","affiliation":[{"name":"Laboratory of Intracellular Bacterial Pathogens, National Centre for Biotechnology (CNB)-CSIC, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4268-2316","authenticated-orcid":false,"given":"M. Graciela","family":"Pucciarelli","sequence":"additional","affiliation":[{"name":"Laboratory of Intracellular Bacterial Pathogens, National Centre for Biotechnology (CNB)-CSIC, 28049 Madrid, Spain"},{"name":"Department of Molecular Biology, Universidad Aut\u00f3noma de Madrid, Centro de Biologia Molecular Severo Ochoa (CBM) CSIC-UAM, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0691-7154","authenticated-orcid":false,"given":"Alvaro Dar\u00edo","family":"Ortega","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Facultad de Ciencias Biol\u00f3gicas, Universidad Complutense de Madrid, 28040 Madrid, Spain"},{"name":"Department of Molecular Biology, Universidad Aut\u00f3noma de Madrid, Centro de Biologia Molecular Severo Ochoa (CBM) CSIC-UAM, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,8,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.gene.2018.02.068","article-title":"Small RNA-Mediated Regulation in Bacteria: A Growing Palette of Diverse Mechanisms","volume":"656","author":"Dutta","year":"2018","journal-title":"Gene"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1016\/j.molcel.2011.08.022","article-title":"Regulation by Small RNAs in Bacteria: Expanding Frontiers","volume":"43","author":"Storz","year":"2011","journal-title":"Mol. Cell"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Felden, B., and Augagneur, Y. (2021). Diversity and Versatility in Small RNA-Mediated Regulation in Bacterial Pathogens. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.719977"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1146\/annurev-micro-030117-020335","article-title":"Regulating Bacterial Virulence with RNA","volume":"71","author":"Quereda","year":"2017","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Ortega, A.D., Quereda, J.J., Pucciarelli, M.G., and Garc\u00eda-del Portillo, F. (2014). Non-Coding RNA Regulation in Pathogenic Bacteria Located inside Eukaryotic Cells. Front. Cell. Infect. Microbiol., 4.","DOI":"10.3389\/fcimb.2014.00162"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1913","DOI":"10.1093\/nar\/gkn050","article-title":"Small RNAs Encoded within Genetic Islands of Salmonella typhimurium Show Host-Induced Expression and Role in Virulence","volume":"36","author":"Hershberg","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Wurtzel, O., Sesto, N., Mellin, J.R., Karunker, I., Edelheit, S., B\u00e9cavin, C., Archambaud, C., Cossart, P., and Sorek, R. (2012). Comparative Transcriptomics of Pathogenic and Non-pathogenic Listeria Species. Mol. Syst. Biol., 8.","DOI":"10.1038\/msb.2012.11"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1038\/nature08080","article-title":"The Listeria Transcriptional Landscape from Saprophytism to Virulence","volume":"459","author":"Dussurget","year":"2009","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4235","DOI":"10.1093\/nar\/gkr033","article-title":"The Intracellular SRNA Transcriptome of Listeria monocytogenes during Growth in Macrophages","volume":"39","author":"Mraheil","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"469","DOI":"10.4161\/rna.19317","article-title":"Dynamics of Salmonella Small RNA Expression in Non-Growing Bacteria Located inside Eukaryotic Cells","volume":"9","author":"Ortega","year":"2012","journal-title":"RNA Biol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Srikumar, S., Kr\u00f6ger, C., H\u00e9brard, M., Colgan, A., Owen, S.V., Sivasankaran, S.K., Cameron, A.D.S., Hokamp, K., and Hinton, J.C.D. (2015). RNA-Seq Brings New Insights to the Intra-Macrophage Transcriptome of Salmonella typhimurium. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1005262"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Wang, L., Ji, C., Xia, X., Cai, X., Meng, Q., and Qiao, J. (2022). A Regulatory SRNA Rli43 Is Involved in the Modulation of Biofilm Formation and Virulence in Listeria monocytogenes. Pathogens, 11.","DOI":"10.3390\/pathogens11101137"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2509","DOI":"10.1080\/21505594.2021.1975526","article-title":"Pathogenicity and Virulence of Listeria monocytogenes: A Trip from Environmental to Medical Microbiology","volume":"12","author":"Quereda","year":"2021","journal-title":"Virulence"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1128\/CMR.14.3.584-640.2001","article-title":"Listeria pathogenesis and Molecular Virulence Determinants","volume":"14","author":"Kuhn","year":"2001","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1046\/j.1462-5822.2003.00348.x","article-title":"Evidence Implicating the 5\u2032 Untranslated Region of Listeria monocytogenes ActA in the Regulation of Bacterial Actin-Based Motility","volume":"6","author":"Wong","year":"2004","journal-title":"Cell Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1128\/iai.59.1.65-72.1991","article-title":"Molecular Cloning, Sequencing, and Identification of a Metalloprotease Gene from Listeria monocytogenes That Is Species Specific and Physically Linked to the Listeriolysin Gene","volume":"59","author":"Domann","year":"1991","journal-title":"Infect. Immun."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.tim.2006.05.001","article-title":"Control of Listeria monocytogenes Virulence by 5\u2032-Untranslated RNA","volume":"14","author":"Loh","year":"2006","journal-title":"Trends Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"aad9822","DOI":"10.1126\/science.aad9822","article-title":"Term-Seq Reveals Abundant Ribo-Regulation of Antibiotics Resistance in Bacteria","volume":"352","author":"Dar","year":"2016","journal-title":"Science"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4027","DOI":"10.1016\/j.celrep.2020.03.006","article-title":"An MRNA-MRNA Interaction Couples Expression of a Virulence Factor and Its Chaperone in Listeria monocytogenes","volume":"30","author":"Ignatov","year":"2020","journal-title":"Cell Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1460","DOI":"10.1111\/j.1365-2958.2005.04780.x","article-title":"The 5\u2032 Untranslated Region-Mediated Enhancement of Intracellular Listeriolysin O Production Is Required for Listeria monocytogenes Pathogenicity","volume":"57","author":"Shen","year":"2005","journal-title":"Mol. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1111\/j.1365-2958.1994.tb00390.x","article-title":"Transcriptional Regulation of PrfA and PrfA-Regulated Virulence Genes in Listeria monocytogenes","volume":"11","author":"Bohne","year":"1994","journal-title":"Mol. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1083\/jcb.137.6.1381","article-title":"Proteolytic Pathways of Activation and Degradation of a Bacterial Phospholipase C during Intracellular Infection by Listeria monocytogenes","volume":"137","author":"Marquis","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1128\/IAI.00130-16","article-title":"The Metalloprotease Mpl Supports Listeria monocytogenes Dissemination through Resolution of Membrane Protrusions into Vacuoles","volume":"84","author":"Alvarez","year":"2016","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/nrmicro2560","article-title":"Termination and Antitermination: RNA Polymerase Runs a Stop Sign","volume":"9","author":"Santangelo","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1093\/nar\/gkw749","article-title":"Computational Prediction of Regulatory, Premature Transcription Termination in Bacteria","volume":"45","author":"Millman","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/j.cell.2009.08.046","article-title":"A Trans-Acting Riboswitch Controls Expression of the Virulence Regulator PrfA in Listeria monocytogenes","volume":"139","author":"Loh","year":"2009","journal-title":"Cell"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"R343","DOI":"10.1016\/j.cub.2023.03.069","article-title":"Riboswitches","volume":"33","author":"Salvail","year":"2023","journal-title":"Curr. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"W435","DOI":"10.1093\/nar\/gkx279","article-title":"IntaRNA 2.0: Enhanced and Customizable Prediction of RNA\u2013RNA Interactions","volume":"45","author":"Mann","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e00186-16","DOI":"10.1128\/mSystems.00186-16","article-title":"Listeriomics: An Interactive Web Platform for Systems Biology of Listeria","volume":"2","author":"Koutero","year":"2017","journal-title":"mSystems"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1980","DOI":"10.1093\/nar\/19.8.1980-a","article-title":"Purification or RNA and RNA\u2014Protein Complexes by an R17 Coat Protein Affinity Method","volume":"19","author":"Bardwell","year":"1991","journal-title":"Nucleic Acids Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.ymeth.2016.11.011","article-title":"Identification of Unknown RNA Partners Using MAPS","volume":"117","author":"Lalaouna","year":"2017","journal-title":"Methods"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1576","DOI":"10.1128\/iai.61.4.1576-1580.1993","article-title":"The Zinc Metalloprotease of Listeria monocytogenes Is Required for Maturation of Phosphatidylcholine Phospholipase C: Direct Evidence Obtained by Gene Complementation","volume":"61","author":"Poyart","year":"1993","journal-title":"Infect. Immun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1128\/iai.60.3.916-921.1992","article-title":"Reduced Virulence of a Listeria monocytogenes Phospholipase-Deficient Mutant Obtained by Transposon Insertion into the Zinc Metalloprotease Gene","volume":"60","author":"Raveneau","year":"1992","journal-title":"Infect. Immun."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Chakravarty, S., and Mass\u00e9, E. (2019). RNA-Dependent Regulation of Virulence in Pathogenic Bacteria. Front. Cell. Infect. Microbiol., 9.","DOI":"10.3389\/fcimb.2019.00337"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Krawczyk-Balska, A., \u0141adziak, M., Burmistrz, M., \u015acibek, K., and Kallipolitis, B.H. (2021). RNA-Mediated Control in Listeria monocytogenes: Insights Into Regulatory Mechanisms and Roles in Metabolism and Virulence. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.622829"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1128\/JB.187.8.2836-2845.2005","article-title":"Enhanced Synthesis of Internalin A in Aro Mutants of Listeria monocytogenes Indicates Posttranscriptional Control of the InlAB MRNA","volume":"187","author":"Stritzker","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/S0092-8674(02)00905-4","article-title":"An RNA Thermosensor Controls Expression of Virulence Genes in Listeria monocytogenes","volume":"110","author":"Johansson","year":"2002","journal-title":"Cell"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Turnbough, C.L. (2019). Regulation of Bacterial Gene Expression by Transcription Attenuation. Microbiol. Mol. Biol. Rev., 83.","DOI":"10.1128\/MMBR.00019-19"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.cell.2016.09.004","article-title":"SRNA-Mediated Control of Transcription Termination in E. coli","volume":"167","author":"Sedlyarova","year":"2016","journal-title":"Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"34886","DOI":"10.1074\/jbc.M114.583013","article-title":"Novel Mechanism of Hemin Capture by Hbp2, the Hemoglobin-Binding Hemophore from Listeria monocytogenes","volume":"289","author":"Malmirchegini","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2840","DOI":"10.1074\/jbc.M409526200","article-title":"Staphylococcus aureus IsdG and IsdI, Heme-Degrading Enzymes with Structural Similarity to Monooxygenases","volume":"280","author":"Wu","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"dos Santos, P.T., Menendez-Gil, P., Sabharwal, D., Christensen, J.H., Brunhede, M.Z., Lilleb\u00e6k, E.M.S., and Kallipolitis, B.H. (2018). The Small Regulatory RNAs LhrC1\u20135 Contribute to the Response of Listeria monocytogenes to Heme Toxicity. Front. Microbiol., 9.","DOI":"10.3389\/fmicb.2018.00599"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"103096","DOI":"10.1016\/j.isci.2021.103096","article-title":"Wisdom of the Crowds: A Suggested Polygenic Plan for Small-RNA-Mediated Regulation in Bacteria","volume":"24","author":"Goldberger","year":"2021","journal-title":"iScience"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.mib.2007.06.001","article-title":"Target Identification of Small Noncoding RNAs in Bacteria","volume":"10","author":"Vogel","year":"2007","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Acebo, P., Herranz, C., Espenberger, L.B., G\u00f3mez-sanz, A., Terr\u00f3n, M.C., Luque, D., and Amblar, M. (2021). A Small Non-coding Rna Modulates Expression of Pilus-1 Type in Streptococcus pneumoniae. Microorganisms, 9.","DOI":"10.3390\/microorganisms9091883"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"6396","DOI":"10.1093\/nar\/gkz274","article-title":"Transcription Attenuation-Derived Small RNA RnTrpL Regulates Tryptophan Biosynthesis Gene Expression in Trans","volume":"47","author":"Melior","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e0013421","DOI":"10.1128\/mSphere.00134-21","article-title":"A Small Regulatory RNA Generated from the MalK 59 Untranslated Region Targets Gluconeogenesis in Vibrio Species","volume":"6","author":"Luo","year":"2021","journal-title":"Msphere"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"10964","DOI":"10.1093\/nar\/gks847","article-title":"An Archaeal SRNA Targeting Cis-and Trans-Encoded MRNAs via Two Distinct Domains","volume":"40","author":"Pernitzsch","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.molcel.2021.12.030","article-title":"Global RNA Interactome of Salmonella Discovers a 5\u2032 UTR Sponge for the MicF Small RNA That Connects Membrane Permeability to Transport Capacity","volume":"82","author":"Matera","year":"2022","journal-title":"Mol. Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.mib.2015.12.006","article-title":"The Unmasking of \u201cjunk\u201d RNA Reveals Novel SRNAs: From Processed RNA Fragments to Marooned Riboswitches","volume":"30","author":"Garsin","year":"2016","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e62438","DOI":"10.7554\/eLife.62438","article-title":"Regulatory Roles of Escherichia coli 5\u2032 UTR and ORF-Internal RNAs Detected by 3\u2032 End Mapping","volume":"10","author":"Adams","year":"2021","journal-title":"Elife"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1126\/science.1063447","article-title":"Comparative Genomics of Listeria Species","volume":"294","author":"Glaser","year":"2001","journal-title":"Science"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/0378-1119(90)90336-P","article-title":"High Efficiency Transformation of Escherichia coli with Plasmids","volume":"96","author":"Inoue","year":"1990","journal-title":"Gene"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"4994","DOI":"10.1093\/nar\/gkx190","article-title":"An in vivo Reporter Assay for SRNA-Directed Gene Control in Gram-Positive Bacteria: Identifying a Novel SRNA Target in Staphylococcus aureus","volume":"45","author":"Ivain","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3625","DOI":"10.1128\/AEM.02612-09","article-title":"Single-Cell Techniques Using Chromosomally Tagged Fluorescent Bacteria to Study Listeria monocytogenes Infection Processes","volume":"76","author":"Balestrino","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2685","DOI":"10.1242\/jcs.065920","article-title":"Human G3BP1 Interacts with Beta-F1-ATPase MRNA and Inhibits Its Translation","volume":"123","author":"Ortega","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2849","DOI":"10.1093\/bioinformatics\/btn544","article-title":"IntaRNA: Efficient Prediction of Bacterial SRNA Targets Incorporating Target Site Accessibility and Seed Regions","volume":"24","author":"Busch","year":"2008","journal-title":"Bioinformatics"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast Gapped-Read Alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nbt.1621","article-title":"Transcript Assembly and Quantification by RNA-Seq Reveals Unannotated Transcripts and Isoform Switching during Cell Differentiation","volume":"28","author":"Trapnell","year":"2010","journal-title":"Nat. Biotechnol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/17\/9380\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:45:11Z","timestamp":1760111111000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/17\/9380"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,29]]},"references-count":59,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2024,9]]}},"alternative-id":["ijms25179380"],"URL":"https:\/\/doi.org\/10.3390\/ijms25179380","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,29]]}}}