{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T23:15:23Z","timestamp":1792710923041,"version":"4.5.0"},"reference-count":71,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,2,5]],"date-time":"2025-02-05T00:00:00Z","timestamp":1738713600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001807","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de S\u00e3o Paulo","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>The protozoan parasite <jats:italic>Leishmania<\/jats:italic> spp. is a causative agent of leishmaniasis, a disease that affects millions of people in more than 80 countries worldwide. Apart from its medical relevance, this organism has a genetic organization that is unique among eukaryotes. Studies of the mechanisms regulating gene expression in <jats:italic>Leishmania<\/jats:italic> led us to investigate noncoding RNAs (ncRNAs) as regulatory elements. We previously identified differentially expressed (DE) ncRNAs in <jats:italic>Leishmania braziliensis<\/jats:italic> with potential roles in the parasite biology and development. Herein, we present a functional analysis of one such DE ncRNA, the 147-nucleotide-long transcript ncRNA97, which is preferentially expressed in amastigotes, the replicative form within mammalian phagocytes. By RT-qPCR the ncRNA97 was detected in greater quantities in the nucleus under physiological conditions and in the cytoplasm under nutritional stress. Interestingly, the transcript is protected at the 5\u2019 end but is not processed by the canonical trypanosomatid <jats:italic>trans<\/jats:italic>-splicing mechanism, according to the RNA circularization assay. ncRNA97 knockout (<jats:sup>KO<\/jats:sup>) and addback (<jats:sup>AB<\/jats:sup>) transfectants were generated and subjected to phenotypic analysis, which revealed that the lack of ncRNA97 impairs the starvation response and differentiation to the infective form. Comparative transcriptomics of ncRNA97<jats:sup>KO<\/jats:sup> and parental cells revealed that transcripts encoding amastigote-specific proteins were affected. This pioneering work demonstrates that ncRNAs contribute to the developmental regulatory mechanisms of <jats:italic>Leishmania<\/jats:italic>.<\/jats:p>","DOI":"10.3389\/fcimb.2025.1513908","type":"journal-article","created":{"date-parts":[[2025,2,5]],"date-time":"2025-02-05T07:35:24Z","timestamp":1738740924000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["A short ncRNA modulates gene expression and affects stress response and parasite differentiation in Leishmania braziliensis"],"prefix":"10.3389","volume":"15","author":[{"suffix":"Jr","given":"Jos\u00e9 C.","family":"Quilles","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline R.","family":"Espada","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lissur A.","family":"Orsine","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T\u00e2nia A.","family":"Defina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Let\u00edcia","family":"Almeida","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fab\u00edola","family":"Holetz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela K.","family":"Cruz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,2,5]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/MCB.00344-16","article-title":"Phosphorylation of Translation Initiation 2-Alpha in Leishmania donovani under stress is necessary for Parasite Survival","volume":"37","author":"Abhishek","year":"2017","journal-title":"Mol. Cell. Biol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1016\/j.pt.2024.06.003","article-title":"LeishGEM: genome-wide deletion mutant fitness and protein localisations in Leishmania","volume":"40","author":"Aellig","year":"2024","journal-title":"Trends Parasitol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1016\/j.ijpara.2007.04.003","article-title":"Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies","volume":"37","author":"Bates","year":"2007","journal-title":"Int. J. Parasitol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-023-40883-w","article-title":"Novel insights into the role of long non-coding RNA in the human malaria parasite, Plasmodium falciparum","volume":"14","author":"Batugedara","year":"2023","journal-title":"Nat. Commun."},{"key":"B5","doi-asserted-by":"publisher","first-page":"170095","DOI":"10.1098\/rsos.170095","article-title":"A CRISPR Cas9 high-throughput genome editing toolkit for kinetoplastids Subject Category: Subject Areas","volume":"4","author":"Beneke","year":"2017","journal-title":"R. Soc Open Sci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1128\/mcb.10.1.28-36.1990","article-title":"The product of the H19 gene may function as an RNA","volume":"10","author":"Brannan","year":"1990","journal-title":"Mol. Cell. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"18321","DOI":"10.1073\/pnas.0909641106","article-title":"Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast","volume":"106","author":"Bumgarner","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pgen.1007378","article-title":"LncRNA Jpx induces Xist expression in mice using both trans and cis mechanisms","volume":"14","author":"Carmona","year":"2018","journal-title":"PloS Genet."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ijms19051310","article-title":"Noncoding RNA: RNA regulatory networks in cancer","volume":"19","author":"Chan","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"2609","DOI":"10.1093\/nar\/gky1287","article-title":"Small nucleolar RNAs controlling rRNA processing in Trypanosoma brucei","volume":"47","author":"Chikne","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.molbiopara.2014.06.005","article-title":"Networks of gene expression regulation in Trypanosoma brucei","volume":"195","author":"Clayton","year":"2014","journal-title":"Mol. Biochem. Parasitol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.mib.2016.04.018","article-title":"Gene expression in kinetoplastids","volume":"32","author":"Clayton","year":"2016","journal-title":"Curr. Opin. Microbiol."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0008668","article-title":"The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages","volume":"5","author":"Daigneault","year":"2010","journal-title":"PLoS One"},{"key":"B14","doi-asserted-by":"publisher","first-page":"1271","DOI":"10.1074\/mcp.RA118.001307","article-title":"The mRNA-bound Proteome of Leishmania mexicana: Novel genetic insight into an ancient parasite*","volume":"18","author":"De Pablos","year":"2019","journal-title":"Mol. Cell. Proteomics"},{"key":"B15","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/j.mib.2016.08.004","article-title":"Developmental differentiation in Leishmania lifecycle progression: post-transcriptional control conducts the orchestra","volume":"34","author":"De Pablos","year":"2016","journal-title":"Curr. Opin. Microbiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.ppat.1005296","article-title":"Amastin knockdown in leishmania Braziliensis affects parasite-macrophage interaction and results in impaired viability of intracellular amastigotes","volume":"11","author":"de Paiva","year":"2015","journal-title":"PLoS Pathog."},{"key":"B17","doi-asserted-by":"publisher","first-page":"2033","DOI":"10.1128\/EC.00147-06","article-title":"A novel class of developmentally regulated noncoding RNAs in Leishmania","volume":"5","author":"Dumas","year":"2006","journal-title":"Eukaryot. Cell"},{"key":"B18","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1038\/nature20149","article-title":"Local regulation of gene expression by lncRNA promoters, transcription and splicing","volume":"539","author":"Engreitz","year":"2016","journal-title":"Nature"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2013.00168","article-title":"Identification and function of long non-coding RNA","volume":"7","author":"Ernst","year":"2013","journal-title":"Front. Cell. Neurosci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ncrna5010017","article-title":"Long non-coding RNAs in the regulation of gene expression: Physiology and disease","volume":"5","author":"Fernandes","year":"2019","journal-title":"Non-coding RNA"},{"key":"B21","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.molbiopara.2017.04.002","article-title":"Evidence of putative non-coding RNAs from Leishmania untranslated regions","volume":"214","author":"Freitas Castro","year":"2017","journal-title":"Mol. Biochem. Parasitol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-018-07949-6","article-title":"A tRNA half modulates translation as stress response in Trypanosoma brucei","volume":"10","author":"Fricker","year":"2019","journal-title":"Nat. Commun."},{"key":"B23","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1038\/nrg2504","article-title":"Small silencing RNAs: An expanding universe","volume":"10","author":"Ghildiyal","year":"2009","journal-title":"Nat. Rev. Genet."},{"key":"B24","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1038\/s41576-019-0184-5","article-title":"Regulation of gene expression by cis-acting long non-coding RNAs","volume":"21","author":"Gil","year":"2020","journal-title":"Nat. Rev. Genet."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1408","DOI":"10.1177\/0022146515594631.Marriage","article-title":"Messenger RNA modifications - Form, distribution and function","volume":"352","author":"Gilbert","year":"2016","journal-title":"Science (80-.)."},{"key":"B26","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1093\/nar\/gkn188","article-title":"The vienna RNA websuite","volume":"36","author":"Gruber","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1126\/sciadv.abn2706","article-title":"A long noncoding RNA promotes parasite differentiation in African trypanosomes","volume":"8","author":"Guegan","year":"2022","journal-title":"Sci. Adv."},{"key":"B28","doi-asserted-by":"publisher","first-page":"835","DOI":"10.1038\/nature09267","article-title":"Mammalian microRNAs predominantly act to decrease target mRNA levels","volume":"466","author":"Guo","year":"2010","journal-title":"Nature"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.21769\/BioProtoc.1533","article-title":"Circular RT-PCR assay using Arabidopsis samples","volume":"5","author":"Hang","year":"2015","journal-title":"Bio-Protocol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"3061","DOI":"10.3390\/biomedicines10123061","article-title":"Transcription factors and ncRNAs associated with CYP3A expression in human liver and small intestine assessed with weighted gene co-expression network analysis","volume":"10","author":"Huang","year":"2022","journal-title":"Biomedicines"},{"key":"B31","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/S0166-6851(03)00006-9","article-title":"A processed short transcript of Leishmania, ODD1","volume":"127","author":"Iribar","year":"2003","journal-title":"Mol. Biochem. Parasitol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/database\/baw167","article-title":"RAIN: RNA-protein association and interaction networks","volume":"2017","author":"Junge","year":"2017","journal-title":"Database"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1084","DOI":"10.1128\/mcb.10.3.1084-1094.1990","article-title":"Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression","volume":"10","author":"Kapler","year":"1990","journal-title":"Mol. Cell. Biol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"B35","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1096\/fj.10-157529","article-title":"Multiple levels of gene regulation mediate differentiation of the intracellular pathogen Leishmania","volume":"25","author":"Lahav","year":"2011","journal-title":"FASEB J."},{"key":"B36","doi-asserted-by":"publisher","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":"B37","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1101\/gad.7.6.996","article-title":"Coupling of poly(A) site selection and trans-splicing in Leishmania","volume":"7","author":"Lebowitz","year":"1993","journal-title":"Gene Dev."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkt956","article-title":"An optimized streptavidin-binding RNA aptamer for purification of ribonucleoprotein complexes identifies novel ARE-binding proteins","volume":"42","author":"Leppek","year":"2014","journal-title":"Nucleic Acid Research"},{"key":"B39","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1261\/rna.7174805","article-title":"A genome-wide analysis of C\/D and H\/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification","volume":"11","author":"Liang","year":"2005","journal-title":"RNA"},{"key":"B40","doi-asserted-by":"publisher","first-page":"12174","DOI":"10.1073\/pnas.1614594113","article-title":"Structure and assembly model for the trypanosoma cruzi 60s ribosomal subunit","volume":"113","author":"Liu","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B41","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1021\/acsinfecdis.1c00509","article-title":"Functional study of leishmania Braziliensis protein arginine methyltransferases (PRMTs) reveals that PRMT1 and PRMT5 are required for macrophage infection","volume":"8","author":"Lorenzon","year":"2022","journal-title":"ACS Infect. Dis."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.ymeth.2018.10.023","article-title":"Analysis of RNA 5\u2032 ends: Phosphate enumeration and cap characterization","volume":"155","author":"Luciano","year":"2019","journal-title":"Methods"},{"key":"B44","doi-asserted-by":"publisher","first-page":"3840","DOI":"10.1016\/j.molcel.2022.09.036","article-title":"Alternative cleavage and polyadenylation generates downstream uncapped RNA isoforms with translation potential","volume":"82","author":"Malka","year":"2022","journal-title":"Mol. Cell"},{"key":"B45","doi-asserted-by":"publisher","first-page":"140","DOI":"10.2174\/1389202918666170911163517","article-title":"Epigenetic regulation of transcription in trypanosomatid protozoa","volume":"19","author":"Mart\u00ednez-calvillo","year":"2018","journal-title":"Current Genomics"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/0471250953.bi1206s46","article-title":"RNA secondary structure analysis using RNAstructure","author":"Mathews","year":"2014","journal-title":"Curr. Protoc. Bioinforma."},{"key":"B47","doi-asserted-by":"publisher","first-page":"491","DOI":"10.1101\/gad.8.4.491","article-title":"A common pyrimidine-rich motif governs trans-splicing and polyadenylation of tubulin polycistronic pre-mRNA in trypanosomes","volume":"8","author":"Matthews","year":"1994","journal-title":"Genes Dev."},{"key":"B48","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/s41580-022-00566-8","article-title":"Long non-coding RNAs: definitions, functions, challenges and recommendations","volume":"24","author":"Mattick","year":"2023","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"2393","DOI":"10.1093\/nar\/gkq1158","article-title":"Expression of distinct RNAs from 3\u2032 untranslated regions","volume":"39","author":"Mercer","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"B50","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1016\/j.cell.2015.10.012","article-title":"5\u2032 UTR m6A promotes cap-independent translation","volume":"163","author":"Meyer","year":"2015","journal-title":"Cell"},{"key":"B51","doi-asserted-by":"publisher","first-page":"2002","DOI":"10.1111\/j.1365-2966.2012.21196.x","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"B52","doi-asserted-by":"publisher","first-page":"2943","DOI":"10.1093\/bioinformatics\/btac166","article-title":"Analysing high-throughput sequencing data in Python with HTSeq 2.0","volume":"38","author":"Putri","year":"2022","journal-title":"Bioinformatics"},{"key":"B53","doi-asserted-by":"publisher","first-page":"4028","DOI":"10.1128\/JCM.02064-12","article-title":"Association between an emerging disseminated form of leishmaniasis and Leishmania (Viannia) Braziliensis strain polymorphisms","volume":"50","author":"Queiroz","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"B54","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.molbiopara.2005.01.006","article-title":"Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp","volume":"140","author":"Rochette","year":"2005","journal-title":"Mol. Biochem. Parasitol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"2129","DOI":"10.1101\/gr.122945.111","article-title":"Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania","volume":"21","author":"Rogers","year":"2011","journal-title":"Genome Res."},{"key":"B56","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1080\/15476286.2019.1574161","article-title":"Comparative transcriptomics in Leishmania Braziliensis: disclosing differential gene expression of coding and putative noncoding RNAs across developmental stages","volume":"16","author":"Ruy","year":"2019","journal-title":"RNA Biol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/wrna.1681","article-title":"RNA methyltransferase METTL16: Targets and function","volume":"13","author":"Satterwhite","year":"2022","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"B58","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.molbiopara.2006.11.011","article-title":"Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation","volume":"152","author":"Saxena","year":"2007","journal-title":"Mol. Biochem. Parasitol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.parint.2017.10.009","article-title":"Involvement of STI1 protein in the differentiation process of Trypanosoma cruzi","volume":"67","author":"Schmidt","year":"2018","journal-title":"Parasitol. Int."},{"key":"B60","doi-asserted-by":"publisher","first-page":"1175","DOI":"10.1093\/nar\/gkz1149","article-title":"Integrative analyses of noncoding RNAs reveal the potential mechanisms augmenting tumor Malignancy in lung adenocarcinoma","volume":"48","author":"Shih","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1756-3305-5-160","article-title":"Proteinases as virulence factors in Leishmania spp. infection in mammals","volume":"5","author":"Silva-Almeida","year":"2012","journal-title":"Parasites Vectors"},{"key":"B62","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1006\/expr.2001.4656","article-title":"A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation","volume":"99","author":"Sp\u00e4th","year":"2001","journal-title":"Exp. Parasitol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0294236","article-title":"SRplot: A free online platform for data visualization and graphing","volume":"18","author":"Tang","year":"2023","journal-title":"PLoS One"},{"key":"B64","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1128\/mcb.13.1.720","article-title":"Temporal order of RNA-processing reactions in trypanosomes: rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts","volume":"13","author":"Ullu","year":"1993","journal-title":"Mol. Cell. Biol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00603-018-1496-z","article-title":"Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes","volume":"3","author":"Vandesompele","year":"2002","journal-title":"Genome Biol."},{"key":"B66","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1073\/pnas.1619369114","article-title":"Identification of NAD+ capped mRNAs in Saccharomyces cerevisiae","volume":"114","author":"Walters","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B67","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/S0166-6851(97)00115-1","article-title":"Molecular characterization of the heat-inducible LmSTI1 protein of Leishmania major","volume":"89","author":"Webb","year":"1997","journal-title":"Mol. Biochem. Parasitol."},{"key":"B68","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1016\/S0166-6851(00)00290-5","article-title":"A new developmentally regulated gene family in Leishmania amastigotes encoding a homolog of amastin surface proteins","volume":"110","author":"Wu","year":"2000","journal-title":"Mol. Biochem. Parasitol."},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1016\/j.heliyon.2023.e13076","article-title":"Ribosomal protein L31 (RPL31) inhibits the proliferation and migration of gastric cancer cells","volume":"9","author":"Wu","year":"2023","journal-title":"Heliyon"},{"key":"B70","doi-asserted-by":"publisher","first-page":"194","DOI":"10.5483\/BMBRep.2017.50.4.040","article-title":"Translational control of mRNAs by 3\u2019-Untranslated region binding proteins","volume":"50","author":"Yamashita","year":"2017","journal-title":"BMB Rep."},{"key":"B71","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1261\/rna.035683.112","article-title":"Comparative transcriptome analysis of small noncoding RNAs in different stages of Trypanosoma brucei","volume":"19","author":"Zheng","year":"2013","journal-title":"RNA"}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1513908\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,5]],"date-time":"2025-02-05T07:35:29Z","timestamp":1738740929000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2025.1513908\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,5]]},"references-count":71,"alternative-id":["10.3389\/fcimb.2025.1513908"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2025.1513908","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,2,5]]},"article-number":"1513908"}}