The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway
Summary Among trypanosomatid protozoa the mechanism of RNA interference (RNAi) has been investigated in Trypanosoma brucei and to a lesser extent in Leishmania braziliensis. Although these two parasitic organisms belong to the same family, they are evolutionarily distantly related raising questions...
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Veröffentlicht in: | Molecular microbiology 2013-02, Vol.87 (3), p.580-593 |
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creator | Atayde, Vanessa D. Shi, Huafang Franklin, Joseph B. Carriero, Nicholas Notton, Timothy Lye, Lon‐Fye Owens, Katherine Beverley, Stephen M. Tschudi, Christian Ullu, Elisabetta |
description | Summary
Among trypanosomatid protozoa the mechanism of RNA interference (RNAi) has been investigated in Trypanosoma brucei and to a lesser extent in Leishmania braziliensis. Although these two parasitic organisms belong to the same family, they are evolutionarily distantly related raising questions about the conservation of the RNAi pathway. Here we carried out an in‐depth analysis of small interfering RNAs (siRNAs) associated with L. braziliensis Argonaute1 (LbrAGO1). In contrast to T. brucei, Leishmania siRNAs are sensitive to 3′ end oxidation, indicating the absence of blocking groups, and the Leishmania genome does not code for a HEN1 RNA 2′‐O‐methyltransferase, which modifies small RNA 3′ ends. Consistent with this observation, ∼ 20% of siRNA 3′ ends carry non‐templated uridines. Thus siRNA biogenesis, and most likely their metabolism, is different in these organisms. Similarly to T. brucei, putative mobile elements and repeats constitute the major Leishmania siRNA‐producing loci and AGO1 ablation leads to accumulation of long transcripts derived from putative mobile elements. However, contrary to T. brucei, no siRNAs were detected from other genomic regions with the potential to form double‐stranded RNA, namely sites of convergent transcription and inverted repeats. Thus, our results indicate that organism‐specific diversification has occurred in the RNAi pathway during evolution of the trypanosomatid lineage. |
doi_str_mv | 10.1111/mmi.12117 |
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Among trypanosomatid protozoa the mechanism of RNA interference (RNAi) has been investigated in Trypanosoma brucei and to a lesser extent in Leishmania braziliensis. Although these two parasitic organisms belong to the same family, they are evolutionarily distantly related raising questions about the conservation of the RNAi pathway. Here we carried out an in‐depth analysis of small interfering RNAs (siRNAs) associated with L. braziliensis Argonaute1 (LbrAGO1). In contrast to T. brucei, Leishmania siRNAs are sensitive to 3′ end oxidation, indicating the absence of blocking groups, and the Leishmania genome does not code for a HEN1 RNA 2′‐O‐methyltransferase, which modifies small RNA 3′ ends. Consistent with this observation, ∼ 20% of siRNA 3′ ends carry non‐templated uridines. Thus siRNA biogenesis, and most likely their metabolism, is different in these organisms. Similarly to T. brucei, putative mobile elements and repeats constitute the major Leishmania siRNA‐producing loci and AGO1 ablation leads to accumulation of long transcripts derived from putative mobile elements. However, contrary to T. brucei, no siRNAs were detected from other genomic regions with the potential to form double‐stranded RNA, namely sites of convergent transcription and inverted repeats. Thus, our results indicate that organism‐specific diversification has occurred in the RNAi pathway during evolution of the trypanosomatid lineage.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.12117</identifier><identifier>PMID: 23217017</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Argonaute Proteins - genetics ; Bacteria ; Biosynthesis ; Gene Expression Regulation ; Genetic Variation ; Leishmania braziliensis ; Leishmania braziliensis - genetics ; Metabolism ; Oxidation ; Parasitic protozoa ; Ribonucleic acid ; RNA ; RNA, Small Interfering - chemistry ; RNA, Small Interfering - genetics ; Trypanosoma brucei ; Trypanosoma brucei brucei - genetics ; Viannia braziliensis</subject><ispartof>Molecular microbiology, 2013-02, Vol.87 (3), p.580-593</ispartof><rights>2012 Blackwell Publishing Ltd</rights><rights>2012 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. Feb 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmmi.12117$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.12117$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,315,782,786,887,1419,1435,27931,27932,45581,45582,46416,46840</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23217017$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Atayde, Vanessa D.</creatorcontrib><creatorcontrib>Shi, Huafang</creatorcontrib><creatorcontrib>Franklin, Joseph B.</creatorcontrib><creatorcontrib>Carriero, Nicholas</creatorcontrib><creatorcontrib>Notton, Timothy</creatorcontrib><creatorcontrib>Lye, Lon‐Fye</creatorcontrib><creatorcontrib>Owens, Katherine</creatorcontrib><creatorcontrib>Beverley, Stephen M.</creatorcontrib><creatorcontrib>Tschudi, Christian</creatorcontrib><creatorcontrib>Ullu, Elisabetta</creatorcontrib><title>The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Among trypanosomatid protozoa the mechanism of RNA interference (RNAi) has been investigated in Trypanosoma brucei and to a lesser extent in Leishmania braziliensis. Although these two parasitic organisms belong to the same family, they are evolutionarily distantly related raising questions about the conservation of the RNAi pathway. Here we carried out an in‐depth analysis of small interfering RNAs (siRNAs) associated with L. braziliensis Argonaute1 (LbrAGO1). In contrast to T. brucei, Leishmania siRNAs are sensitive to 3′ end oxidation, indicating the absence of blocking groups, and the Leishmania genome does not code for a HEN1 RNA 2′‐O‐methyltransferase, which modifies small RNA 3′ ends. Consistent with this observation, ∼ 20% of siRNA 3′ ends carry non‐templated uridines. Thus siRNA biogenesis, and most likely their metabolism, is different in these organisms. Similarly to T. brucei, putative mobile elements and repeats constitute the major Leishmania siRNA‐producing loci and AGO1 ablation leads to accumulation of long transcripts derived from putative mobile elements. However, contrary to T. brucei, no siRNAs were detected from other genomic regions with the potential to form double‐stranded RNA, namely sites of convergent transcription and inverted repeats. Thus, our results indicate that organism‐specific diversification has occurred in the RNAi pathway during evolution of the trypanosomatid lineage.</description><subject>Argonaute Proteins - genetics</subject><subject>Bacteria</subject><subject>Biosynthesis</subject><subject>Gene Expression Regulation</subject><subject>Genetic Variation</subject><subject>Leishmania braziliensis</subject><subject>Leishmania braziliensis - genetics</subject><subject>Metabolism</subject><subject>Oxidation</subject><subject>Parasitic protozoa</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Small Interfering - chemistry</subject><subject>RNA, Small Interfering - genetics</subject><subject>Trypanosoma brucei</subject><subject>Trypanosoma brucei brucei - genetics</subject><subject>Viannia braziliensis</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUstuFDEQtBCILAkHfgBZ4hIOk_g1rwtSFPGItAEpSiJulmemJ9vRjD2xPRst_8H_4t2ECLjQF7e7q8uldhHyhrMjnuJ4HPGIC87LZ2TBZZFnos6r52TB6pxlshLf98irEG4Z45IV8iXZE1LwkvFyQX5eroCG6Oc2zh6osR31MIGPDtPV9TSMZhgo2gi-B4_2hl58PQmpQJeAYTUai4YeXqOxKXlPG29-4IBgA4bEtAYz0A7X4AP22JqIzm5nY3o1-s1krAtuTOVuS4t0MnF1bzYH5EVvhgCvH899cvXp4-Xpl2z57fPZ6ckymxQTZcZVU0KrcsU6YQBUkdesqTsBeSNUU_Sd7EpWFqIWZa2qom_aooEq7w3UBTRpG_vkwwPvNDcjdC3Y6M2gJ4-j8RvtDOq_OxZX-sattczzQkiWCA4fCby7myFEPWJoYRiMBTcHzaWQZZ2i-j9UVIIpXsutrHf_QG_d7G3axA7FlaqYSKi3f4p_Uv37cxPg-AFwjwNsnvqc6a1rdHKN3rlGn5-f7RL5C5l8tzw</recordid><startdate>201302</startdate><enddate>201302</enddate><creator>Atayde, Vanessa D.</creator><creator>Shi, Huafang</creator><creator>Franklin, Joseph B.</creator><creator>Carriero, Nicholas</creator><creator>Notton, Timothy</creator><creator>Lye, Lon‐Fye</creator><creator>Owens, Katherine</creator><creator>Beverley, Stephen M.</creator><creator>Tschudi, Christian</creator><creator>Ullu, Elisabetta</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201302</creationdate><title>The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway</title><author>Atayde, Vanessa D. ; Shi, Huafang ; Franklin, Joseph B. ; Carriero, Nicholas ; Notton, Timothy ; Lye, Lon‐Fye ; Owens, Katherine ; Beverley, Stephen M. ; Tschudi, Christian ; Ullu, Elisabetta</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p4027-14b7ec4540d2aee46590b9d2e5b24b6fd3d707629279486fbc6be85fae96eb013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Argonaute Proteins - genetics</topic><topic>Bacteria</topic><topic>Biosynthesis</topic><topic>Gene Expression Regulation</topic><topic>Genetic Variation</topic><topic>Leishmania braziliensis</topic><topic>Leishmania braziliensis - genetics</topic><topic>Metabolism</topic><topic>Oxidation</topic><topic>Parasitic protozoa</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Small Interfering - chemistry</topic><topic>RNA, Small Interfering - genetics</topic><topic>Trypanosoma brucei</topic><topic>Trypanosoma brucei brucei - genetics</topic><topic>Viannia braziliensis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Atayde, Vanessa D.</creatorcontrib><creatorcontrib>Shi, Huafang</creatorcontrib><creatorcontrib>Franklin, Joseph B.</creatorcontrib><creatorcontrib>Carriero, Nicholas</creatorcontrib><creatorcontrib>Notton, Timothy</creatorcontrib><creatorcontrib>Lye, Lon‐Fye</creatorcontrib><creatorcontrib>Owens, Katherine</creatorcontrib><creatorcontrib>Beverley, Stephen M.</creatorcontrib><creatorcontrib>Tschudi, Christian</creatorcontrib><creatorcontrib>Ullu, Elisabetta</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Atayde, Vanessa D.</au><au>Shi, Huafang</au><au>Franklin, Joseph B.</au><au>Carriero, Nicholas</au><au>Notton, Timothy</au><au>Lye, Lon‐Fye</au><au>Owens, Katherine</au><au>Beverley, Stephen M.</au><au>Tschudi, Christian</au><au>Ullu, Elisabetta</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2013-02</date><risdate>2013</risdate><volume>87</volume><issue>3</issue><spage>580</spage><epage>593</epage><pages>580-593</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Among trypanosomatid protozoa the mechanism of RNA interference (RNAi) has been investigated in Trypanosoma brucei and to a lesser extent in Leishmania braziliensis. Although these two parasitic organisms belong to the same family, they are evolutionarily distantly related raising questions about the conservation of the RNAi pathway. Here we carried out an in‐depth analysis of small interfering RNAs (siRNAs) associated with L. braziliensis Argonaute1 (LbrAGO1). In contrast to T. brucei, Leishmania siRNAs are sensitive to 3′ end oxidation, indicating the absence of blocking groups, and the Leishmania genome does not code for a HEN1 RNA 2′‐O‐methyltransferase, which modifies small RNA 3′ ends. Consistent with this observation, ∼ 20% of siRNA 3′ ends carry non‐templated uridines. Thus siRNA biogenesis, and most likely their metabolism, is different in these organisms. Similarly to T. brucei, putative mobile elements and repeats constitute the major Leishmania siRNA‐producing loci and AGO1 ablation leads to accumulation of long transcripts derived from putative mobile elements. However, contrary to T. brucei, no siRNAs were detected from other genomic regions with the potential to form double‐stranded RNA, namely sites of convergent transcription and inverted repeats. Thus, our results indicate that organism‐specific diversification has occurred in the RNAi pathway during evolution of the trypanosomatid lineage.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>23217017</pmid><doi>10.1111/mmi.12117</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Argonaute Proteins - genetics Bacteria Biosynthesis Gene Expression Regulation Genetic Variation Leishmania braziliensis Leishmania braziliensis - genetics Metabolism Oxidation Parasitic protozoa Ribonucleic acid RNA RNA, Small Interfering - chemistry RNA, Small Interfering - genetics Trypanosoma brucei Trypanosoma brucei brucei - genetics Viannia braziliensis |
title | The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway |
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