Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion by the Production of Two Length Variants from the Prematurely Interrupted tssM Gene
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{"title"=>"Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion by the Production of Two Length Variants from the Prematurely Interrupted tssM Gene", "type"=>"journal", "authors"=>[{"first_name"=>"Erwan", "last_name"=>"Gueguen", "scopus_author_id"=>"7003451470"}, {"first_name"=>"Norma M.", "last_name"=>"Wills", "scopus_author_id"=>"7005848657"}, {"first_name"=>"John F.", "last_name"=>"Atkins", "scopus_author_id"=>"7201885723"}, {"first_name"=>"Eric", "last_name"=>"Cascales", "scopus_author_id"=>"6603332760"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84919663848", "doi"=>"10.1371/journal.pgen.1004869", "pui"=>"601033587", "pmid"=>"25474156", "scopus"=>"2-s2.0-84919663848", "issn"=>"15537404"}, "id"=>"15fa8b08-9925-3bf5-83f5-86cb492ee810", "abstract"=>"The Type VI secretion system (T6SS) mediates toxin delivery into both eukaryotic and prokaryotic cells. It is composed of a cytoplasmic structure resembling the tail of contractile bacteriophages anchored to the cell envelope through a membrane complex composed of the TssL and TssM inner membrane proteins and of the TssJ outer membrane lipoprotein. The C-terminal domain of TssM is required for its interaction with TssJ, and for the function of the T6SS. In Citrobacter rodentium, the tssM1 gene does not encode the C-terminal domain. However, the stop codon is preceded by a run of 11 consecutive adenosines. In this study, we demonstrate that this poly-A tract is a transcriptional slippery site that induces the incorporation of additional adenosines, leading to frameshifting, and hence the production of two TssM1 variants, including a full-length canonical protein. We show that both forms of TssM1, and the ratio between these two forms, are required for the function of the T6SS in C. rodentium. Finally, we demonstrate that the tssM gene associated with the Yersinia pseudotuberculosis T6SS-3 gene cluster is also subjected to transcriptional frameshifting.", "link"=>"http://www.mendeley.com/research/transcriptional-frameshifting-rescues-citrobacter-rodentium-type-vi-secretion-production-two-length", "reader_count"=>13, "reader_count_by_academic_status"=>{"Researcher"=>2, "Student > Ph. D. Student"=>4, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>2, "Student > Ph. D. Student"=>4, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>6, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1822093"], "description"=>"<p>(A) Representation of the nucleotide sequence of <i>C. rodentium tssM1</i>. The 11-nt poly-A tract is shown in red. The codons and the amino-acids resulting from translation of the WT sequence, as well as those produced from +1 or +2 frameshifting are indicated (stops identified by the asterisks) with the size of the corresponding TssM1 variants. (B) Schematic representation of the putative localizations and topologies of the TssM1[1–807] (produced from the WT sequence), TssM1-FL (produced from +1 frameshifting) and TssM1[1–802] (produced from +2 frameshifting) proteins. The locations of the N-terminal FLAG and C-terminal 6×His epitope tags are indicated by red and blue balls respectively (IM, inner membrane; OM, outer membrane). (C) Western-blot analyses of <i>C. rodentium</i> cells producing (WT) or not (vector) the TssM1 protein bearing a FLAG-epitope tag at the N-terminus and a 6×His tag upstream the stop codon resulting from +1 frameshifting. Crude extracts from 10<sup>9</sup> cells were subjected to 10%-acrylamide SDS-PAGE and immunodetection using the anti-FLAG and anti-5His monoclonal antibodies. The positions of the TssM1-FL and -[1–807] variants are indicated on the right, with the schematic representation in the middle. The relative intensities of these two TssM1 variants are indicated (as %). Molecular weight markers (in kDa) are indicated on the left.</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260531, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_C_rodentium_tssM1_gene_encode_two_size_variants_/1260531", "title"=>"The <i>C. rodentium tssM1</i> gene encode two size variants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822097"], "description"=>"<p>(A) Representation of the nucleotide sequence of <i>C. rodentium tssM1</i> and of the mutagenized variants used in panel (B). The poly-A tract is shown in red, the mutagenized nucleotides are shown in green. (B) Western-blot analyses of <i>C. rodentium</i> cells producing the indicated TssM1 protein variant bearing a FLAG-epitope tag at the N-terminus and a 6×His tag upstream the stop codon resulting from +1 frameshifting. Crude extracts from 10<sup>9</sup> cells were subjected to 10%-acrylamide SDS-PAGE and immunodetection using the anti-FLAG and anti-5His monoclonal antibodies. The positions of the TssM1-FL and -[1–807] variants are indicated on the right, with the schematic representation in the middle. The relative intensities of these two TssM1 variants are indicated (as %). Molecular weight markers (in kDa) are indicated on the left. (C) Representation of the nucleotide sequence of <i>C. rodentium tssM1</i> constructs used for fluorescence studies shown in panel (D). The poly-A tract is shown in red, the mutagenized nucleotides are shown in green and additional nucleotides are shown in blue. (D) Fluorescence levels (in arbitrary units, A.U.) of cells producing the different TssM1 variants shown in panel (C).</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260535, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_TssM1_full_length_variant_is_produced_through_slippage_on_a_poly_A_tract_/1260535", "title"=>"The TssM1 full-length variant is produced through slippage on a poly-A tract.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822133"], "description"=>"<p>ESI/MS analyses. Mass spectra of PCR products encompassing the <i>tssM1</i> poly-A tract generated by RT-PCR from <i>C. rodentium</i> total RNA (mRNA; A) or from a synthetic mRNA (B). The two strands of the PCR products are observable. The molecular mass (in Da) is shown on the <i>x</i> axis, and the relative intensity of the signal is indicated on the <i>y</i> axis. The number of A or T residues in the homopolymeric run is shown above each peak. The measured and predicted masses (in Da) of each peak are shown in the insert for each panel. The difference between predicted and measured masses is expressed as the percentage error for each peak.</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260540, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Frameshifting_is_caused_by_transcriptional_slippage_/1260540", "title"=>"Frameshifting is caused by transcriptional slippage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822148"], "description"=>"<p>(A) <i>C. rodentium</i> WT cells or <i>ΔtssM1</i> cells expressing WT <i>tssM1</i> (WT; producing both forms of TssM1: TssM1-FL and TssM1[1–807]) or TssM1 variants bearing mutations in the poly-A tract (AAG; producing only the TssM1[1–807] variant) or mutations in the poly-A tract and a deletion of the last nucleotide (AAGΔA; producing only the TssM1-FL variant). (B) <i>C. rodentium</i> cells producing the AAGΔA and AAG variants from the chromosome and producing the other variant from the pBAD18 vector. Hcp release assay (top panels). The extracellular proteins were isolated by separating whole cells (C) and the supernatant fraction (S). Proteins were visualized by Coomassie blue staining after 15%-acrylamide SDS-PAGE. Molecular mass markers are indicated on the left. Growth competition assay (bottom panels). Growth competition assay was monitored by mixing fluorescently labeled GFP<sup>+</sup><i>E. coli</i> W3110 prey cells with the indicated strains of <i>C. rodentium</i> as predators. Mixes were spotted onto LB agar supplemented with IPTG (500 µM) and arabinose (2%), and incubated for 14 h at 30°C. The relative fluorescence (upper graph) is expressed in arbitrary units (A.U.) and is the mean of fluorescence levels obtained from three independent experiments (each measured in triplicate). Fluorescent images of the competition assays (obtained with a LI-COR Odyssey imager) are shown below the upper graph.</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260543, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Both_TssM1_size_variants_are_required_for_activity_of_the_CTS1_T6SS_/1260543", "title"=>"Both TssM1 size variants are required for activity of the CTS1 T6SS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822178"], "description"=>"<p>Hcp release assays. <i>C. rodentium</i> Δ<i>tssM1</i> cells expressing WT <i>tssM1</i> (WT; producing both forms of TssM1: TssM1-FL and TssM1[1–807]) or TssM1 variants bearing mutations in the poly-A tract (AAG; producing only the TssM1[1–807] variant) or mutations in the poly-A tract and a deletion of the last nucleotide (AAG<i>Δ</i>A; producing only the TssM1-FL variant) from the pASK-IBA37+ vector (A) or producing the indicated variants from the pBAD18 and pASK-IBA37+ vectors (B). Extracellular proteins were isolated by separating whole cells (C) and the supernatant fraction (S) from cultures induced with arabinose and anhydrotetracyclin. TssM1 variants were immunodetected using the anti-FLAG monoclonal antibody (upper panels). The relative intensities of the short and long TssM1 variants are indicated (as %). Total proteins were visualized by Coomassie blue staining (lower panels). Molecular mass markers are indicated on the left.</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260556, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_ratio_between_the_two_TssM1_variants_is_critical_for_CTS1_T6SS_function_/1260556", "title"=>"The ratio between the two TssM1 variants is critical for CTS1 T6SS function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822187"], "description"=>"<p>(A) Representation of the nucleotide sequence of <i>Y. pseudotuberculosis tssM3</i>. The poly-A tract is shown in red. The codons and the amino-acids resulting from translation of the WT sequence, as well as those produced from +1 or +2 frameshifting are indicated with the size of the TssM3 variants. (B) Western-blot analyses of <i>Y. pseudotuberculosis</i> cells producing the TssM3 WT protein or a derivative mutated in the poly-A tract (AAG) bearing a FLAG-epitope tag at the N-terminus. Crude extracts from 10<sup>9</sup> cells were subjected to 10%-acrylamide SDS-PAGE and immunodetection using the anti-FLAG monoclonal antibody. The positions of the TssM3-FL and -[1–802] variants are indicated on the right using the schematic representation. The relative intensities of these two variants are indicated (as %). Molecular weight markers (in kDa) are indicated on the left. (C) Representation of the nucleotide sequence of <i>Y. pseudotuberculosis tssM3</i> constructs used for fluorescence studies shown in panel (D). The poly-A tract is shown in red and additional nucleotides are shown in blue. (D) Fluorescence levels (in arbitrary units, A.U.) of cells producing the different TssM1 variants shown in panel (C).</p>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260565, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcriptional_slippage_is_conserved_in_Y_pseudotuberculosis_/1260565", "title"=>"Transcriptional slippage is conserved in <i>Y. pseudotuberculosis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:18:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1822189", "https://ndownloader.figshare.com/files/1822190"], "description"=>"<div><p>The Type VI secretion system (T6SS) mediates toxin delivery into both eukaryotic and prokaryotic cells. It is composed of a cytoplasmic structure resembling the tail of contractile bacteriophages anchored to the cell envelope through a membrane complex composed of the TssL and TssM inner membrane proteins and of the TssJ outer membrane lipoprotein. The C-terminal domain of TssM is required for its interaction with TssJ, and for the function of the T6SS. In <i>Citrobacter rodentium</i>, the <i>tssM1</i> gene does not encode the C-terminal domain. However, the stop codon is preceded by a run of 11 consecutive adenosines. In this study, we demonstrate that this poly-A tract is a transcriptional slippery site that induces the incorporation of additional adenosines, leading to frameshifting, and hence the production of two TssM1 variants, including a full-length canonical protein. We show that both forms of TssM1, and the ratio between these two forms, are required for the function of the T6SS in <i>C. rodentium</i>. Finally, we demonstrate that the <i>tssM</i> gene associated with the <i>Yersinia pseudotuberculosis</i> T6SS-3 gene cluster is also subjected to transcriptional frameshifting.</p></div>", "links"=>[], "tags"=>["Transcriptional Frameshifting Rescues Citrobacter rodentium Type VI Secretion", "frameshifting", "tssM 1 gene", "TssM 1 variants", "type VI secretion system", "membrane", "T 6SS mediates toxin delivery", "Yersinia pseudotuberculosis T 6SS gene cluster", "function", "adenosine", "transcriptional", "T 6SS", "tssj", "protein", "Prematurely Interrupted tssM Gene"], "article_id"=>1260567, "categories"=>["Biological Sciences"], "users"=>["Erwan Gueguen", "Norma M. Wills", "John F. Atkins", "Eric Cascales"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004869.s001", "https://dx.doi.org/10.1371/journal.pgen.1004869.s002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Transcriptional_Frameshifting_Rescues_Citrobacter_rodentium_Type_VI_Secretion_by_the_Production_of_Two_Length_Variants_from_the_Prematurely_Interrupted_tssM_Gene/1260567", "title"=>"Transcriptional Frameshifting Rescues <i>Citrobacter rodentium</i> Type VI Secretion by the Production of Two Length Variants from the Prematurely Interrupted <i>tssM</i> Gene", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-04 03:18:21"}

PMC Usage Stats | Further Information

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Relative Metric

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