The HIV-1 Rev Protein Enhances Encapsidation of Unspliced and Spliced, RRE-Containing Lentiviral Vector RNA
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{"title"=>"The HIV-1 Rev Protein Enhances Encapsidation of Unspliced and Spliced, RRE-Containing Lentiviral Vector RNA", "type"=>"journal", "authors"=>[{"first_name"=>"Bastian", "last_name"=>"Grewe", "scopus_author_id"=>"16244739200"}, {"first_name"=>"Katrin", "last_name"=>"Ehrhardt", "scopus_author_id"=>"36155278400"}, {"first_name"=>"Bianca", "last_name"=>"Hoffmann", "scopus_author_id"=>"56277650700"}, {"first_name"=>"Maik", "last_name"=>"Blissenbach", "scopus_author_id"=>"16243934400"}, {"first_name"=>"Sabine", "last_name"=>"Brandt", "scopus_author_id"=>"57197893347"}, {"first_name"=>"Klaus", "last_name"=>"Überla", "scopus_author_id"=>"7006244554"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23133650", "issn"=>"19326203", "sgr"=>"84868311398", "pui"=>"365979043", "scopus"=>"2-s2.0-84868311398", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0048688"}, "id"=>"6b7848d5-bcc4-32e0-9316-645f7b204e3b", "abstract"=>"BACKGROUND During the RNA encapsidation process of human immunodeficiency virus (HIV) viral genomic, unspliced RNA (gRNA) is preferentially incorporated into assembling virions. However, a certain amount of spliced viral transcripts can also be detected in viral particles. Recently, we observed that nuclear export of HIV and lentiviral vector gRNA by Rev is required for efficient encapsidation. Since singly-spliced HIV transcripts also contain the Rev-response element (RRE), we investigated if the encapsidation efficiency of RRE-containing spliced HIV-vector transcripts is also increased by the viral Rev protein. FINDINGS Starting with a lentiviral vector imitating the splicing pattern of HIV, we constructed vectors that express an unspliced transcript either identical in sequence to the singly-spliced or the fully-spliced RNA of the parental construct. After transfection of the different lentiviral vectors cytoplasmic and virion-associated RNA levels and vector titers were determined in the presence and absence of Rev. Rev enhanced the infectious titer of vectors containing an RRE 6 to 37-fold. Furthermore, Rev strongly increased encapsidation efficiencies of all RRE-containing transcripts up to 200-fold. However, a good correlation between encapsidation efficiency and lentiviral vector titer could only be observed for the gRNA. The infectious titer of the vector encoding the fully-spliced RNA without RRE as well as the encapsidation efficiency of all transcripts lacking the RRE was not influenced by Rev. Interestingly, the splicing process itself did not seem to interfere with packaging, since the encapsidation efficiencies of the same RNA expressed either by splicing or as an unspliced transcript did not differ significantly. CONCLUSIONS Rev-mediated nuclear export enhances the encapsidation efficiency of RRE-containing lentiviral vector RNAs independently of whether they have been spliced or not.", "link"=>"http://www.mendeley.com/research/hiv1-rev-protein-enhances-encapsidation-unspliced-spliced-rrecontaining-lentiviral-vector-rna", "reader_count"=>24, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>2, "Other"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>2, "Other"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>9, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "France"=>1, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/293961"], "description"=>"<div><h3>Background</h3><p>During the RNA encapsidation process of human immunodeficiency virus (HIV) viral genomic, unspliced RNA (gRNA) is preferentially incorporated into assembling virions. However, a certain amount of spliced viral transcripts can also be detected in viral particles. Recently, we observed that nuclear export of HIV and lentiviral vector gRNA by Rev is required for efficient encapsidation. Since singly-spliced HIV transcripts also contain the Rev-response element (RRE), we investigated if the encapsidation efficiency of RRE-containing spliced HIV-vector transcripts is also increased by the viral Rev protein.</p> <h3>Findings</h3><p>Starting with a lentiviral vector imitating the splicing pattern of HIV, we constructed vectors that express an unspliced transcript either identical in sequence to the singly-spliced or the fully-spliced RNA of the parental construct. After transfection of the different lentiviral vectors cytoplasmic and virion-associated RNA levels and vector titers were determined in the presence and absence of Rev. Rev enhanced the infectious titer of vectors containing an RRE 6 to 37-fold. Furthermore, Rev strongly increased encapsidation efficiencies of all RRE-containing transcripts up to 200-fold. However, a good correlation between encapsidation efficiency and lentiviral vector titer could only be observed for the gRNA. The infectious titer of the vector encoding the fully-spliced RNA without RRE as well as the encapsidation efficiency of all transcripts lacking the RRE was not influenced by Rev. Interestingly, the splicing process itself did not seem to interfere with packaging, since the encapsidation efficiencies of the same RNA expressed either by splicing or as an unspliced transcript did not differ significantly.</p> <h3>Conclusions</h3><p>Rev-mediated nuclear export enhances the encapsidation efficiency of RRE-containing lentiviral vector RNAs independently of whether they have been spliced or not.</p> </div>", "links"=>[], "tags"=>["hiv-1", "rev", "enhances", "encapsidation", "unspliced", "rre-containing", "lentiviral", "vector", "rna"], "article_id"=>117875, "categories"=>["Molecular Biology", "Cancer", "Microbiology"], "users"=>["Bastian Grewe", "Katrin Ehrhardt", "Bianca Hoffmann", "Maik Blissenbach", "Sabine Brandt", "Klaus Überla"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0048688"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_HIV_1_Rev_Protein_Enhances_Encapsidation_of_Unspliced_and_Spliced_RRE_Containing_Lentiviral_Vector_RNA__/117875", "title"=>"The HIV-1 Rev Protein Enhances Encapsidation of Unspliced and Spliced, RRE-Containing Lentiviral Vector RNA", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-11-01 02:11:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/549818"], "description"=>"<p>A) The HIV-1 provirus NL4.3 and the HIV-1-vector V<sup>H</sup>genomic are shown. Large parts of the <i>gag, pol</i> and <i>env</i> genes are deleted in V<sup>H</sup>genomic (see white bars in the deleted regions marked by shaded areas). The remaining <i>gag</i> sequence contains parts of the encapsidation signal (Psi, Ψ) and the <i>env</i> fragments contain splicing regulatory elements as well as the RRE. Due to deletions (shaded squares) and frameshift mutations (black asterisks in <i>gag</i> and <i>rev</i>) no viral genes are expressed from V<sup>H</sup>genomic. Both vectors are drawn to scale. B) Schematic representation of the lentiviral vectors V<sup>H</sup>genomic, V<sup>H</sup>env and V<sup>H</sup>nef. The intron between SD1 and SA5 or the introns between SD1 and SA5 and between SD4 and SA7 were deleted from V<sup>H</sup>genomic in V<sup>H</sup>env or V<sup>H</sup>nef, respectively. Unspliced and spliced transcripts with splice sites (5′ splice sites in green and 3′ splice sites in blue) and <i>cis</i>-acting splicing regulatory elements (in orange) are shown. Please note that the unspliced Msd1-sa5 RNA of V<sup>H</sup>env is identical in sequence to the singly-spliced SD1-SA5 RNA of V<sup>H</sup>genomic. Furthermore, the unspliced Msd1-sa5+Msd4-sa7 RNA of V<sup>H</sup>nef is identical to the fully-spliced SD1-SA5+SD4-SA7 RNA of V<sup>H</sup>genomic and the singly-spliced Msd1-sa5+SD4-SA7 RNA of V<sup>H</sup>env. Arrowheads represent RT-PCR primers. C) and D) After cotransfection of lentiviral vectors with <i>tat</i> and <i>rev</i> expression plasmids into HEK293T cells cytoplasmic RNA was isolated and analyzed by RT-PCR with primer pairs depicted in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048688#pone-0048688-g001\" target=\"_blank\">figure 1B</a>. Agarose gel electrophoretic analyses of PCR products are shown. The amplification products were sequenced to verify splicing between the indicated splice sites.</p>", "links"=>[], "tags"=>["lentiviral"], "article_id"=>220310, "categories"=>["Microbiology", "Molecular Biology", "Virology", "Infectious Diseases"], "users"=>["Bastian Grewe", "Katrin Ehrhardt", "Bianca Hoffmann", "Maik Blissenbach", "Sabine Brandt", "Klaus Überla"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0048688.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Construction_of_lentiviral_vectors_/220310", "title"=>"Construction of lentiviral vectors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-01 00:05:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/549940"], "description"=>"<p>A) Cellular lysates and viral particles were harvested two days after transfection of HEK293T cells and were analyzed by an anti-CA Western Blot. The expression plasmid UTRgpRRE contains wild type <i>gag/gagpol</i> gene sequences combined with a part of the viral 5′UTR and the RRE. The Rev-independent <i>gag/gagpol</i> expression plasmid Hgp<sup>syn</sup> encodes proteins with wild type amino acid sequences but the gene sequence is dramatically altered due to codon-optimization. B) HEK293 cells were infected with supernatants containing VSV-G pseudotyped lentiviral vectors produced in the presence or absence of Rev. Constant high Gag/GagPol protein levels were provided during vector production by cotransfection of the Rev-independent codon-optimized expression plasmid Hgp<sup>syn</sup>. Two days later green fluorescent cells were counted to obtain the infectious titer as GFP forming units per ml of cell culture supernatant (GFU/ml). Titer of the negative control without VSV-G and Gag/GagPol was below 50 GFU/ml (data not shown). Mean values with SEM (standard error of mean) of log10 transformed results obtained in at least 4 independent experiments are shown. Statistical analysis was performed with an unpaired two-tailed t-test with 95% confidence interval. ***, p≤0.001; **, p≤0.01; *, p≤0.05; n.s., not statistically significant.</p>", "links"=>[], "tags"=>["infectious", "lentiviral", "vector"], "article_id"=>220428, "categories"=>["Microbiology", "Molecular Biology", "Virology", "Infectious Diseases"], "users"=>["Bastian Grewe", "Katrin Ehrhardt", "Bianca Hoffmann", "Maik Blissenbach", "Sabine Brandt", "Klaus Überla"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0048688.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rev_dependency_of_the_infectious_lentiviral_vector_titer_/220428", "title"=>"Rev-dependency of the infectious lentiviral vector titer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-01 00:07:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/550054"], "description"=>"<p>A) Cytoplasmic RNA was extracted two days after transfection and analyzed using quantitative RT-PCR protocols (please see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048688#pone.0048688.s001\" target=\"_blank\">Materials and Methods S1</a> for experimental details). Transcript copy numbers per µg of cytoplasmic RNA are shown. B) Virion-associated RNA was isolated from cell culture supernatants of cells analyzed in A. Transcript copy numbers per ml of cellular supernatant were obtained after RT-qPCR analyses. Unspliced RNA levels of V<sup>H</sup>genomic are shown in green. RNA levels of the singly-spliced SD1-SA5 RNA of V<sup>H</sup>genomic and the unspliced Msd1-sa5 transcript of V<sup>H</sup>env are depicted in blue. These RNAs represent the class of singly-spliced transcripts. Shown in red are transcript levels of the multiply-spliced SD1-SA5+SD4-SA7 RNA of V<sup>H</sup>genomic, the singly-spliced Msd1-sa5+SD4-SA7 RNA of V<sup>H</sup>env and the unspliced Msd1-sa5+Msd4-sa7 RNA of V<sup>H</sup>nef. These RNAs correspond to the class of fully-spliced transcripts. Mean values with SEM of log10 transformed RNA copy numbers obtained in 5 independent experiments are shown. Statistical analysis was performed with a one-way ANOVA combined with the Newman-Keuls post-test. ***, p≤0.001; **, p≤0.01; *, p≤0.05; n.s., not statistically significant.</p>", "links"=>[], "tags"=>["virion-associated", "lentiviral", "vector", "rna", "levels"], "article_id"=>220539, "categories"=>["Microbiology", "Molecular Biology", "Virology", "Infectious Diseases"], "users"=>["Bastian Grewe", "Katrin Ehrhardt", "Bianca Hoffmann", "Maik Blissenbach", "Sabine Brandt", "Klaus Überla"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0048688.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cytoplasmic_and_virion_associated_lentiviral_vector_RNA_levels_in_the_presence_and_absence_of_Rev_/220539", "title"=>"Cytoplasmic and virion-associated lentiviral vector RNA levels in the presence and absence of Rev.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-01 00:08:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/550164"], "description"=>"<p>The ratio of virion-associated and cytoplasmic RNA levels defines the encapsidation efficiency for all lentiviral vector transcripts detected. The log10 transformed ratios were calculated for each single data pair obtained in each single experiment for all the different RNA species examined. Mean values with SEM obtained are shown. Statistical analysis was performed with a one-way ANOVA combined with the Newman-Keuls post-test. ***, p≤0.001; **, p≤0.01; *, p≤0.05; n.s., not statistically significant.</p>", "links"=>[], "tags"=>["Virology", "Infectious diseases", "microbiology", "molecular biology"], "article_id"=>220657, "categories"=>["Microbiology", "Molecular Biology", "Virology", "Infectious Diseases"], "users"=>["Bastian Grewe", "Katrin Ehrhardt", "Bianca Hoffmann", "Maik Blissenbach", "Sabine Brandt", "Klaus Überla"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0048688.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Encapsidation_efficiency_in_the_presence_and_absence_of_Rev_/220657", "title"=>"Encapsidation efficiency in the presence and absence of Rev.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-01 00:10:57"}

PMC Usage Stats | Further Information

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Relative Metric

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