The Streptococcus pneumoniae Pilus-1 Displays a Biphasic Expression Pattern
Publication Date
June 22, 2011
Journal
PLOS ONE
Authors
Gabriella De Angelis, Monica Moschioni, Alessandro Muzzi, Alfredo Pezzicoli, et al
Volume
6
Issue
6
Pages
e21269
DOI
https://dx.plos.org/10.1371/journal.pone.0021269
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0021269
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21731688
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3120856
Europe PMC
http://europepmc.org/abstract/MED/21731688
Web of Science
000292033700054
Scopus
79959464867
Mendeley
http://www.mendeley.com/research/streptococcus-pneumoniae-pilus1-displays-biphasic-expression-pattern
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Mendeley | Further Information

{"title"=>"The streptococcus pneumoniae Pilus-1 displays a biphasic expression pattern", "type"=>"journal", "authors"=>[{"first_name"=>"Gabriella", "last_name"=>"de Angelis", "scopus_author_id"=>"35338810800"}, {"first_name"=>"Monica", "last_name"=>"Moschioni", "scopus_author_id"=>"6508124734"}, {"first_name"=>"Alessandro", "last_name"=>"Muzzi", "scopus_author_id"=>"23474621400"}, {"first_name"=>"Alfredo", "last_name"=>"Pezzicoli", "scopus_author_id"=>"14421308000"}, {"first_name"=>"Stefano", "last_name"=>"Censini", "scopus_author_id"=>"6701795733"}, {"first_name"=>"Isabel", "last_name"=>"Delany", "scopus_author_id"=>"6602488716"}, {"first_name"=>"Morena Lo", "last_name"=>"Sapio", "scopus_author_id"=>"56622826900"}, {"first_name"=>"Antonia", "last_name"=>"Sinisi", "scopus_author_id"=>"26868142600"}, {"first_name"=>"Claudio", "last_name"=>"Donati", "scopus_author_id"=>"7003921934"}, {"first_name"=>"Vega", "last_name"=>"Masignani", "scopus_author_id"=>"6603149430"}, {"first_name"=>"Michèle A.", "last_name"=>"Barocchi", "scopus_author_id"=>"12752355200"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-79959464867", "sgr"=>"79959464867", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0021269", "pmid"=>"21731688", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"361997116"}, "id"=>"a3da1a38-af29-343a-ba87-58f3c042872b", "abstract"=>"The Streptococcus pneumoniae pilus-1 is encoded by pilus islet 1 (PI-1), which has three clonal variants (clade I, II and III) and is present in about 30% of clinical pneumococcal isolates. In vitro and in vivo assays have demonstrated that pilus-1 is involved in attachment to epithelial cells and virulence, as well as protection in mouse models of infection. Several reports suggest that pilus-1 expression is tightly regulated and involves the interplay of numerous genetic regulators, including the PI-1 positive regulator RlrA. In this report we provide evidence that pilus expression, when analyzed at the single-cell level in PI-1 positive strains, is biphasic. In fact, the strains present two phenotypically different sub-populations of bacteria, one that expresses the pilus, while the other does not. The proportions of these two phenotypes are variable among the strains tested and are not influenced by genotype, serotype, growth conditions, colony morphology or by the presence of antibodies directed toward the pilus components. Two sub-populations, enriched in pilus expressing or not expressing bacteria were obtained by means of colony selection and immuno-detection methods for five strains. PI-1 sequencing in the two sub-populations revealed the absence of mutations, thus indicating that the biphasic expression observed is not due to a genetic modification within PI-1. Microarray expression profile and western blot analyses on whole bacterial lysates performed comparing the two enriched sub-populations, revealed that pilus expression is regulated at the transcriptional level (on/off regulation), and that there are no other genes, in addition to those encoded by PI-1, concurrently regulated across the strains tested. Finally, we provide evidence that the over-expression of the RrlA positive regulator is sufficient to induce pilus expression in pilus-1 negative bacteria. Overall, the data presented here suggest that the observed biphasic pilus expression phenotype could be an example of bistability in pneumococcus", "link"=>"http://www.mendeley.com/research/streptococcus-pneumoniae-pilus1-displays-biphasic-expression-pattern", "reader_count"=>22, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Master"=>1, "Other"=>1, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Master"=>1, "Other"=>1, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Italy"=>1}, "group_count"=>2}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/383514", "https://ndownloader.figshare.com/files/383550", "https://ndownloader.figshare.com/files/383609", "https://ndownloader.figshare.com/files/383663", "https://ndownloader.figshare.com/files/383714", "https://ndownloader.figshare.com/files/383771", "https://ndownloader.figshare.com/files/383809", "https://ndownloader.figshare.com/files/383850"], "description"=>"<div><p>The <em>Streptococcus pneumoniae</em> pilus-1 is encoded by pilus islet 1 (PI-1), which has three clonal variants (clade I, II and III) and is present in about 30% of clinical pneumococcal isolates. <em>In vitro</em> and <em>in vivo</em> assays have demonstrated that pilus-1 is involved in attachment to epithelial cells and virulence, as well as protection in mouse models of infection. Several reports suggest that pilus-1 expression is tightly regulated and involves the interplay of numerous genetic regulators, including the PI-1 positive regulator RlrA. In this report we provide evidence that pilus expression, when analyzed at the single-cell level in PI-1 positive strains, is biphasic. In fact, the strains present two phenotypically different sub-populations of bacteria, one that expresses the pilus, while the other does not. The proportions of these two phenotypes are variable among the strains tested and are not influenced by genotype, serotype, growth conditions, colony morphology or by the presence of antibodies directed toward the pilus components. Two sub-populations, enriched in pilus expressing or not expressing bacteria were obtained by means of colony selection and immuno-detection methods for five strains. PI-1 sequencing in the two sub-populations revealed the absence of mutations, thus indicating that the biphasic expression observed is not due to a genetic modification within PI-1. Microarray expression profile and western blot analyses on whole bacterial lysates performed comparing the two enriched sub-populations, revealed that pilus expression is regulated at the transcriptional level (on/off regulation), and that there are no other genes, in addition to those encoded by PI-1, concurrently regulated across the strains tested. Finally, we provide evidence that the over-expression of the RrlA positive regulator is sufficient to induce pilus expression in pilus-1 negative bacteria. Overall, the data presented here suggest that the observed biphasic pilus expression phenotype could be an example of bistability in pneumococcus.</p> </div>", "links"=>[], "tags"=>["pilus-1", "displays", "biphasic"], "article_id"=>135737, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.s001", "https://dx.doi.org/10.1371/journal.pone.0021269.s002", "https://dx.doi.org/10.1371/journal.pone.0021269.s003", "https://dx.doi.org/10.1371/journal.pone.0021269.s004", "https://dx.doi.org/10.1371/journal.pone.0021269.s005", "https://dx.doi.org/10.1371/journal.pone.0021269.s006", "https://dx.doi.org/10.1371/journal.pone.0021269.s007", "https://dx.doi.org/10.1371/journal.pone.0021269.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Streptococcus_pneumoniae_Pilus_1_Displays_a_Biphasic_Expression_Pattern/135737", "title"=>"The <em>Streptococcus pneumoniae</em> Pilus-1 Displays a Biphasic Expression Pattern", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-06-22 01:35:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/762670"], "description"=>"<p>A) TIGR4 bacteria were labeled with anti-RrgA, RrgB clade I, RrgC, BgaA (beta-galactosidase), PhtA (pneumococcal histidine triad protein A) or PspC (pneumococcal surface protein C, also known as CbpA,) primary antibodies (1∶400 dilution), and with FITC anti-mouse IgG secondary antibodies (1∶100 dilution). Bacterial staining was analyzed by flow cytometry (FACS-Calibur). Sera of mice immunized with PBS were used as negative control. B,C) TIGR4 bacteria were processed for immunofluorescence, stained with mouse anti-RrgB antibodies (1∶2000 dilution) (red) and with <i>S. pneumoniae</i> anti-capsular antibodies (Omniserum 1∶2000 dilution) (green). Imaging was performed with a confocal microscope. Scale bar is 4 µm in panel B and 1 µm in panel C.</p>", "links"=>[], "tags"=>["components", "biphasic"], "article_id"=>433037, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pilus_components_display_a_biphasic_expression_pattern_/433037", "title"=>"Pilus components display a biphasic expression pattern.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 00:50:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/762786"], "description"=>"<p>Bacteria containing either PI-1 clade I (A), clade II (B) or clade III (C), were labeled with clade specific anti-RrgB antibodies (1∶400 dilution) and FITC anti-mouse IgG secondary antibodies (1∶100 dilution). Pilus-1 expression was then analyzed by flow cytometry (FACS-Calibur).</p>", "links"=>[], "tags"=>["correlated", "genotype", "clade"], "article_id"=>433148, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pilus_expression_ratio_is_not_correlated_with_serotype_genotype_or_clade_type_/433148", "title"=>"Pilus expression ratio is not correlated with serotype, genotype or clade type.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 00:52:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/762909"], "description"=>"<p>A) TIGR4 pilus-1 expression was revealed on single colonies by colony immunoblot using anti-RrgB clade I antibodies (green, black and red circles correspond to colonies displaying low, medium or high RrgB specific signal intensities, respectively). Bacteria recovered from the growth of different colonies were stained with anti-RrgB clade I antibodies and analyzed by flow cytometry (B). The bacteria expressing (Pil+) and non- expressing (Pil-) the pilus-1 are indicated in the L (green) and H (red) enriched sub-populations, and in the wt (black). H and L sub-populations were stained for immunofluorescence (C and D). Bacteria were incubated with mouse anti-RrgB antibodies (1∶2000 dilution) (red) and with <i>S.pneumoniae</i> anti-capsular antibodies (Omniserum 1∶2000 dilution) (green). Imaging was performed with a confocal microscope. Scale bar is 5 µm.</p>", "links"=>[], "tags"=>["enriched", "pilus-1", "expressing"], "article_id"=>433275, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stable_separation_of_enriched_high_H_and_low_L_pilus_1_expressing_sub_populations_/433275", "title"=>"Stable separation of enriched high (H) and low (L) pilus-1 expressing sub-populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 00:54:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/763062"], "description"=>"<p>WB analysis performed on whole bacterial lysates of TIGR4 H (H), L (L) or TIGR4 L depleted of RrgB positive bacteria (D), using polyclonal mouse antisera against RrgA, RrgB, RrgC (see High molecular weight ladders), SrtC-1, SrtC-2 ,SrtC-3 (see bands indicated by arrows) and SrtA (used as loading control).</p>", "links"=>[], "tags"=>["encoded", "proteins", "rrgb"], "article_id"=>433428, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI_1_encoded_proteins_are_not_expressed_in_RrgB_negative_bacteria_/433428", "title"=>"PI-1 encoded proteins are not expressed in RrgB negative bacteria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 00:57:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/763163"], "description"=>"<p><b>A)</b> High and low pilus expressing sub-populations of strains TIGR4 (Clade I), 19F Taiwan 14 (Clade I), OREP4 (Clade I), 6B Finland 14 (Clade II) and 35B SME 15 (Clade III) were labeled with clade specific anti-RrgB antibodies (1∶400 dilution) and FITC anti-mouse IgG secondary antibodies (1∶100 dilution). Pilus-1 expression was then analyzed by flow cytometry (FACS-Calibur). <b>B)</b> Schematic representation of PI-1. <b>C)</b> Log<sub>2</sub> ratio values indicating the PI-1 genes differential expression in High vs. Low pilus expressing sub-populations in the five above mentioned strains, as measured by spotted DNA microarray analysis. The data are measures of relative gene expression during <i>in vitro</i> growth in liquid cultures. The values reported for each gene are the mean of all the spots and their replicates within the array and of two independent experiments (bars represent standard deviations). <b>D)</b> Absolute gene expression levels of PI-1 genes measured for TIGR4 high and low pilus expressing sub-populations by microarray hybridization. Absolute expression levels reported for each gene are the mean of all the spots and their replicates within the array and of two independent experiments (bars represent the obtained standard deviations).</p>", "links"=>[], "tags"=>["regulated", "transcriptional"], "article_id"=>433525, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pilus_1_expression_is_regulated_at_the_transcriptional_level_/433525", "title"=>"Pilus-1 expression is regulated at the transcriptional level.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 00:58:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/763282"], "description"=>"<p>TIGR4 low pilus expressing bacteria transformed with <i>pMU1328</i> (panels A-C), <i>pMU1328-Pc-rlrA</i> (panels D-F), with <i>pMU1328-Pc-rrgB</i> (panels G-I) or with <i>pMU1328-Pc-srtC-2</i> (panels J-L) were processed for confocal microscopy immuno-fluorescence analysis by incubating <i>S. pneumoniae</i> with anti-capsular antibodies (Omniserum 1∶2000 dilution) (green, left panels) and mouse anti-RrgB antibodies (1∶2000 dilution) (red, central panels). Right panels represent the merged signal of the left and central panels. Scale bar is 4 µm.</p>", "links"=>[], "tags"=>["pilus", "induces"], "article_id"=>433648, "categories"=>["Genetics", "Microbiology"], "users"=>["Gabriella De Angelis", "Monica Moschioni", "Alessandro Muzzi", "Alfredo Pezzicoli", "Stefano Censini", "Isabel Delany", "Morena Lo Sapio", "Antonia Sinisi", "Claudio Donati", "Vega Masignani", "Michèle A. Barocchi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021269.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RlrA_expression_in_pilus_negative_Pil_bacteria_induces_pilus_polymerization_/433648", "title"=>"RlrA expression in pilus negative (Pil-) bacteria induces pilus polymerization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-22 01:00:48"}

PMC Usage Stats | Further Information

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