The Transcription Factors Atf1 and Pcr1 Are Essential for Transcriptional Induction of the Extracellular Maltase Agl1 in Fission Yeast
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{"title"=>"The transcription factors Atf1 and Pcr1 are essential for transcriptional induction of the extracellular maltase Agl1 in fission yeast", "type"=>"journal", "authors"=>[{"first_name"=>"Hiroaki", "last_name"=>"Kato", "scopus_author_id"=>"55628536148"}, {"first_name"=>"Shintaro", "last_name"=>"Kira", "scopus_author_id"=>"56001565000"}, {"first_name"=>"Makoto", "last_name"=>"Kawamukai", "scopus_author_id"=>"7006026304"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"372116619", "sgr"=>"84892415707", "issn"=>"19326203", "pmid"=>"24224056", "scopus"=>"2-s2.0-84892415707", "doi"=>"10.1371/journal.pone.0080572", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"c9108ac9-162d-3fb6-a696-5ca8c6e68a45", "abstract"=>"The fission yeast Schizosaccharomyces pombe secretes the extracellular maltase Agl1, which hydrolyzes maltose into glucose, thereby utilizing maltose as a carbon source. Whether other maltases contribute to efficient utilization of maltose and how Agl1 expression is regulated in response to switching of carbon sources are unknown. In this study, we show that three other possible maltases and the maltose transporter Sut1 are not required for efficient utilization of maltose. Transcription of agl1 was induced when the carbon source was changed from glucose to maltose. This was dependent on Atf1 and Pcr1, which are highly conserved transcription factors that regulate stress-responsive genes in various stress conditions. Atf1 and Pcr1 generally bind the TGACGT motif as a heterodimer. The agl1 gene lacks the exact motif, but has many degenerate TGACGT motifs in its promoter and coding region. When the carbon source was switched from glucose to maltose, Atf1 and Pcr1 associated with the promoters and coding regions of agl1, fbp1, and gpx1, indicating that the Atf1-Pcr1 heteromer binds a variety of regions in its target genes to induce their transcription. In addition, the association of Mediator with these genes was dependent on Atf1 and Pcr1. These data indicate that Atf1 and Pcr1 induce the transcription of agl1, which allows efficient utilization of extracellular maltose.", "link"=>"http://www.mendeley.com/research/transcription-factors-atf1-pcr1-essential-transcriptional-induction-extracellular-maltase-agl1-fissi", "reader_count"=>16, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>12, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Australia"=>1, "Chile"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1268818"], "description"=>"<p>(A) Med7 associates with <i>agl1</i> in maltose-utilizing cells. Cells expressing the indicated proteins were cultured as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3B</a> and used for ChIP analysis. The levels of the indicated proteins at the target regions of <i>agl1</i> (presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3A</a>) were normalized against the levels at <i>act1</i>. Glc: glucose; Mal: maltose. *<i>P</i><0.05, **<i>P</i><0.01 (Student's t-test). (B) The increased Med7 occupancy at <i>agl1</i> depends on Atf1 and Pcr1. Cells of the indicated strains were cultured as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3B</a> and used for ChIP analysis. The levels of Med7 associated with the indicated genes relative to the level of Med7 associated with <i>act1</i> in cells grown in maltose-containing medium. The fold change compared to levels in cells grown in glucose-containing medium is shown. Error bars, s.d. (n=3).</p>", "links"=>[], "tags"=>["associates", "genes", "switching", "carbon", "glucose", "maltose", "atf1-", "pcr1-dependent"], "article_id"=>842249, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080572.g005", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Med7_associates_with_its_target_genes_upon_switching_of_the_carbon_source_from_glucose_to_maltose_in_an_Atf1_and_Pcr1_dependent_manner_/842249", "title"=>"Med7 associates with its target genes upon switching of the carbon source from glucose to maltose in an Atf1- and Pcr1-dependent manner.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-05 03:12:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1268816"], "description"=>"<p>(A) Schematic representation of the <i>agl1</i> locus. Positions relative to the transcriptional start site of <i>agl1</i> are indicated. (B) Atf1 and Pcr1 are required to increase the mRNA level of <i>agl1</i>. Cells of the indicated strains exponentially growing in YE were washed twice, resuspended in YE or YEM, and incubated at 30°C for 2 hours. Total RNA was used for RT-PCR analysis. Expression levels of the indicated genes relative to the level of the constitutive <i>act1</i> gene in the indicated strains grown in maltose-containing medium. The fold change compared to levels in cells grown in glucose-containing medium is shown. (C) RNA polymerase II and histone H3 occupancy of <i>agl1</i> before and after the carbon source change. Wild-type cells cultured as described in (B) were used for ChIP analysis. The levels of RNA polymerase II and histone H3 at target regions of <i>agl1</i> that are presented in (A) were normalized against their levels at <i>act1</i>. Glc: glucose; Mal: maltose; Pol II: RNA polymerase II. *<i>P</i><0.05, **<i>P</i><0.01 (Student's t-test). (D) The increased RNA polymerase II occupancy at <i>agl1</i> depends on Atf1 and Pcr1. Cells of the indicated strains were cultured as described in (B) and then used for ChIP analysis of RNA polymerase II. Levels of RNA polymerase II associated with the indicated genes relative to the level associated with <i>act1</i> in cells grown in maltose-containing medium. The fold change compared to levels in cells grown in glucose-containing medium is shown. (E) The decreased histone H3 occupancy at <i>agl1</i> depends on Atf1. Cells of the indicated strains were cultured as described in (B) and then used for ChIP analysis of histone H3 as described in (D). Error bars, s.d. (n=3).</p>", "links"=>[], "tags"=>["pcr1", "positively", "agl1", "transcriptional"], "article_id"=>842247, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080572.g003", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Atf1_and_Pcr1_positively_regulate_the_expression_of_Agl1_at_the_transcriptional_level_/842247", "title"=>"Atf1 and Pcr1 positively regulate the expression of Agl1 at the transcriptional level.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-05 03:12:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1268817"], "description"=>"<p>(A) Atf1 and Pcr1 associate with <i>agl1</i> in maltose-utilizing cells. Cells expressing the indicated proteins were cultured as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3B</a> and used for ChIP analysis. The levels of the indicated proteins at the target regions of <i>agl1</i> (presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3A</a>) were normalized against their levels at <i>act1</i>. Glc: glucose; Mal: maltose. *<i>P</i><0.05, **<i>P</i><0.01 (Student's t-test). (B) The increased level of Atf1 at <i>agl1</i> depends upon Pcr1, and vice versa. Cells of the indicated strains were cultured as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080572#pone-0080572-g003\" target=\"_blank\">Figure 3B</a> and used for ChIP analysis. The levels of the indicated proteins associated with the indicated genes relative to the levels associated with <i>act1</i> in cells grown in maltose-containing medium. The fold change compared to levels in cells grown in glucose-containing medium is shown. Error bars, s.d. (n=3).</p>", "links"=>[], "tags"=>["pcr1", "genes", "switching", "carbon", "glucose", "maltose"], "article_id"=>842248, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080572.g004", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Atf1_and_Pcr1_associate_with_their_target_genes_upon_switching_of_the_carbon_source_from_glucose_to_maltose_in_a_manner_dependent_on_each_other_/842248", "title"=>"Atf1 and Pcr1 associate with their target genes upon switching of the carbon source from glucose to maltose in a manner dependent on each other.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-05 03:12:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1268815"], "description"=>"<p>(A) Suppression of the slow growth of <i>atf1∆</i> and <i>pcr1∆</i> mutants on maltose-containing medium by neighboring colonies requires the <i>agl1</i> gene. Strains (indicated on the left) were spotted onto the centers of YEM plates on which <i>atf1∆</i> or <i>pcr1∆</i> cells had been spread, and were incubated for 3 days at 30°C. (B) Model describing how neighboring wild-type colonies suppress the slow growth of mutant cells. Wild-type cells secrete the extracellular maltase Agl1 in an Atf1- and Pcr1-dependent manner. Agl1 hydrolyzes maltose into glucose, which is then taken up and utilized by the neighboring mutant cells. (C) Schematic representation of the four possible maltases in fission yeast. The positions of the glycoside hydrolase domains and the lengths (number of amino acids) of each protein are indicated. (D) The <i>agl1∆</i> mutant grows slowly on maltose-containing plates. The indicated strains were streaked onto plates containing the indicated sugar and incubated at 30°C for 3 days. (E) Growth of the <i>agl1∆</i> mutant does not recover following switching from glucose- to maltose- containing medium. Cells of the indicated strains exponentially growing in YE were washed twice, resuspended in YE or YEM, and incubated at 30°C for the indicated number of hours. (F) Additional deletion of possible maltase-encoding genes does not enhance the slow growth phenotype of <i>agl1∆</i> cells on YEM plates. The indicated strains were serially diluted, spotted onto plates containing the indicated sugars, and incubated at 30°C for 5 days. Note: wild-type cells must not be spotted onto the same plates in this experiment because they secrete Agl1 and thereby affect the growth of neighboring mutant colonies.</p>", "links"=>[], "tags"=>["maltose"], "article_id"=>842246, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080572.g002", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Agl1_is_responsible_for_efficient_maltose_utilization_/842246", "title"=>"Agl1 is responsible for efficient maltose utilization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-05 03:12:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1268820", "https://ndownloader.figshare.com/files/1268821", "https://ndownloader.figshare.com/files/1268822", "https://ndownloader.figshare.com/files/1268823", "https://ndownloader.figshare.com/files/1268824", "https://ndownloader.figshare.com/files/1268825"], "description"=>"<div><p>The fission yeast <i>Schizosaccharomyces pombe</i> secretes the extracellular maltase Agl1, which hydrolyzes maltose into glucose, thereby utilizing maltose as a carbon source. Whether other maltases contribute to efficient utilization of maltose and how Agl1 expression is regulated in response to switching of carbon sources are unknown. In this study, we show that three other possible maltases and the maltose transporter Sut1 are not required for efficient utilization of maltose. Transcription of <i>agl1</i> was induced when the carbon source was changed from glucose to maltose. This was dependent on Atf1 and Pcr1, which are highly conserved transcription factors that regulate stress-responsive genes in various stress conditions. Atf1 and Pcr1 generally bind the TGACGT motif as a heterodimer. The <i>agl1</i> gene lacks the exact motif, but has many degenerate TGACGT motifs in its promoter and coding region. When the carbon source was switched from glucose to maltose, Atf1 and Pcr1 associated with the promoters and coding regions of <i>agl1</i>, <i>fbp1</i>, and <i>gpx1</i>, indicating that the Atf1-Pcr1 heteromer binds a variety of regions in its target genes to induce their transcription. In addition, the association of Mediator with these genes was dependent on Atf1 and Pcr1. These data indicate that Atf1 and Pcr1 induce the transcription of <i>agl1</i>, which allows efficient utilization of extracellular maltose.</p> </div>", "links"=>[], "tags"=>["transcription", "atf1", "pcr1", "transcriptional", "induction", "extracellular", "maltase", "agl1", "fission"], "article_id"=>842250, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0080572.s001", "https://dx.doi.org/10.1371/journal.pone.0080572.s002", "https://dx.doi.org/10.1371/journal.pone.0080572.s003", "https://dx.doi.org/10.1371/journal.pone.0080572.s004", "https://dx.doi.org/10.1371/journal.pone.0080572.s005", "https://dx.doi.org/10.1371/journal.pone.0080572.s006"], "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Transcription_Factors_Atf1_and_Pcr1_Are_Essential_for_Transcriptional_Induction_of_the_Extracellular_Maltase_Agl1_in_Fission_Yeast_/842250", "title"=>"The Transcription Factors Atf1 and Pcr1 Are Essential for Transcriptional Induction of the Extracellular Maltase Agl1 in Fission Yeast", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-11-05 03:12:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1268814"], "description"=>"<p>(A) Fission yeast spores fail to form colonies when grown on maltose-containing medium. Wild-type (mating-type: <i>h</i><sup>90</sup>) tetrads were dissected on YE (glucose-containing) and YEM (maltose-containing) plates, and incubated at 30°C for 3 days. (B) <i>atf1∆</i> and <i>pcr1∆</i> mutants grow slowly on maltose-containing plates. Wild-type, <i>atf1∆</i>, and <i>pcr1∆</i> strains were streaked on plates containing the indicated sugar(s) and incubated at 30°C for 3 days. (C) Growth of <i>atf1∆</i> and <i>pcr1∆</i> mutants does not recover following switching from glucose- to maltose-containing medium. Cells of the indicated strains exponentially growing in YE were washed twice, resuspended in YE or YEM, and incubated at 30°C for the indicated number of hours. </p>", "links"=>[], "tags"=>["pcr1", "maltose"], "article_id"=>842245, "categories"=>["Biological Sciences"], "users"=>["Hiroaki Kato", "Shintaro Kira", "Makoto Kawamukai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080572.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Atf1_and_Pcr1_are_required_for_efficient_maltose_utilization_/842245", "title"=>"Atf1 and Pcr1 are required for efficient maltose utilization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-05 03:12:10"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"4", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"7", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"2", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"10", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[284, 491, 620, 738, 843, 945, 1043, 1137, 1225, 1315, 1400, 1479, 1555]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[254, 431, 547, 651, 748, 842, 932, 1017, 1098, 1178, 1259, 1336, 1404]}, {"subject_area"=>"/Physical sciences/Chemistry", "average_usage"=>[247, 429, 544, 647, 747, 842, 929, 1012, 1099, 1179, 1263, 1339, 1409]}]}
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