Cardiac Development in Zebrafish and Human Embryonic Stem Cells Is Inhibited by Exposure to Tobacco Cigarettes and E-Cigarettes
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{"title"=>"Cardiac development in zebrafish and human embryonic stem cells is inhibited by exposure to tobacco cigarettes and ecigarettes", "type"=>"journal", "authors"=>[{"first_name"=>"Nathan J.", "last_name"=>"Palpant", "scopus_author_id"=>"19934254600"}, {"first_name"=>"Peter", "last_name"=>"Hofsteen", "scopus_author_id"=>"55595942500"}, {"first_name"=>"Lil", "last_name"=>"Pabon", "scopus_author_id"=>"13105276800"}, {"first_name"=>"Hans", "last_name"=>"Reinecke", "scopus_author_id"=>"35511668800"}, {"first_name"=>"Charles E.", "last_name"=>"Murry", "scopus_author_id"=>"7006341337"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"604392700", "sgr"=>"84929340188", "issn"=>"19326203", "pmid"=>"25978043", "scopus"=>"2-s2.0-84929340188", "doi"=>"10.1371/journal.pone.0126259", "isbn"=>"10.1371/journal.pone.0126259"}, "id"=>"2f5368aa-21f2-303f-83f5-daad65e618ac", "abstract"=>"BACKGROUND Maternal smoking is a risk factor for low birth weight and other adverse developmental outcomes. OBJECTIVE We sought to determine the impact of standard tobacco cigarettes and e-cigarettes on heart development in vitro and in vivo. METHODS Zebrafish (Danio rerio) were used to assess developmental effects in vivo and cardiac differentiation of human embryonic stem cells (hESCs) was used as a model for in vitro cardiac development. RESULTS In zebrafish, exposure to both types of cigarettes results in broad, dose-dependent developmental defects coupled with severe heart malformation, pericardial edema and reduced heart function. Tobacco cigarettes are more toxic than e-cigarettes at comparable nicotine concentrations. During cardiac differentiation of hESCs, tobacco smoke exposure results in a delayed transition through mesoderm. Both types of cigarettes decrease expression of cardiac transcription factors in cardiac progenitor cells, suggesting a persistent delay in differentiation. In definitive human cardiomyocytes, both e-cigarette- and tobacco cigarette-treated samples showed reduced expression of sarcomeric genes such as MLC2v and MYL6. Furthermore, tobacco cigarette-treated samples had delayed onset of beating and showed low levels and aberrant localization of N-cadherin, reduced myofilament content with significantly reduced sarcomere length, and increased expression of the immature cardiac marker smooth muscle alpha-actin. CONCLUSION These data indicate a negative effect of both tobacco cigarettes and e-cigarettes on heart development in vitro and in vivo. Tobacco cigarettes are more toxic than E-cigarettes and exhibit a broader spectrum of cardiac developmental defects.", "link"=>"http://www.mendeley.com/research/cardiac-development-zebrafish-human-embryonic-stem-cells-inhibited-exposure-tobacco-cigarettes-eciga", "reader_count"=>51, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>5, "Researcher"=>3, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Other"=>4, "Student > Master"=>7, "Student > Bachelor"=>9, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Student > Doctoral Student"=>5, "Researcher"=>3, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Other"=>4, "Student > Master"=>7, "Student > Bachelor"=>9, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>9, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemistry"=>1, "Psychology"=>4, "Social Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Psychology"=>{"Psychology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"United Kingdom"=>1}, "group_count"=>10}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2070959"], "description"=>"<p>(a) Expression level of cardiac transcription factors GATA4 and NKX2.5 (a) and calcium handling proteins including the L-type calcium channel and SERCA2a, and the junctional protein CNX43 (b) by quantitative RT-PCR in cells treated with 6.8 μM e-cigarette or tobacco cigarette extracts vs. control. (c-d) Representative immunocytochemistry (c) and quantification (e) for NKX2.5 in fetal cardiomyocytes with various cigarette treatments compared to control. (e-f) Representative immunohistochemistry (e) and quantification (f) for the junction protein cadherin in fetal hESC cardiomyocytes with various cigarette treatments compared to control. Inset shown to the right. Arrows indicate perinuclear expression of cadherin. n ≥ 6 per group. Scale bar = 100 μm. * P < 0.05.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417352, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g005", "stats"=>{"downloads"=>0, "page_views"=>53, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_hESC_derived_fetal_cardiomyocyte_transcription_factor_calcium_handling_and_junction_protein_expression_/1417352", "title"=>"Analysis of hESC derived fetal cardiomyocyte transcription factor, calcium handling, and junction protein expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070932"], "description"=>"<p>Assessment of zebrafish survival over 72 h with increasing concentrations of pure nicotine, e-cigarettes and tobacco cigarettes extracts or vehicle control (0.1% DMSO). n ≥ 3 (independent experiments with each n containing between 24–48 animals per treatment). * P < 0.05, hpe = hours post exposure.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417333, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g001", "stats"=>{"downloads"=>3, "page_views"=>74, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Zebrafish_embryo_larval_survival_analysis_following_escalating_doses_of_nicotine_e_cigarette_and_tobacco_extracts_/1417333", "title"=>"Zebrafish embryo-larval survival analysis following escalating doses of nicotine, e-cigarette and tobacco extracts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070954"], "description"=>"<p>(a) Timeline of differentiation protocol for cardiac directed differentiation of hESCs. (b-e) Analysis of cardiac endpoints including intrinsic beating rate (b) cardiomyocyte yield (c), cardiomyocyte purity (d), and cardiomyocyte immaturity based on percent cTnT<sup>+</sup>/SMA<sup>+</sup> (e) and representative flow cytometry plots (f) on day 14 of differentiation with increasing doses of purified e-cigarette and tobacco cigarette extracts. n ≥ 6 per group. * P < 0.05.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417347, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g003", "stats"=>{"downloads"=>1, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_e_cigarette_and_tobacco_cigarette_on_hESC_cardiac_differentiation_/1417347", "title"=>"Analysis of e-cigarette and tobacco cigarette on hESC cardiac differentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070968", "https://ndownloader.figshare.com/files/2070969", "https://ndownloader.figshare.com/files/2070970", "https://ndownloader.figshare.com/files/2070971", "https://ndownloader.figshare.com/files/2070972"], "description"=>"<div><p>Background</p><p>Maternal smoking is a risk factor for low birth weight and other adverse developmental outcomes.</p><p>Objective</p><p>We sought to determine the impact of standard tobacco cigarettes and e-cigarettes on heart development <i>in vitro</i> and <i>in vivo</i>.</p><p>Methods</p><p>Zebrafish (<i>Danio rerio</i>) were used to assess developmental effects <i>in vivo</i> and cardiac differentiation of human embryonic stem cells (hESCs) was used as a model for <i>in vitro</i> cardiac development.</p><p>Results</p><p>In zebrafish, exposure to both types of cigarettes results in broad, dose-dependent developmental defects coupled with severe heart malformation, pericardial edema and reduced heart function. Tobacco cigarettes are more toxic than e-cigarettes at comparable nicotine concentrations. During cardiac differentiation of hESCs, tobacco smoke exposure results in a delayed transition through mesoderm. Both types of cigarettes decrease expression of cardiac transcription factors in cardiac progenitor cells, suggesting a persistent delay in differentiation. In definitive human cardiomyocytes, both e-cigarette- and tobacco cigarette-treated samples showed reduced expression of sarcomeric genes such as MLC2v and MYL6. Furthermore, tobacco cigarette-treated samples had delayed onset of beating and showed low levels and aberrant localization of N-cadherin, reduced myofilament content with significantly reduced sarcomere length, and increased expression of the immature cardiac marker smooth muscle alpha-actin.</p><p>Conclusion</p><p>These data indicate a negative effect of both tobacco cigarettes and e-cigarettes on heart development <i>in vitro</i> and <i>in vivo</i>. Tobacco cigarettes are more toxic than E-cigarettes and exhibit a broader spectrum of cardiac developmental defects.</p></div>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417358, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0126259.s001", "https://dx.doi.org/10.1371/journal.pone.0126259.s002", "https://dx.doi.org/10.1371/journal.pone.0126259.s003", "https://dx.doi.org/10.1371/journal.pone.0126259.s004", "https://dx.doi.org/10.1371/journal.pone.0126259.s005"], "stats"=>{"downloads"=>11, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cardiac_Development_in_Zebrafish_and_Human_Embryonic_Stem_Cells_Is_Inhibited_by_Exposure_to_Tobacco_Cigarettes_and_E_Cigarettes_/1417358", "title"=>"Cardiac Development in Zebrafish and Human Embryonic Stem Cells Is Inhibited by Exposure to Tobacco Cigarettes and E-Cigarettes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070944"], "description"=>"<p>(a) Representative whole mount images of zebrafish at 72 hpe showing normal, mild, intermediate, and severe cardiac developmental defects. v = ventricle, At = atrium. (b-c) Analysis of percent zebrafish with heart defects (b) severity of heart defects and (c). (d) Analysis of heart function in control, e-cigarette and tobacco treated groups at 72 hpe. (e) Quantitative RT-PCR analysis (fold change from control) of a panel of genes with critical roles in early heart development at 24 hpe. n ≥ 3 (independent experiments with each n containing between 24–48 animals per treatment). For qRT-PCR, n = 3 with each n consisting of 28–35 embryos from independent breeding pools. * P < 0.05, hpe = hours post exposure; N = Nicotine, E = E-cigarette, T = Tobacco.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417337, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g002", "stats"=>{"downloads"=>0, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cardiac_developmental_defects_observed_in_zebrafish_treated_with_cigarette_smoke_/1417337", "title"=>"Cardiac developmental defects observed in zebrafish treated with cigarette smoke.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070961"], "description"=>"<p>(a) Quantitative RT-PCR analysis of early developmental myofilament proteins including the atrial myosin light chain MLC2a, the myosin isoform α-MHC and cardiac troponin T (cTnT) in cells treated with 6.8 μM e-cigarette or tobacco cigarette extracts vs. control. (b-c) Immunohistochemistry (b) and quantification (c) of the myofilament proteins cardiac troponin T (cTnT) in combination with phalloidin and nuclear counterstain DAPI in control cells or those treated with 6.8 μM e-cigarette or 6.8 μM tobacco cigarette extracts. Scale bar = 100 μm for cTnT. (d) Quantitative RT-PCR analysis of mature developmental myofilament isoforms including the ventricular myosin light chain MLC2v and the myosin isoform β-MHC in cells treated 6.8 μM e-cigarette or tobacco cigarette extracts vs. control. (e) Quantitation of sarcomere length as measured from samples stained for α-actinin by immunohistochemistry comparing control vs. 6.8 μM e-cigarette or tobacco cigarette. (f-h) Quantitative RT-PCR (f) immunohistochemistry (g) and quantification of IHC (h) for the immature cardiac marker smooth muscle actin (SMA) in control vs. cells treated with 6.8 μM e-cigarette or tobacco cigarette extract. n ≥ 6 per group. Scale bar = 100 μm. * P < 0.05.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417354, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g006", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_cardiac_myofilament_and_structural_protein_expression_/1417354", "title"=>"Analysis of cardiac myofilament and structural protein expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/2070956"], "description"=>"<p>(a-c) Quantitative RT-PCR analysis of expression levels on day 2 of differentiation for genes involved in mesoderm development following exposure to 6.8 μM e-cigarette, or tobacco cigarette extract. Analysis included the pan mesendoderm marker Brachyury T (T) (b), mesendoderm genes involved in patterning anterior primitive streak, NODAL and goosecoid (GSC) (c), and cardiogenic mesoderm genes eomesodermin (EOMES) and MESP1. (d) Quantitative RT-PCR analysis of cardiac progenitor cell markers on day 5 of differentiation including GATA4 and NKX2.5. (e) Quantitative RT-PCR analysis of Wnt/β-catenin ligands WNT3a, WNT8a, WNT5a and Wnt/β-catenin signaling inhibitors DKK1 and TMEM88 between days 2 and 5 of differentiation. (f) Time course analysis of onset of beating during cardiac differentiation. n ≥ 6 per group. * P < 0.05.</p>", "links"=>[], "tags"=>["tobacco cigarettes", "differentiation", "MYL", "Heart development", "human embryonic stem cells", "tobacco smoke exposure results", "cigarettes decrease expression", "mlc"], "article_id"=>1417349, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Nathan J. Palpant", "Peter Hofsteen", "Lil Pabon", "Hans Reinecke", "Charles E. Murry"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0126259.g004", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_cigarette_exposure_on_cardiogenic_mesoderm_development_/1417349", "title"=>"Impact of cigarette exposure on cardiogenic mesoderm development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-15 04:04:45"}

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{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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