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Comprehensive Transcriptional Profiling of the Gastrointestinal Tract of Ruminants from Birth to Adulthood Reveals Strong Developmental Stage Specific Gene Expression

View ORCID ProfileStephen J. Bush, Mary E. B. McCulloch, Charity Muriuki, View ORCID ProfileMazdak Salavati, View ORCID ProfileGemma M. Davis, View ORCID ProfileIseabail L. Farquhar, View ORCID ProfileZofia M. Lisowski, View ORCID ProfileAlan L. Archibald, David A. Hume and View ORCID ProfileEmily L. Clark
G3: Genes, Genomes, Genetics February 1, 2019 vol. 9 no. 2 359-373; https://doi.org/10.1534/g3.118.200810
Stephen J. Bush
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Stephen J. Bush
Mary E. B. McCulloch
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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Charity Muriuki
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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Mazdak Salavati
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Mazdak Salavati
Gemma M. Davis
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Gemma M. Davis
Iseabail L. Farquhar
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Iseabail L. Farquhar
Zofia M. Lisowski
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Zofia M. Lisowski
Alan L. Archibald
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Alan L. Archibald
David A. Hume
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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Emily L. Clark
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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  • ORCID record for Emily L. Clark
  • For correspondence: emily.clark@roslin.ed.ac.uk
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    Figure 1

    Diagrammatic representation of the morphological changes that occur in the gastrointestinal tract of a sheep during the transition from (A) pre-ruminant to (B) ruminant. The 14 regions sampled for this study are numbered (12 samples from each of the lambs and 2 from the adult animals only – esophagus and rectum). The esophageal groove is indicated with dotted lines.

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    Figure 2

    Gene-to-gene network graph of sheep GI tract tissues alongside alveolar macrophages, esophageal tissue and liver with the nodes collapsed by class to illustrate the relative size of each cluster. The top 20 largest clusters are annotated by function. Created using Graphia Professional with parameters Pearson’s R = 0.85, MCLi = 2.2, Minimum Component Size = 2, Minimum Cluster Size = 2.

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    Figure 3

    Comparative analysis of the expression of five C-type lectin genes, measured as transcripts per million (TPM), across three GI tract tissues (large colon, ileum and rumen) and alveolar macrophages in sheep and goats.

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    Figure 4

    Sample-to-sample network graph of sheep GI tract samples colored according to developmental stage. Created using Graphia Professional with parameters Pearson’s R = 0.85, MCLi = 2.2, Minimum Component Size = 2, Minimum Cluster Size = 2.

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    Figure 5

    Principal Component Analysis of macrophage associated signatures in the sheep GI tract illustrating separation by tissue (A & B) and developmental stage (C & D) in three and four components, respectively. The mean of each group was used as the center of the circle colored-by-group with a confidence interval of 0.95 as the ellipse size.

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    Figure 6

    The top 25 differentially expressed genes up-regulated and top 25 down-regulated genes between goat and sheep in the rumen, ileum and colon of age-matched one-week old animals.

Tables

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  • Table 1 Details of animals and samples from the GI tract and other tissues included in this study
    SpeciesBreedDevelopmental StageSexGI Tract TissuesReference & ENA Study Accession
    SheepTexel x Scottish BlackfaceBirth (neonate/ pre-ruminant)1 male, 2 femalesStomachClark et al. 2017 (PRJEB19199)
    Abomasum, Pylorus
    SheepTexel x Scottish BlackfaceOne Week (transition from pre-ruminant to ruminant)1 male, 2 femalesLarge Intestine
    Cecum, Colon Spiral, Colon Large
    SheepTexel x Scottish Blackface8 Weeks (ruminant)2 males, 1 femaleSmall Intestine
    Duodenum, Ileum, Jejunum, Peyer’s Patch
    SheepTexel x Scottish BlackfaceAdult (GI tract) (2 years)3 males, 3 femalesRumen Complex
    Omasum, Reticulum, Rumen
    SheepTexel x Scottish BlackfaceAdult (2 years)3 males, 3 femalesEsophageal Mucosa, Esophageal Muscle, Rectum, Liver, Alveolar MacrophagesClark et al. 2017 (PRJEB19199)
    SheepTexel8 – 9 Months1 femaleAbomasum, Colon, Cecum, Rectum, Rumen, Omentum, Peyer’s PatchJiang et al. 2014 (PRJEB6169)
    SheepTexelAdult (>2 years)1 male, 1 female
    GoatCrossbredOne Week3 maleIleum, Rumen, Colon Large, Alveolar MacrophagesThis Study (PRJEB23196)
  • Table 2 Examples of differentially expressed genes identified using pairwise comparison of abomasum, rumen and ileum samples from sheep at one-week vs. newborn and 8 weeks vs. 1 week. The gene expression estimate (as TPM) at the earliest developmental stage in each comparison is included as TPM 1 and at the later developmental stage as TPM 2
    GeneTissueDevelopmental StageFold ChangeP-ValueDirectionTPM 1TPM 2
    COL1A1Rumen8 Weeks vs. 1 Week2.13.3x10−5Up29,26992,501
    Ileum8 Weeks vs. 1 Week−2.38.5x10−15Down35,5066919
    COL1A2Rumen8 Weeks vs. 1 Week2.17.3x10−5Up25,91980,206
    Ileum8 Weeks vs. 1 Week−2.15.6x10−14Down33,3847541
    KRT36Rumen8 Weeks vs. 1 Week3.96.5x10−8Up638469,503
    HMGCS2RumenOne Week vs. Newborn8.42.3x10−50Up6619,467
    SLC14A1RumenOne Week vs. Newborn2.49.3x10−16Up218110,158
    IL36ARumen8 Weeks vs. 1 Week3.71.4x10−5Up2752647
    CLEC4EIleum8 Weeks vs. 1 Week2.42.7x10−4Up1576
    PIPRumen8 Weeks vs. 1 Week3.15.1x10−7Up3752113
    IFIT2IleumOne Week vs. Newborn2.01.8x10−6Up76275
    IFIT3Abomasum8 Weeks vs. 1 Week3.17.7x10−31Up337439
    MX1Abomasum8 Weeks vs. 1 Week2.15.5x10−21Up10481307
    RumenOne Week vs. Newborn3.61.2x10−5Up2202256
    DUOXA2RumenOne Week vs. Newborn4.13.2x10−5Up12168
    IDO1IleumOne Week vs. Newborn4.22.0x10−8Up881467

Additional Files

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  • Supplemental material for Bush et al., 2018

    Supplemental material available at Figshare: https://doi.org/10.25387/g3.6741575

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    Volume 9 Issue 2, February 2019

    G3: Genes|Genomes|Genetics: 9 (2)

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    Comprehensive Transcriptional Profiling of the Gastrointestinal Tract of Ruminants from Birth to Adulthood Reveals Strong Developmental Stage Specific Gene Expression

    View ORCID ProfileStephen J. Bush, Mary E. B. McCulloch, Charity Muriuki, View ORCID ProfileMazdak Salavati, View ORCID ProfileGemma M. Davis, View ORCID ProfileIseabail L. Farquhar, View ORCID ProfileZofia M. Lisowski, View ORCID ProfileAlan L. Archibald, David A. Hume and View ORCID ProfileEmily L. Clark
    G3: Genes, Genomes, Genetics February 1, 2019 vol. 9 no. 2 359-373; https://doi.org/10.1534/g3.118.200810
    Stephen J. Bush
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
    • Find this author on Google Scholar
    • Find this author on PubMed
    • Search for this author on this site
    • ORCID record for Stephen J. Bush
    Mary E. B. McCulloch
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
    • Find this author on Google Scholar
    • Find this author on PubMed
    • Search for this author on this site
    Charity Muriuki
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • Find this author on PubMed
    • Search for this author on this site
    Mazdak Salavati
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • Search for this author on this site
    • ORCID record for Mazdak Salavati
    Gemma M. Davis
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Gemma M. Davis
    Iseabail L. Farquhar
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Iseabail L. Farquhar
    Zofia M. Lisowski
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Zofia M. Lisowski
    Alan L. Archibald
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Alan L. Archibald
    David A. Hume
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    Emily L. Clark
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Emily L. Clark
    • For correspondence: emily.clark@roslin.ed.ac.uk
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    Citation

    Comprehensive Transcriptional Profiling of the Gastrointestinal Tract of Ruminants from Birth to Adulthood Reveals Strong Developmental Stage Specific Gene Expression

    View ORCID ProfileStephen J. Bush, Mary E. B. McCulloch, Charity Muriuki, View ORCID ProfileMazdak Salavati, View ORCID ProfileGemma M. Davis, View ORCID ProfileIseabail L. Farquhar, View ORCID ProfileZofia M. Lisowski, View ORCID ProfileAlan L. Archibald, David A. Hume and View ORCID ProfileEmily L. Clark
    G3: Genes, Genomes, Genetics February 1, 2019 vol. 9 no. 2 359-373; https://doi.org/10.1534/g3.118.200810
    Stephen J. Bush
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
    • Find this author on Google Scholar
    • Find this author on PubMed
    • Search for this author on this site
    • ORCID record for Stephen J. Bush
    Mary E. B. McCulloch
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
    • Find this author on Google Scholar
    • Find this author on PubMed
    • Search for this author on this site
    Charity Muriuki
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • Search for this author on this site
    Mazdak Salavati
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • Search for this author on this site
    • ORCID record for Mazdak Salavati
    Gemma M. Davis
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Gemma M. Davis
    Iseabail L. Farquhar
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Iseabail L. Farquhar
    Zofia M. Lisowski
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Zofia M. Lisowski
    Alan L. Archibald
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • ORCID record for Alan L. Archibald
    David A. Hume
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    Emily L. Clark
    The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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    • Search for this author on this site
    • ORCID record for Emily L. Clark
    • For correspondence: emily.clark@roslin.ed.ac.uk

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