Different Blood Cell-Derived Transcriptome Signatures in Cows Exposed to Vaccination Pre- or Postpartum
Periparturient cows have been found to reveal immunosuppression, frequently associated with increased susceptibility to uterine and mammary infections. To improve understanding of the causes and molecular regulatory mechanisms accounting for this phenomenon around calving, we examined the effect of...
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description | Periparturient cows have been found to reveal immunosuppression, frequently associated with increased susceptibility to uterine and mammary infections. To improve understanding of the causes and molecular regulatory mechanisms accounting for this phenomenon around calving, we examined the effect of an antigen challenge on gene expression modulation on cows prior to (BC) or after calving (AC) using whole transcriptome sequencing (RNAseq). The transcriptome analysis of the cows' blood identified a substantially higher number of loci affected in BC cows (2,235) in response to vaccination compared to AC cows (208) and revealed a divergent transcriptional profile specific for each group. In BC cows, a variety of loci involved in immune defense and cellular signaling processes were transcriptionally activated, whereas protein biosynthesis and posttranslational processes were tremendously impaired in response to vaccination. Furthermore, energy metabolism in the blood cells of BC cows was shifted from oxidative phosphorylation to the glycolytic system. In AC cows, the number and variety of regulated pathways involved in immunomodulation and maintenance of immnunocompetence are considerably lower after vaccination, and upregulation of arginine degradation was suggested as an immunosuppressive mechanism. Elevated transcript levels of erythrocyte-specific genes involved in gas exchange processes were a specific transcriptional signature in AC cows pointing to hematopoiesis activation. The divergent and substantially lower magnitude of transcriptional modulation in response to vaccination in AC cows provides evidence for a suppressed immune capacity of early lactating cows on the molecular level and demonstrates that an efficient immune response of cows is related to their physiological and metabolic status. |
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To improve understanding of the causes and molecular regulatory mechanisms accounting for this phenomenon around calving, we examined the effect of an antigen challenge on gene expression modulation on cows prior to (BC) or after calving (AC) using whole transcriptome sequencing (RNAseq). The transcriptome analysis of the cows' blood identified a substantially higher number of loci affected in BC cows (2,235) in response to vaccination compared to AC cows (208) and revealed a divergent transcriptional profile specific for each group. In BC cows, a variety of loci involved in immune defense and cellular signaling processes were transcriptionally activated, whereas protein biosynthesis and posttranslational processes were tremendously impaired in response to vaccination. Furthermore, energy metabolism in the blood cells of BC cows was shifted from oxidative phosphorylation to the glycolytic system. In AC cows, the number and variety of regulated pathways involved in immunomodulation and maintenance of immnunocompetence are considerably lower after vaccination, and upregulation of arginine degradation was suggested as an immunosuppressive mechanism. Elevated transcript levels of erythrocyte-specific genes involved in gas exchange processes were a specific transcriptional signature in AC cows pointing to hematopoiesis activation. The divergent and substantially lower magnitude of transcriptional modulation in response to vaccination in AC cows provides evidence for a suppressed immune capacity of early lactating cows on the molecular level and demonstrates that an efficient immune response of cows is related to their physiological and metabolic status.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0136927</identifier><identifier>PMID: 26317664</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antigen-antibody reactions ; Antigens ; Arginine ; Biology ; Biosynthesis ; Blood ; Blood cells ; Cancer ; Cattle ; Cows (Cattle) ; Dendritic cells ; Disease susceptibility ; Energy metabolism ; Erythrocytes ; Female ; Gas exchange ; Gene expression ; Gene Expression Profiling - methods ; Gene Regulatory Networks ; Genetic aspects ; Genomes ; Glycolysis ; Hematopoiesis ; Hypoxia ; Immune response ; Immune system ; Immunology ; Immunomodulation ; Immunosuppression ; Kinases ; Loci ; Metabolism ; Modulation ; Molecular chains ; Observations ; Oxidative phosphorylation ; Phosphorylation ; Postpartum ; Postpartum Period - blood ; Postpartum Period - genetics ; Postpartum Period - immunology ; Pregnancy - blood ; Pregnancy - genetics ; Pregnancy - immunology ; Protein biosynthesis ; Proteins ; Regulatory mechanisms (biology) ; Sequence Analysis, RNA - methods ; Transcription ; Transcription (Genetics) ; Transcriptome ; Uterus ; Vaccination ; Vaccination - veterinary</subject><ispartof>PloS one, 2015-08, Vol.10 (8), p.e0136927-e0136927</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Weikard et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Weikard et al 2015 Weikard et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-d6b69c783c315ca7b56eb75e4c029f43f7b8c5c08a83c5cb8945ab0c5834df3b3</citedby><cites>FETCH-LOGICAL-c692t-d6b69c783c315ca7b56eb75e4c029f43f7b8c5c08a83c5cb8945ab0c5834df3b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4552870/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4552870/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26317664$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Browning, Glenn F.</contributor><creatorcontrib>Weikard, Rosemarie</creatorcontrib><creatorcontrib>Demasius, Wiebke</creatorcontrib><creatorcontrib>Hadlich, Frieder</creatorcontrib><creatorcontrib>Kühn, Christa</creatorcontrib><title>Different Blood Cell-Derived Transcriptome Signatures in Cows Exposed to Vaccination Pre- or Postpartum</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Periparturient cows have been found to reveal immunosuppression, frequently associated with increased susceptibility to uterine and mammary infections. To improve understanding of the causes and molecular regulatory mechanisms accounting for this phenomenon around calving, we examined the effect of an antigen challenge on gene expression modulation on cows prior to (BC) or after calving (AC) using whole transcriptome sequencing (RNAseq). The transcriptome analysis of the cows' blood identified a substantially higher number of loci affected in BC cows (2,235) in response to vaccination compared to AC cows (208) and revealed a divergent transcriptional profile specific for each group. In BC cows, a variety of loci involved in immune defense and cellular signaling processes were transcriptionally activated, whereas protein biosynthesis and posttranslational processes were tremendously impaired in response to vaccination. Furthermore, energy metabolism in the blood cells of BC cows was shifted from oxidative phosphorylation to the glycolytic system. In AC cows, the number and variety of regulated pathways involved in immunomodulation and maintenance of immnunocompetence are considerably lower after vaccination, and upregulation of arginine degradation was suggested as an immunosuppressive mechanism. Elevated transcript levels of erythrocyte-specific genes involved in gas exchange processes were a specific transcriptional signature in AC cows pointing to hematopoiesis activation. The divergent and substantially lower magnitude of transcriptional modulation in response to vaccination in AC cows provides evidence for a suppressed immune capacity of early lactating cows on the molecular level and demonstrates that an efficient immune response of cows is related to their physiological and metabolic status.</description><subject>Animals</subject><subject>Antigen-antibody reactions</subject><subject>Antigens</subject><subject>Arginine</subject><subject>Biology</subject><subject>Biosynthesis</subject><subject>Blood</subject><subject>Blood cells</subject><subject>Cancer</subject><subject>Cattle</subject><subject>Cows (Cattle)</subject><subject>Dendritic cells</subject><subject>Disease susceptibility</subject><subject>Energy metabolism</subject><subject>Erythrocytes</subject><subject>Female</subject><subject>Gas exchange</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Regulatory Networks</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Glycolysis</subject><subject>Hematopoiesis</subject><subject>Hypoxia</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunology</subject><subject>Immunomodulation</subject><subject>Immunosuppression</subject><subject>Kinases</subject><subject>Loci</subject><subject>Metabolism</subject><subject>Modulation</subject><subject>Molecular chains</subject><subject>Observations</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Postpartum</subject><subject>Postpartum Period - blood</subject><subject>Postpartum Period - genetics</subject><subject>Postpartum Period - immunology</subject><subject>Pregnancy - blood</subject><subject>Pregnancy - genetics</subject><subject>Pregnancy - immunology</subject><subject>Protein biosynthesis</subject><subject>Proteins</subject><subject>Regulatory mechanisms (biology)</subject><subject>Sequence Analysis, RNA - methods</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Transcriptome</subject><subject>Uterus</subject><subject>Vaccination</subject><subject>Vaccination - veterinary</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk01v1DAQhiMEoqXwDxBEQkJwyOLE8UcuSGVbYKVKrWjp1XKcSdarJE5tp5R_j5dNqw3qAflgy_PMO-MZTxS9TtEixSz9tDGj7WW7GEwPC5RiWmTsSXSYFjhLaIbw073zQfTCuQ1CBHNKn0cHGcUpozQ_jJoTXddgoffxl9aYKl5C2yYnYPUtVPGVlb1TVg_edBBf6qaXfrTgYt3HS_PLxad3g3EB9Ca-lkrpYNemjy8sJLGx8YVxfpDWj93L6FktWwevpv0o-vn19Gr5PTk7_7ZaHp8lKuTvk4qWtFCMY4VToiQrCYWSEcgVyoo6xzUruSIKcRkQokpe5ESWSBGO86rGJT6K3u50h9Y4MdXIiZQhTihjmAditSMqIzdisLqT9rcwUou_F8Y2ImSsVQuC8qLICKaoQiRnlZRFRaGGIgSipZQsaH2eoo1lB5UKZbSynYnOLb1ei8bcipyQjDMUBD5MAtbcjOC86LRToQWyBzPu8uYFSfk21rt_0MdfN1GNDA_QfW1CXLUVFcd5RoMUYzRQi0eosCrotAofqtbhfubwceYQGA93vpGjc2J1-eP_2fPrOft-j12DbP3amXbc_iI3B_MdqKxxzkL9UOQUie083FdDbOdBTPMQ3N7sN-jB6X4A8B_hZgYr</recordid><startdate>20150828</startdate><enddate>20150828</enddate><creator>Weikard, Rosemarie</creator><creator>Demasius, Wiebke</creator><creator>Hadlich, Frieder</creator><creator>Kühn, Christa</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>COVID</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150828</creationdate><title>Different Blood Cell-Derived Transcriptome Signatures in Cows Exposed to Vaccination Pre- or Postpartum</title><author>Weikard, Rosemarie ; Demasius, Wiebke ; Hadlich, Frieder ; Kühn, Christa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-d6b69c783c315ca7b56eb75e4c029f43f7b8c5c08a83c5cb8945ab0c5834df3b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Antigen-antibody reactions</topic><topic>Antigens</topic><topic>Arginine</topic><topic>Biology</topic><topic>Biosynthesis</topic><topic>Blood</topic><topic>Blood cells</topic><topic>Cancer</topic><topic>Cattle</topic><topic>Cows (Cattle)</topic><topic>Dendritic cells</topic><topic>Disease susceptibility</topic><topic>Energy metabolism</topic><topic>Erythrocytes</topic><topic>Female</topic><topic>Gas exchange</topic><topic>Gene expression</topic><topic>Gene Expression Profiling - methods</topic><topic>Gene Regulatory Networks</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Glycolysis</topic><topic>Hematopoiesis</topic><topic>Hypoxia</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunology</topic><topic>Immunomodulation</topic><topic>Immunosuppression</topic><topic>Kinases</topic><topic>Loci</topic><topic>Metabolism</topic><topic>Modulation</topic><topic>Molecular chains</topic><topic>Observations</topic><topic>Oxidative phosphorylation</topic><topic>Phosphorylation</topic><topic>Postpartum</topic><topic>Postpartum Period - blood</topic><topic>Postpartum Period - genetics</topic><topic>Postpartum Period - immunology</topic><topic>Pregnancy - blood</topic><topic>Pregnancy - genetics</topic><topic>Pregnancy - immunology</topic><topic>Protein biosynthesis</topic><topic>Proteins</topic><topic>Regulatory mechanisms (biology)</topic><topic>Sequence Analysis, RNA - methods</topic><topic>Transcription</topic><topic>Transcription (Genetics)</topic><topic>Transcriptome</topic><topic>Uterus</topic><topic>Vaccination</topic><topic>Vaccination - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Weikard, Rosemarie</au><au>Demasius, Wiebke</au><au>Hadlich, Frieder</au><au>Kühn, Christa</au><au>Browning, Glenn F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Different Blood Cell-Derived Transcriptome Signatures in Cows Exposed to Vaccination Pre- or Postpartum</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-08-28</date><risdate>2015</risdate><volume>10</volume><issue>8</issue><spage>e0136927</spage><epage>e0136927</epage><pages>e0136927-e0136927</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Periparturient cows have been found to reveal immunosuppression, frequently associated with increased susceptibility to uterine and mammary infections. To improve understanding of the causes and molecular regulatory mechanisms accounting for this phenomenon around calving, we examined the effect of an antigen challenge on gene expression modulation on cows prior to (BC) or after calving (AC) using whole transcriptome sequencing (RNAseq). The transcriptome analysis of the cows' blood identified a substantially higher number of loci affected in BC cows (2,235) in response to vaccination compared to AC cows (208) and revealed a divergent transcriptional profile specific for each group. In BC cows, a variety of loci involved in immune defense and cellular signaling processes were transcriptionally activated, whereas protein biosynthesis and posttranslational processes were tremendously impaired in response to vaccination. Furthermore, energy metabolism in the blood cells of BC cows was shifted from oxidative phosphorylation to the glycolytic system. In AC cows, the number and variety of regulated pathways involved in immunomodulation and maintenance of immnunocompetence are considerably lower after vaccination, and upregulation of arginine degradation was suggested as an immunosuppressive mechanism. Elevated transcript levels of erythrocyte-specific genes involved in gas exchange processes were a specific transcriptional signature in AC cows pointing to hematopoiesis activation. The divergent and substantially lower magnitude of transcriptional modulation in response to vaccination in AC cows provides evidence for a suppressed immune capacity of early lactating cows on the molecular level and demonstrates that an efficient immune response of cows is related to their physiological and metabolic status.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26317664</pmid><doi>10.1371/journal.pone.0136927</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antigen-antibody reactions Antigens Arginine Biology Biosynthesis Blood Blood cells Cancer Cattle Cows (Cattle) Dendritic cells Disease susceptibility Energy metabolism Erythrocytes Female Gas exchange Gene expression Gene Expression Profiling - methods Gene Regulatory Networks Genetic aspects Genomes Glycolysis Hematopoiesis Hypoxia Immune response Immune system Immunology Immunomodulation Immunosuppression Kinases Loci Metabolism Modulation Molecular chains Observations Oxidative phosphorylation Phosphorylation Postpartum Postpartum Period - blood Postpartum Period - genetics Postpartum Period - immunology Pregnancy - blood Pregnancy - genetics Pregnancy - immunology Protein biosynthesis Proteins Regulatory mechanisms (biology) Sequence Analysis, RNA - methods Transcription Transcription (Genetics) Transcriptome Uterus Vaccination Vaccination - veterinary |
title | Different Blood Cell-Derived Transcriptome Signatures in Cows Exposed to Vaccination Pre- or Postpartum |
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