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Derivation of Induced Trophoblast Cell Lines in Cattle by Doxycycline-Inducible piggyBac Vectors

Trophectoderm lineage specification is one of the earliest differentiation events in mammalian development. The trophoblast lineage, which is derived from the trophectoderm, mediates implantation and placental formation. However, the processes involved in trophoblastic differentiation and placental...

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Published in:PloS one 2016-12, Vol.11 (12), p.e0167550-e0167550
Main Authors: Kawaguchi, Takamasa, Cho, Dooseon, Hayashi, Masafumi, Tsukiyama, Tomoyuki, Kimura, Koji, Matsuyama, Shuichi, Minami, Naojiro, Yamada, Masayasu, Imai, Hiroshi
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cited_by cdi_FETCH-LOGICAL-c835t-48e9e17272b1cee0c9b20a246a719f58456ffbf7600046455b73affa4fb8051e3
cites cdi_FETCH-LOGICAL-c835t-48e9e17272b1cee0c9b20a246a719f58456ffbf7600046455b73affa4fb8051e3
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creator Kawaguchi, Takamasa
Cho, Dooseon
Hayashi, Masafumi
Tsukiyama, Tomoyuki
Kimura, Koji
Matsuyama, Shuichi
Minami, Naojiro
Yamada, Masayasu
Imai, Hiroshi
description Trophectoderm lineage specification is one of the earliest differentiation events in mammalian development. The trophoblast lineage, which is derived from the trophectoderm, mediates implantation and placental formation. However, the processes involved in trophoblastic differentiation and placental formation in cattle remain unclear due to interspecies differences when compared with other model systems and the small repertoire of available trophoblast cell lines. Here, we describe the generation of trophoblast cell lines (biTBCs) from bovine amnion-derived cells (bADCs) using an induced pluripotent stem cell technique. bADCs were introduced with piggyBac vectors containing doxycycline (Dox)-inducible transcription factors (Oct3⁄4(POU5F1), Sox2, Klf4, and c-Myc). Colonies that appeared showed a flattened epithelial-like morphology similar to cobblestones, had a more definite cell boundary between cells, and frequently formed balloon-like spheroids similar to trophoblastic vesicles (TVs). biTBCs were propagated for over 60 passages and expressed trophoblast-related (CDX2, ELF5, ERRβ, and IFN-τ) and pluripotency-related genes (endogenous OCT3/4, SOX2, KLF4, and c-MYC). Furthermore, when biTBCs were induced to differentiate by removing Dox from culture, they formed binucleate cells and began to express pregnancy-related genes (PL, PRP1, and PAG1). This is the first report demonstrating that the induction of pluripotency in bovine amniotic cells allows the generation of trophoblastic cell lines that possess trophoblast stem cell-like characteristics and have the potential to differentiate into the extra-embryonic cell lineage. These cell lines can be a new cell source as a model for studying trophoblast cell lineages and implantation processes in cattle.
doi_str_mv 10.1371/journal.pone.0167550
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The trophoblast lineage, which is derived from the trophectoderm, mediates implantation and placental formation. However, the processes involved in trophoblastic differentiation and placental formation in cattle remain unclear due to interspecies differences when compared with other model systems and the small repertoire of available trophoblast cell lines. Here, we describe the generation of trophoblast cell lines (biTBCs) from bovine amnion-derived cells (bADCs) using an induced pluripotent stem cell technique. bADCs were introduced with piggyBac vectors containing doxycycline (Dox)-inducible transcription factors (Oct3⁄4(POU5F1), Sox2, Klf4, and c-Myc). Colonies that appeared showed a flattened epithelial-like morphology similar to cobblestones, had a more definite cell boundary between cells, and frequently formed balloon-like spheroids similar to trophoblastic vesicles (TVs). biTBCs were propagated for over 60 passages and expressed trophoblast-related (CDX2, ELF5, ERRβ, and IFN-τ) and pluripotency-related genes (endogenous OCT3/4, SOX2, KLF4, and c-MYC). Furthermore, when biTBCs were induced to differentiate by removing Dox from culture, they formed binucleate cells and began to express pregnancy-related genes (PL, PRP1, and PAG1). This is the first report demonstrating that the induction of pluripotency in bovine amniotic cells allows the generation of trophoblastic cell lines that possess trophoblast stem cell-like characteristics and have the potential to differentiate into the extra-embryonic cell lineage. 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genetics</topic><topic>SOXB1 Transcription Factors - metabolism</topic><topic>Spheroids</topic><topic>Stem cells</topic><topic>Transcription factors</topic><topic>Trophectoderm</topic><topic>Trophoblasts - cytology</topic><topic>Trophoblasts - drug effects</topic><topic>Trophoblasts - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kawaguchi, Takamasa</creatorcontrib><creatorcontrib>Cho, Dooseon</creatorcontrib><creatorcontrib>Hayashi, Masafumi</creatorcontrib><creatorcontrib>Tsukiyama, Tomoyuki</creatorcontrib><creatorcontrib>Kimura, Koji</creatorcontrib><creatorcontrib>Matsuyama, Shuichi</creatorcontrib><creatorcontrib>Minami, Naojiro</creatorcontrib><creatorcontrib>Yamada, Masayasu</creatorcontrib><creatorcontrib>Imai, Hiroshi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale_Opposing Viewpoints In Context</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest_Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - 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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>Kawaguchi, Takamasa</au><au>Cho, Dooseon</au><au>Hayashi, Masafumi</au><au>Tsukiyama, Tomoyuki</au><au>Kimura, Koji</au><au>Matsuyama, Shuichi</au><au>Minami, Naojiro</au><au>Yamada, Masayasu</au><au>Imai, Hiroshi</au><au>Knott, Jason Glenn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Derivation of Induced Trophoblast Cell Lines in Cattle by Doxycycline-Inducible piggyBac Vectors</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-12-01</date><risdate>2016</risdate><volume>11</volume><issue>12</issue><spage>e0167550</spage><epage>e0167550</epage><pages>e0167550-e0167550</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Trophectoderm lineage specification is one of the earliest differentiation events in mammalian development. The trophoblast lineage, which is derived from the trophectoderm, mediates implantation and placental formation. However, the processes involved in trophoblastic differentiation and placental formation in cattle remain unclear due to interspecies differences when compared with other model systems and the small repertoire of available trophoblast cell lines. Here, we describe the generation of trophoblast cell lines (biTBCs) from bovine amnion-derived cells (bADCs) using an induced pluripotent stem cell technique. bADCs were introduced with piggyBac vectors containing doxycycline (Dox)-inducible transcription factors (Oct3⁄4(POU5F1), Sox2, Klf4, and c-Myc). Colonies that appeared showed a flattened epithelial-like morphology similar to cobblestones, had a more definite cell boundary between cells, and frequently formed balloon-like spheroids similar to trophoblastic vesicles (TVs). biTBCs were propagated for over 60 passages and expressed trophoblast-related (CDX2, ELF5, ERRβ, and IFN-τ) and pluripotency-related genes (endogenous OCT3/4, SOX2, KLF4, and c-MYC). Furthermore, when biTBCs were induced to differentiate by removing Dox from culture, they formed binucleate cells and began to express pregnancy-related genes (PL, PRP1, and PAG1). This is the first report demonstrating that the induction of pluripotency in bovine amniotic cells allows the generation of trophoblastic cell lines that possess trophoblast stem cell-like characteristics and have the potential to differentiate into the extra-embryonic cell lineage. These cell lines can be a new cell source as a model for studying trophoblast cell lineages and implantation processes in cattle.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27907214</pmid><doi>10.1371/journal.pone.0167550</doi><tpages>e0167550</tpages><orcidid>https://orcid.org/0000-0002-0067-5804</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
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issn 1932-6203
1932-6203
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source PubMed (Medline); ProQuest - Publicly Available Content Database
subjects Amnion
Amnion - cytology
Amnion - drug effects
Amnion - metabolism
Amniotic cells
Animals
Antibiotics
Beef cattle
Biology
Biology and Life Sciences
Biomarkers - metabolism
Biotechnology
c-Myc protein
Cattle
CDX2 protein
Cell culture
Cell Line
Cell lineage
Cell Lineage - drug effects
Cell lines
Colonies
Comparative analysis
Cytology
Differentiation
Dosage and administration
Doxycycline
Doxycycline - pharmacology
Ectoderm - cytology
Ectoderm - drug effects
Ectoderm - metabolism
Embryos
Female
Fibroblasts
Founder Effect
Gene Expression
Genes
Genetic aspects
Genetic Vectors - chemistry
Genetic Vectors - metabolism
Grasslands
Growth factors
Implantation
Induced Pluripotent Stem Cells - cytology
Induced Pluripotent Stem Cells - drug effects
Induced Pluripotent Stem Cells - metabolism
Interferon
KLF4 protein
Kruppel-Like Transcription Factors - genetics
Kruppel-Like Transcription Factors - metabolism
Laboratories
Life sciences
Livestock
Mammals
Morphology
Myc protein
Oct-4 protein
Octamer Transcription Factor-3 - genetics
Octamer Transcription Factor-3 - metabolism
Placenta
Pluripotency
Pregnancy
Proto-Oncogene Proteins c-myc - genetics
Proto-Oncogene Proteins c-myc - metabolism
Research and Analysis Methods
SOXB1 Transcription Factors - genetics
SOXB1 Transcription Factors - metabolism
Spheroids
Stem cells
Transcription factors
Trophectoderm
Trophoblasts - cytology
Trophoblasts - drug effects
Trophoblasts - metabolism
title Derivation of Induced Trophoblast Cell Lines in Cattle by Doxycycline-Inducible piggyBac Vectors
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