FGF18 impairs blastocyst viability, DNA double-strand breaks and maternal recognition of pregnancy genes
Embryonic mortality in cattle is high, reaching 10–40 % in vivo and 60–70 % in vitro. Death of embryos involves reduced expression of genes related to embryonic viability, inhibition of DNA repair and increased DNA damage. In follicular granulosa cells, FGF18 from the theca layer increases apoptosis...
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| Veröffentlicht in: | Theriogenology 2024-09, Vol.225, p.81-88 |
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| creator | Goetten, André Lucio Fontana Barreta, Marcos Henrique Pinto da Silva, Yago Bertolin, Kalyne Koch, Júlia Rocha, Cecilia Constantino Dias Gonçalves, Paulo Bayard Price, Christopher Alan Antoniazzi, Alfredo Quites Portela, Valerio Marques |
| description | Embryonic mortality in cattle is high, reaching 10–40 % in vivo and 60–70 % in vitro. Death of embryos involves reduced expression of genes related to embryonic viability, inhibition of DNA repair and increased DNA damage. In follicular granulosa cells, FGF18 from the theca layer increases apoptosis and DNA damage, so we hypothesized that FGF18 may also affect the oocyte and contribute to early embryonic death. The aims of this study were to identify the effects of FGF18 on cumulus expansion, oocyte maturation and embryo development from cleavage to blastocyst stage using a conventional bovine in vitro embryo production system using ovaries of abattoir origin. Addition of FGF18 during in-vitro maturation did not affect FSH-induced cumulus expansion or rates of nuclear maturation. When FGF18 was present in the culture system, rates of cleavage were not affected however, blastocyst and expanded blastocyst development was substantially inhibited (P |
| doi_str_mv | 10.1016/j.theriogenology.2024.05.020 |
| format | Article |
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•FGF18 had no effect on cumulus expansion, oocyte nuclear maturation, or embryo development from cleavage stage.•FGF18 added during IVM increased DNA double-strand breaks in cleavage-stage embryos.•FGF18 impaired development to the blastocyst and expanded blastocyst stages.•FGF18 added during embryo culture reduced abundance of PTGS2 mRNA, an embryo viability marker, and mRNA encoding IFNT2, a protein responsible for maternal recognition of pregnancy.</description><identifier>ISSN: 0093-691X</identifier><identifier>EISSN: 1879-3231</identifier><identifier>DOI: 10.1016/j.theriogenology.2024.05.020</identifier><identifier>PMID: 38796960</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; apoptosis ; blastocyst ; Blastocyst - drug effects ; Blastocyst - physiology ; Cattle ; death ; DNA ; DNA Breaks, Double-Stranded ; DNA damage ; DNA repair ; Embryo Culture Techniques - veterinary ; Embryo development ; embryogenesis ; Embryonic Development - drug effects ; embryonic mortality ; Female ; FGF ; Fibroblast Growth Factors - genetics ; Fibroblast Growth Factors - metabolism ; Gene Expression Regulation, Developmental - drug effects ; histones ; IFNT2 ; In Vitro Oocyte Maturation Techniques - veterinary ; Oocyte maturation ; oocytes ; Pregnancy ; slaughterhouses ; viability</subject><ispartof>Theriogenology, 2024-09, Vol.225, p.81-88</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c360t-8da1004f682e38e450bd8a8fccbe4c521378dec09703f27214c379f8d487d143</cites><orcidid>0000-0003-2109-1346 ; 0000-0002-6276-2882</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0093691X24001948$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38796960$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Goetten, André Lucio Fontana</creatorcontrib><creatorcontrib>Barreta, Marcos Henrique</creatorcontrib><creatorcontrib>Pinto da Silva, Yago</creatorcontrib><creatorcontrib>Bertolin, Kalyne</creatorcontrib><creatorcontrib>Koch, Júlia</creatorcontrib><creatorcontrib>Rocha, Cecilia Constantino</creatorcontrib><creatorcontrib>Dias Gonçalves, Paulo Bayard</creatorcontrib><creatorcontrib>Price, Christopher Alan</creatorcontrib><creatorcontrib>Antoniazzi, Alfredo Quites</creatorcontrib><creatorcontrib>Portela, Valerio Marques</creatorcontrib><title>FGF18 impairs blastocyst viability, DNA double-strand breaks and maternal recognition of pregnancy genes</title><title>Theriogenology</title><addtitle>Theriogenology</addtitle><description>Embryonic mortality in cattle is high, reaching 10–40 % in vivo and 60–70 % in vitro. Death of embryos involves reduced expression of genes related to embryonic viability, inhibition of DNA repair and increased DNA damage. In follicular granulosa cells, FGF18 from the theca layer increases apoptosis and DNA damage, so we hypothesized that FGF18 may also affect the oocyte and contribute to early embryonic death. The aims of this study were to identify the effects of FGF18 on cumulus expansion, oocyte maturation and embryo development from cleavage to blastocyst stage using a conventional bovine in vitro embryo production system using ovaries of abattoir origin. Addition of FGF18 during in-vitro maturation did not affect FSH-induced cumulus expansion or rates of nuclear maturation. When FGF18 was present in the culture system, rates of cleavage were not affected however, blastocyst and expanded blastocyst development was substantially inhibited (P < 0.05), indicating a delay of blastulation. The number of phosphorylated histone H2AFX foci per nucleus, a marker of DNA damage, was higher in cleavage-stage embryos cultured with FGF18 than in those from control group (P < 0.05). Furthermore, FGF18 decreased accumulation of PTGS2 and IFNT2 mRNA in blastocysts. In conclusion, these novel findings suggest that FGF18 plays a role in the regulation of embryonic death during the early stages of development by impairing DNA double-strand break repair and expression of genes associated with embryo viability and maternal recognition of pregnancy during the progression from oocyte to expanded blastocysts.
•FGF18 had no effect on cumulus expansion, oocyte nuclear maturation, or embryo development from cleavage stage.•FGF18 added during IVM increased DNA double-strand breaks in cleavage-stage embryos.•FGF18 impaired development to the blastocyst and expanded blastocyst stages.•FGF18 added during embryo culture reduced abundance of PTGS2 mRNA, an embryo viability marker, and mRNA encoding IFNT2, a protein responsible for maternal recognition of pregnancy.</description><subject>Animals</subject><subject>apoptosis</subject><subject>blastocyst</subject><subject>Blastocyst - drug effects</subject><subject>Blastocyst - physiology</subject><subject>Cattle</subject><subject>death</subject><subject>DNA</subject><subject>DNA Breaks, Double-Stranded</subject><subject>DNA damage</subject><subject>DNA repair</subject><subject>Embryo Culture Techniques - veterinary</subject><subject>Embryo development</subject><subject>embryogenesis</subject><subject>Embryonic Development - drug effects</subject><subject>embryonic mortality</subject><subject>Female</subject><subject>FGF</subject><subject>Fibroblast Growth Factors - genetics</subject><subject>Fibroblast Growth Factors - metabolism</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>histones</subject><subject>IFNT2</subject><subject>In Vitro Oocyte Maturation Techniques - veterinary</subject><subject>Oocyte maturation</subject><subject>oocytes</subject><subject>Pregnancy</subject><subject>slaughterhouses</subject><subject>viability</subject><issn>0093-691X</issn><issn>1879-3231</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkT1vFDEQhi0EIkfgLyAXFBTsMrb3wyvRRIELSBE0Kegsrz178bFrH7Yv0v57fLqARAXVTPHMvKN5CHnDoGbAuvf7Ot9jdGGHPsxht9YceFNDWwOHJ2TDZD9Uggv2lGwABlF1A_t-QV6ktAcA0XXsObkQBeqGDjbkfnuzZZK65aBdTHScdcrBrCnTB6dHN7u8vqMfv15RG47jjFXKUXtLx4j6R6KndtEZo9czjWjCzrvsgqdhooeIO6-9WWm5FNNL8mzSc8JXj_WS3G0_3V1_rm6_3Xy5vrqtjOggV9JqBtBMneQoJDYtjFZqORkzYmNazkQvLRoYehAT7zlrjOiHSdpG9pY14pK8Pa89xPDziCmrxSWD86w9hmNSgrVlg-iB_xuFDvqS2LCCfjijJoaUIk7qEN2i46oYqJMVtVd_W1EnKwpaVayU8dePScdxQftn-LeGAmzPAJbPPDiMKhmH3qB15atZ2eD-L-kXRcKnTw</recordid><startdate>20240901</startdate><enddate>20240901</enddate><creator>Goetten, André Lucio Fontana</creator><creator>Barreta, Marcos Henrique</creator><creator>Pinto da Silva, Yago</creator><creator>Bertolin, Kalyne</creator><creator>Koch, Júlia</creator><creator>Rocha, Cecilia Constantino</creator><creator>Dias Gonçalves, Paulo Bayard</creator><creator>Price, Christopher Alan</creator><creator>Antoniazzi, Alfredo Quites</creator><creator>Portela, Valerio Marques</creator><general>Elsevier Inc</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-2109-1346</orcidid><orcidid>https://orcid.org/0000-0002-6276-2882</orcidid></search><sort><creationdate>20240901</creationdate><title>FGF18 impairs blastocyst viability, DNA double-strand breaks and maternal recognition of pregnancy genes</title><author>Goetten, André Lucio Fontana ; Barreta, Marcos Henrique ; Pinto da Silva, Yago ; Bertolin, Kalyne ; Koch, Júlia ; Rocha, Cecilia Constantino ; Dias Gonçalves, Paulo Bayard ; Price, Christopher Alan ; Antoniazzi, Alfredo Quites ; Portela, Valerio Marques</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c360t-8da1004f682e38e450bd8a8fccbe4c521378dec09703f27214c379f8d487d143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>apoptosis</topic><topic>blastocyst</topic><topic>Blastocyst - drug effects</topic><topic>Blastocyst - physiology</topic><topic>Cattle</topic><topic>death</topic><topic>DNA</topic><topic>DNA Breaks, Double-Stranded</topic><topic>DNA damage</topic><topic>DNA repair</topic><topic>Embryo Culture Techniques - veterinary</topic><topic>Embryo development</topic><topic>embryogenesis</topic><topic>Embryonic Development - drug effects</topic><topic>embryonic mortality</topic><topic>Female</topic><topic>FGF</topic><topic>Fibroblast Growth Factors - genetics</topic><topic>Fibroblast Growth Factors - metabolism</topic><topic>Gene Expression Regulation, Developmental - drug effects</topic><topic>histones</topic><topic>IFNT2</topic><topic>In Vitro Oocyte Maturation Techniques - veterinary</topic><topic>Oocyte maturation</topic><topic>oocytes</topic><topic>Pregnancy</topic><topic>slaughterhouses</topic><topic>viability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Goetten, André Lucio Fontana</creatorcontrib><creatorcontrib>Barreta, Marcos Henrique</creatorcontrib><creatorcontrib>Pinto da Silva, Yago</creatorcontrib><creatorcontrib>Bertolin, Kalyne</creatorcontrib><creatorcontrib>Koch, Júlia</creatorcontrib><creatorcontrib>Rocha, Cecilia Constantino</creatorcontrib><creatorcontrib>Dias Gonçalves, Paulo Bayard</creatorcontrib><creatorcontrib>Price, Christopher Alan</creatorcontrib><creatorcontrib>Antoniazzi, Alfredo Quites</creatorcontrib><creatorcontrib>Portela, Valerio Marques</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Theriogenology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Goetten, André Lucio Fontana</au><au>Barreta, Marcos Henrique</au><au>Pinto da Silva, Yago</au><au>Bertolin, Kalyne</au><au>Koch, Júlia</au><au>Rocha, Cecilia Constantino</au><au>Dias Gonçalves, Paulo Bayard</au><au>Price, Christopher Alan</au><au>Antoniazzi, Alfredo Quites</au><au>Portela, Valerio Marques</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>FGF18 impairs blastocyst viability, DNA double-strand breaks and maternal recognition of pregnancy genes</atitle><jtitle>Theriogenology</jtitle><addtitle>Theriogenology</addtitle><date>2024-09-01</date><risdate>2024</risdate><volume>225</volume><spage>81</spage><epage>88</epage><pages>81-88</pages><issn>0093-691X</issn><eissn>1879-3231</eissn><abstract>Embryonic mortality in cattle is high, reaching 10–40 % in vivo and 60–70 % in vitro. Death of embryos involves reduced expression of genes related to embryonic viability, inhibition of DNA repair and increased DNA damage. In follicular granulosa cells, FGF18 from the theca layer increases apoptosis and DNA damage, so we hypothesized that FGF18 may also affect the oocyte and contribute to early embryonic death. The aims of this study were to identify the effects of FGF18 on cumulus expansion, oocyte maturation and embryo development from cleavage to blastocyst stage using a conventional bovine in vitro embryo production system using ovaries of abattoir origin. Addition of FGF18 during in-vitro maturation did not affect FSH-induced cumulus expansion or rates of nuclear maturation. When FGF18 was present in the culture system, rates of cleavage were not affected however, blastocyst and expanded blastocyst development was substantially inhibited (P < 0.05), indicating a delay of blastulation. The number of phosphorylated histone H2AFX foci per nucleus, a marker of DNA damage, was higher in cleavage-stage embryos cultured with FGF18 than in those from control group (P < 0.05). Furthermore, FGF18 decreased accumulation of PTGS2 and IFNT2 mRNA in blastocysts. In conclusion, these novel findings suggest that FGF18 plays a role in the regulation of embryonic death during the early stages of development by impairing DNA double-strand break repair and expression of genes associated with embryo viability and maternal recognition of pregnancy during the progression from oocyte to expanded blastocysts.
•FGF18 had no effect on cumulus expansion, oocyte nuclear maturation, or embryo development from cleavage stage.•FGF18 added during IVM increased DNA double-strand breaks in cleavage-stage embryos.•FGF18 impaired development to the blastocyst and expanded blastocyst stages.•FGF18 added during embryo culture reduced abundance of PTGS2 mRNA, an embryo viability marker, and mRNA encoding IFNT2, a protein responsible for maternal recognition of pregnancy.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>38796960</pmid><doi>10.1016/j.theriogenology.2024.05.020</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0003-2109-1346</orcidid><orcidid>https://orcid.org/0000-0002-6276-2882</orcidid></addata></record> |
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| subjects | Animals apoptosis blastocyst Blastocyst - drug effects Blastocyst - physiology Cattle death DNA DNA Breaks, Double-Stranded DNA damage DNA repair Embryo Culture Techniques - veterinary Embryo development embryogenesis Embryonic Development - drug effects embryonic mortality Female FGF Fibroblast Growth Factors - genetics Fibroblast Growth Factors - metabolism Gene Expression Regulation, Developmental - drug effects histones IFNT2 In Vitro Oocyte Maturation Techniques - veterinary Oocyte maturation oocytes Pregnancy slaughterhouses viability |
| title | FGF18 impairs blastocyst viability, DNA double-strand breaks and maternal recognition of pregnancy genes |
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