DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis
In the male germline, neonatal prospermatogonia give rise to spermatogonia, which include stem cell population (undifferentiated spermatogonia) that supports continuous spermatogenesis in adults. Although the levels of DNA methyltransferases change dynamically in the neonatal and early postnatal mal...
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| creator | Kubo, Naoki Toh, Hidehiro Shirane, Kenjiro Shirakawa, Takayuki Kobayashi, Hisato Sato, Tetsuya Sone, Hidetoshi Sato, Yasuyuki Tomizawa, Shin-ichi Tsurusaki, Yoshinori Shibata, Hiroki Saitsu, Hirotomo Suzuki, Yutaka Matsumoto, Naomichi Suyama, Mikita Kono, Tomohiro Ohbo, Kazuyuki Sasaki, Hiroyuki |
| description | In the male germline, neonatal prospermatogonia give rise to spermatogonia, which include stem cell population (undifferentiated spermatogonia) that supports continuous spermatogenesis in adults. Although the levels of DNA methyltransferases change dynamically in the neonatal and early postnatal male germ cells, detailed genome-wide DNA methylation profiles of these cells during the stem cell formation and differentiation have not been reported.
To understand the regulation of spermatogonial stem cell formation and differentiation, we examined the DNA methylation and gene expression dynamics of male mouse germ cells at the critical stages: neonatal prospermatogonia, and early postntal (day 7) undifferentiated and differentiating spermatogonia. We found large partially methylated domains similar to those found in cancer cells and placenta in all these germ cells, and high levels of non-CG methylation and 5-hydroxymethylcytosines in neonatal prospermatogonia. Although the global CG methylation levels were stable in early postnatal male germ cells, and despite the reported scarcity of differential methylation in the adult spermatogonial stem cells, we identified many regions showing stage-specific differential methylation in and around genes important for stem cell function and spermatogenesis. These regions contained binding sites for specific transcription factors including the SOX family members.
Our findings show a distinctive and dynamic regulation of DNA methylation during spermatogonial stem cell formation and differentiation in the neonatal and early postnatal testes. Furthermore, we revealed a unique accumulation and distribution of non-CG methylation and 5hmC marks in neonatal prospermatogonia. These findings contrast with the reported scarcity of differential methylation in adult spermatogonial stem cell differentiation and represent a unique phase of male germ cell development. |
| doi_str_mv | 10.1186/s12864-015-1833-5 |
| format | Article |
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To understand the regulation of spermatogonial stem cell formation and differentiation, we examined the DNA methylation and gene expression dynamics of male mouse germ cells at the critical stages: neonatal prospermatogonia, and early postntal (day 7) undifferentiated and differentiating spermatogonia. We found large partially methylated domains similar to those found in cancer cells and placenta in all these germ cells, and high levels of non-CG methylation and 5-hydroxymethylcytosines in neonatal prospermatogonia. Although the global CG methylation levels were stable in early postnatal male germ cells, and despite the reported scarcity of differential methylation in the adult spermatogonial stem cells, we identified many regions showing stage-specific differential methylation in and around genes important for stem cell function and spermatogenesis. These regions contained binding sites for specific transcription factors including the SOX family members.
Our findings show a distinctive and dynamic regulation of DNA methylation during spermatogonial stem cell formation and differentiation in the neonatal and early postnatal testes. Furthermore, we revealed a unique accumulation and distribution of non-CG methylation and 5hmC marks in neonatal prospermatogonia. These findings contrast with the reported scarcity of differential methylation in adult spermatogonial stem cell differentiation and represent a unique phase of male germ cell development.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/s12864-015-1833-5</identifier><identifier>PMID: 26290333</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Animals, Newborn ; Cell Differentiation ; DNA binding proteins ; DNA Methylation ; Gene Expression Profiling - methods ; Gene Expression Regulation, Developmental ; Genetic aspects ; Genetic transcription ; Infants (Newborn) ; Male ; Methyltransferases ; Mice ; Spermatogenesis ; Spermatogonia - cytology ; Spermatogonia - physiology ; Stem Cells - physiology</subject><ispartof>BMC genomics, 2015-08, Vol.16 (1), p.624-624, Article 624</ispartof><rights>COPYRIGHT 2015 BioMed Central Ltd.</rights><rights>Copyright BioMed Central 2015</rights><rights>Kubo et al. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c722t-653d795c58f7ae2901e7bd92bfb325215f826d60cee0e95d4101958fff53eb1a3</citedby><cites>FETCH-LOGICAL-c722t-653d795c58f7ae2901e7bd92bfb325215f826d60cee0e95d4101958fff53eb1a3</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/PMC4546090/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4546090/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26290333$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kubo, Naoki</creatorcontrib><creatorcontrib>Toh, Hidehiro</creatorcontrib><creatorcontrib>Shirane, Kenjiro</creatorcontrib><creatorcontrib>Shirakawa, Takayuki</creatorcontrib><creatorcontrib>Kobayashi, Hisato</creatorcontrib><creatorcontrib>Sato, Tetsuya</creatorcontrib><creatorcontrib>Sone, Hidetoshi</creatorcontrib><creatorcontrib>Sato, Yasuyuki</creatorcontrib><creatorcontrib>Tomizawa, Shin-ichi</creatorcontrib><creatorcontrib>Tsurusaki, Yoshinori</creatorcontrib><creatorcontrib>Shibata, Hiroki</creatorcontrib><creatorcontrib>Saitsu, Hirotomo</creatorcontrib><creatorcontrib>Suzuki, Yutaka</creatorcontrib><creatorcontrib>Matsumoto, Naomichi</creatorcontrib><creatorcontrib>Suyama, Mikita</creatorcontrib><creatorcontrib>Kono, Tomohiro</creatorcontrib><creatorcontrib>Ohbo, Kazuyuki</creatorcontrib><creatorcontrib>Sasaki, Hiroyuki</creatorcontrib><title>DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>In the male germline, neonatal prospermatogonia give rise to spermatogonia, which include stem cell population (undifferentiated spermatogonia) that supports continuous spermatogenesis in adults. Although the levels of DNA methyltransferases change dynamically in the neonatal and early postnatal male germ cells, detailed genome-wide DNA methylation profiles of these cells during the stem cell formation and differentiation have not been reported.
To understand the regulation of spermatogonial stem cell formation and differentiation, we examined the DNA methylation and gene expression dynamics of male mouse germ cells at the critical stages: neonatal prospermatogonia, and early postntal (day 7) undifferentiated and differentiating spermatogonia. We found large partially methylated domains similar to those found in cancer cells and placenta in all these germ cells, and high levels of non-CG methylation and 5-hydroxymethylcytosines in neonatal prospermatogonia. Although the global CG methylation levels were stable in early postnatal male germ cells, and despite the reported scarcity of differential methylation in the adult spermatogonial stem cells, we identified many regions showing stage-specific differential methylation in and around genes important for stem cell function and spermatogenesis. These regions contained binding sites for specific transcription factors including the SOX family members.
Our findings show a distinctive and dynamic regulation of DNA methylation during spermatogonial stem cell formation and differentiation in the neonatal and early postnatal testes. Furthermore, we revealed a unique accumulation and distribution of non-CG methylation and 5hmC marks in neonatal prospermatogonia. These findings contrast with the reported scarcity of differential methylation in adult spermatogonial stem cell differentiation and represent a unique phase of male germ cell development.</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Cell Differentiation</subject><subject>DNA binding proteins</subject><subject>DNA Methylation</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic aspects</subject><subject>Genetic transcription</subject><subject>Infants (Newborn)</subject><subject>Male</subject><subject>Methyltransferases</subject><subject>Mice</subject><subject>Spermatogenesis</subject><subject>Spermatogonia - cytology</subject><subject>Spermatogonia - physiology</subject><subject>Stem Cells - physiology</subject><issn>1471-2164</issn><issn>1471-2164</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><recordid>eNptkktv1DAUhSMEomXgB7BBltiURYrfSTZIo_KqVIHEY205yXXGVWIH20GdHT8dR1NKB6EsHNnfOb73-hTFc4LPCanl60hoLXmJiShJzVgpHhSnhFekpETyh_f-T4onMV5jTKqaisfFCZW0wYyx0-LX209bNEHa7UedrHdIux4N4ADBzRwgxnWv3zs92S6ifgnWDSjOECad_OCd1SOKCSbUwTii3hoDAVyyBzPrUNplKx3GPZp9TE6nLJj8EgEliMnGp8Ujo8cIz27XTfH9_btvFx_Lq88fLi-2V2VXUZpKKVhfNaITtak05OoJVG3f0Na0jApKhKmp7CXuADA0oucEkybDxggGLdFsU7w5-M5LO0Hf5SKDHtUc7KTDXnlt1fGJszs1-J-KCy5xntamOLs1CP7HkmtXk41r19pB7keRCouKUVnRjL78B732S3C5vUzVmGHecPaXGvQIyjrj873daqq2ghMmeX6mTJ3_h8pfD_lJvANj8_6R4NWRIDMJbtKglxjV5dcvxyw5sF3wMQYwd_MgWK0RU4eIqRwxtUZMiax5cX-Qd4o_mWK_ASHAzR4</recordid><startdate>20150820</startdate><enddate>20150820</enddate><creator>Kubo, Naoki</creator><creator>Toh, Hidehiro</creator><creator>Shirane, Kenjiro</creator><creator>Shirakawa, Takayuki</creator><creator>Kobayashi, Hisato</creator><creator>Sato, Tetsuya</creator><creator>Sone, Hidetoshi</creator><creator>Sato, Yasuyuki</creator><creator>Tomizawa, Shin-ichi</creator><creator>Tsurusaki, Yoshinori</creator><creator>Shibata, Hiroki</creator><creator>Saitsu, Hirotomo</creator><creator>Suzuki, Yutaka</creator><creator>Matsumoto, Naomichi</creator><creator>Suyama, Mikita</creator><creator>Kono, Tomohiro</creator><creator>Ohbo, Kazuyuki</creator><creator>Sasaki, Hiroyuki</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150820</creationdate><title>DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis</title><author>Kubo, Naoki ; Toh, Hidehiro ; Shirane, Kenjiro ; Shirakawa, Takayuki ; Kobayashi, Hisato ; Sato, Tetsuya ; Sone, Hidetoshi ; Sato, Yasuyuki ; Tomizawa, Shin-ichi ; Tsurusaki, Yoshinori ; Shibata, Hiroki ; Saitsu, Hirotomo ; Suzuki, Yutaka ; Matsumoto, Naomichi ; Suyama, Mikita ; Kono, Tomohiro ; Ohbo, Kazuyuki ; Sasaki, Hiroyuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c722t-653d795c58f7ae2901e7bd92bfb325215f826d60cee0e95d4101958fff53eb1a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Cell Differentiation</topic><topic>DNA binding proteins</topic><topic>DNA Methylation</topic><topic>Gene Expression Profiling - methods</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetic aspects</topic><topic>Genetic transcription</topic><topic>Infants (Newborn)</topic><topic>Male</topic><topic>Methyltransferases</topic><topic>Mice</topic><topic>Spermatogenesis</topic><topic>Spermatogonia - cytology</topic><topic>Spermatogonia - physiology</topic><topic>Stem Cells - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kubo, Naoki</creatorcontrib><creatorcontrib>Toh, Hidehiro</creatorcontrib><creatorcontrib>Shirane, Kenjiro</creatorcontrib><creatorcontrib>Shirakawa, Takayuki</creatorcontrib><creatorcontrib>Kobayashi, Hisato</creatorcontrib><creatorcontrib>Sato, Tetsuya</creatorcontrib><creatorcontrib>Sone, Hidetoshi</creatorcontrib><creatorcontrib>Sato, Yasuyuki</creatorcontrib><creatorcontrib>Tomizawa, Shin-ichi</creatorcontrib><creatorcontrib>Tsurusaki, Yoshinori</creatorcontrib><creatorcontrib>Shibata, Hiroki</creatorcontrib><creatorcontrib>Saitsu, Hirotomo</creatorcontrib><creatorcontrib>Suzuki, Yutaka</creatorcontrib><creatorcontrib>Matsumoto, Naomichi</creatorcontrib><creatorcontrib>Suyama, Mikita</creatorcontrib><creatorcontrib>Kono, Tomohiro</creatorcontrib><creatorcontrib>Ohbo, Kazuyuki</creatorcontrib><creatorcontrib>Sasaki, Hiroyuki</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 In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kubo, Naoki</au><au>Toh, Hidehiro</au><au>Shirane, Kenjiro</au><au>Shirakawa, Takayuki</au><au>Kobayashi, Hisato</au><au>Sato, Tetsuya</au><au>Sone, Hidetoshi</au><au>Sato, Yasuyuki</au><au>Tomizawa, Shin-ichi</au><au>Tsurusaki, Yoshinori</au><au>Shibata, Hiroki</au><au>Saitsu, Hirotomo</au><au>Suzuki, Yutaka</au><au>Matsumoto, Naomichi</au><au>Suyama, Mikita</au><au>Kono, Tomohiro</au><au>Ohbo, Kazuyuki</au><au>Sasaki, Hiroyuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2015-08-20</date><risdate>2015</risdate><volume>16</volume><issue>1</issue><spage>624</spage><epage>624</epage><pages>624-624</pages><artnum>624</artnum><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>In the male germline, neonatal prospermatogonia give rise to spermatogonia, which include stem cell population (undifferentiated spermatogonia) that supports continuous spermatogenesis in adults. Although the levels of DNA methyltransferases change dynamically in the neonatal and early postnatal male germ cells, detailed genome-wide DNA methylation profiles of these cells during the stem cell formation and differentiation have not been reported.
To understand the regulation of spermatogonial stem cell formation and differentiation, we examined the DNA methylation and gene expression dynamics of male mouse germ cells at the critical stages: neonatal prospermatogonia, and early postntal (day 7) undifferentiated and differentiating spermatogonia. We found large partially methylated domains similar to those found in cancer cells and placenta in all these germ cells, and high levels of non-CG methylation and 5-hydroxymethylcytosines in neonatal prospermatogonia. Although the global CG methylation levels were stable in early postnatal male germ cells, and despite the reported scarcity of differential methylation in the adult spermatogonial stem cells, we identified many regions showing stage-specific differential methylation in and around genes important for stem cell function and spermatogenesis. These regions contained binding sites for specific transcription factors including the SOX family members.
Our findings show a distinctive and dynamic regulation of DNA methylation during spermatogonial stem cell formation and differentiation in the neonatal and early postnatal testes. Furthermore, we revealed a unique accumulation and distribution of non-CG methylation and 5hmC marks in neonatal prospermatogonia. These findings contrast with the reported scarcity of differential methylation in adult spermatogonial stem cell differentiation and represent a unique phase of male germ cell development.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>26290333</pmid><doi>10.1186/s12864-015-1833-5</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | BMC genomics, 2015-08, Vol.16 (1), p.624-624, Article 624 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Springer Nature OA Free Journals; Springer Nature - Complete Springer Journals; PubMed Central |
| subjects | Animals Animals, Newborn Cell Differentiation DNA binding proteins DNA Methylation Gene Expression Profiling - methods Gene Expression Regulation, Developmental Genetic aspects Genetic transcription Infants (Newborn) Male Methyltransferases Mice Spermatogenesis Spermatogonia - cytology Spermatogonia - physiology Stem Cells - physiology |
| title | DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis |
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