Microhomology-mediated circular DNA formation from oligonucleosomal fragments during spermatogenesis

The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we revealed widespread eccDNA formation in human sperms and mouse spermatogenesis. We noted that germline eccDNAs are derived from oligonucleos...

Full description

Saved in:

Bibliographic Details
Published in:	eLife Vol. 12
Main Authors:	Hu, Jun, Zhang, Zhe, Xiao, Sai, Cao, Yalei, Chen, Yinghong, Weng, Jiaming, Jiang, Hui, Li, Wei, Chen, Jia-Yu, Liu, Chao
Format:	Journal Article
Language:	English
Published:	Cambridge eLife Sciences Publications Ltd 17.10.2023 eLife Sciences Publications, Ltd
Subjects:	Bioinformatics Biosynthesis Cell death Circular DNA Developmental Biology DNA fragmentation Euchromatin extrachromosomal circular DNA Genetics and Genomics Genomes Heterochromatin Meiosis microhomology Mitochondrial DNA Morphology Quality control Recombination hot spots Sperm Spermatogenesis
ISSN:	2050-084X, 2050-084X
Online Access:	Get full text
Tags:	Add Tag No Tags, Be the first to tag this record!

Abstract	The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we revealed widespread eccDNA formation in human sperms and mouse spermatogenesis. We noted that germline eccDNAs are derived from oligonucleosomal DNA fragmentation in cells likely undergoing cell death, providing a potential new way for quality assessment of human sperms. Interestingly, small-sized eccDNAs are associated with euchromatin, while large-sized ones are preferentially generated from heterochromatin. By comparing sperm eccDNAs with meiotic recombination hotspots and structural variations, we found that they are barely associated with de novo germline deletions. We further developed a bioinformatics pipeline to achieve nucleotide-resolution eccDNA detection even with the presence of microhomologous sequences that interfere with precise breakpoint identification. Empowered by our method, we provided strong evidence to show that microhomology-mediated end joining is the major eccDNA biogenesis mechanism. Together, our results shed light on eccDNA biogenesis mechanism in mammalian germline cells.
AbstractList	The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we revealed widespread eccDNA formation in human sperms and mouse spermatogenesis. We noted that germline eccDNAs are derived from oligonucleosomal DNA fragmentation in cells likely undergoing cell death, providing a potential new way for quality assessment of human sperms. Interestingly, small-sized eccDNAs are associated with euchromatin, while large-sized ones are preferentially generated from heterochromatin. By comparing sperm eccDNAs with meiotic recombination hotspots and structural variations, we found that they are barely associated with de novo germline deletions. We further developed a bioinformatics pipeline to achieve nucleotide-resolution eccDNA detection even with the presence of microhomologous sequences that interfere with precise breakpoint identification. Empowered by our method, we provided strong evidence to show that microhomology-mediated end joining is the major eccDNA biogenesis mechanism. Together, our results shed light on eccDNA biogenesis mechanism in mammalian germline cells.The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we revealed widespread eccDNA formation in human sperms and mouse spermatogenesis. We noted that germline eccDNAs are derived from oligonucleosomal DNA fragmentation in cells likely undergoing cell death, providing a potential new way for quality assessment of human sperms. Interestingly, small-sized eccDNAs are associated with euchromatin, while large-sized ones are preferentially generated from heterochromatin. By comparing sperm eccDNAs with meiotic recombination hotspots and structural variations, we found that they are barely associated with de novo germline deletions. We further developed a bioinformatics pipeline to achieve nucleotide-resolution eccDNA detection even with the presence of microhomologous sequences that interfere with precise breakpoint identification. Empowered by our method, we provided strong evidence to show that microhomology-mediated end joining is the major eccDNA biogenesis mechanism. Together, our results shed light on eccDNA biogenesis mechanism in mammalian germline cells. The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we revealed widespread eccDNA formation in human sperms and mouse spermatogenesis. We noted that germline eccDNAs are derived from oligonucleosomal DNA fragmentation in cells likely undergoing cell death, providing a potential new way for quality assessment of human sperms. Interestingly, small-sized eccDNAs are associated with euchromatin, while large-sized ones are preferentially generated from heterochromatin. By comparing sperm eccDNAs with meiotic recombination hotspots and structural variations, we found that they are barely associated with de novo germline deletions. We further developed a bioinformatics pipeline to achieve nucleotide-resolution eccDNA detection even with the presence of microhomologous sequences that interfere with precise breakpoint identification. Empowered by our method, we provided strong evidence to show that microhomology-mediated end joining is the major eccDNA biogenesis mechanism. Together, our results shed light on eccDNA biogenesis mechanism in mammalian germline cells.
Author	Hu, Jun Liu, Chao Weng, Jiaming Jiang, Hui Chen, Jia-Yu Li, Wei Cao, Yalei Zhang, Zhe Xiao, Sai Chen, Yinghong
Author_xml	– sequence: 1 givenname: Jun surname: Hu fullname: Hu, Jun – sequence: 2 givenname: Zhe surname: Zhang fullname: Zhang, Zhe – sequence: 3 givenname: Sai surname: Xiao fullname: Xiao, Sai – sequence: 4 givenname: Yalei surname: Cao fullname: Cao, Yalei – sequence: 5 givenname: Yinghong surname: Chen fullname: Chen, Yinghong – sequence: 6 givenname: Jiaming surname: Weng fullname: Weng, Jiaming – sequence: 7 givenname: Hui surname: Jiang fullname: Jiang, Hui – sequence: 8 givenname: Wei surname: Li fullname: Li, Wei – sequence: 9 givenname: Jia-Yu orcidid: 0000-0001-9449-9321 surname: Chen fullname: Chen, Jia-Yu – sequence: 10 givenname: Chao surname: Liu fullname: Liu, Chao
BookMark	eNptkk1rFTEUhgep2Fq78g8MuBFkaj4nyUpK_SpcdaPgLmSSk2kuM8k1mRH67829t4gtZpNw8p6H93w8b05iitA0LzG6FJyzt7AJHi6lwJg_ac4I4qhDkv08-ed92lyUskX1CCYlVs-aUyokE5j1Z437EmxOt2lOUxrvuhlcMAu41oZs18nk9v3Xq9anPJslpNj6nOY2TWFMcbUTpJJmM9WoGWeIS2ndmkMc27KDfUYaIUIJ5UXz1JupwMX9fd78-Pjh-_XnbvPt08311aazjNOlk8wC8s5jTwRVhCKPBZWDUsMwUMWo59gDQ4YoNyCnnJDcD9QLYD1gCgM9b26OXJfMVu9ymE2-08kEfQikPGqTl1CNa-IZGMwIGgRnkjrFEFQCQ70lVHlWWe-OrN061K7YWl420wPow58YbvWYfmuMuMS95JXw-p6Q068VyqLnUCxMk4mQ1qKJFJIownFfpa8eSbdpzbH2qqok40JRuge-OarqxErJ4P-6wUjvt0EftkEftqGq8SO1DcthitVumP6b8wcLj7uZ
CitedBy_id	crossref_primary_10_1038_s41467_024_46691_0 crossref_primary_10_1093_bib_bbae034 crossref_primary_10_1016_j_biotechadv_2025_108693 crossref_primary_10_1111_brv_13151 crossref_primary_10_1111_nph_19984 crossref_primary_10_1186_s12943_024_02187_5 crossref_primary_10_1002_adbi_202400433 crossref_primary_10_1093_nar_gkaf122
Cites_doi	10.1093/humrep/deh130 10.1016/j.cell.2021.10.025 10.3389/fcell.2021.755751 10.1073/pnas.1508825112 10.1095/biolreprod64.2.706 10.1016/j.molcel.2019.04.014 10.3389/fgene.2019.00962 10.1385/1-59259-812-9:001 10.1016/j.tig.2022.02.007 10.1038/s41467-018-03369-8 10.1002/mrd.22644 10.1095/biolreprod64.1.120 10.1073/pnas.1914949117 10.1128/mcb.8.4.1525-1533.1988 10.1002/gcc.20272 10.1093/gigascience/giab008 10.1073/pnas.2102842118 10.3389/fgene.2020.00780 10.1021/acs.accounts.6b00417 10.1093/nar/gkz155 10.1016/j.molcel.2021.11.027 10.1016/j.cell.2016.09.035 10.1093/gbe/evz281 10.1038/s41596-020-0301-0 10.1038/s41586-020-03064-z 10.1186/1471-2105-11-346 10.3389/fcell.2021.675286 10.1186/s12859-019-3160-3 10.1016/j.gpb.2021.08.001 10.1093/nar/gkab984 10.1186/s12859-021-04545-2 10.1093/nar/gkab951 10.3389/fpls.2021.743742 10.1186/gb-2008-9-9-r137 10.1016/j.celrep.2015.05.020 10.1093/bioinformatics/btq033 10.1007/978-0-387-09597-4_1 10.1093/bioinformatics/btl151 10.1093/nar/gkw257 10.1098/rstb.2009.0124 10.1038/sj.onc.1205880 10.1093/nar/gkac259 10.1093/clinchem/hvaa096 10.1002/ctm2.817 10.1186/s12967-021-02927-x 10.1038/s41586-021-04009-w 10.1242/dev.106450 10.1093/bioinformatics/btp324 10.1126/science.1213307 10.1158/1541-7786.MCR-17-0095 10.1111/j.1469-185x.1962.tb01616.x 10.1038/s41422-020-00466-6 10.1101/gr.1970304 10.1016/j.tig.2017.12.010 10.1093/bioinformatics/btu314 10.3389/fphys.2017.00188 10.1016/j.celrep.2017.01.034
ContentType	Journal Article
Copyright	2023, Hu, Zhang et al. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2023, Hu, Zhang et al. 2023, Hu, Zhang et al 2023 Hu, Zhang et al
Copyright_xml	– notice: 2023, Hu, Zhang et al. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2023, Hu, Zhang et al. – notice: 2023, Hu, Zhang et al 2023 Hu, Zhang et al
DBID	AAYXX CITATION 3V. 7X7 7XB 88E 88I 8FE 8FH 8FI 8FJ 8FK ABUWG AFKRA AZQEC BBNVY BENPR BHPHI CCPQU DWQXO FYUFA GHDGH GNUQQ HCIFZ K9. LK8 M0S M1P M2P M7P PHGZM PHGZT PIMPY PJZUB PKEHL PPXIY PQEST PQGLB PQQKQ PQUKI Q9U 7X8 5PM DOA
DOI	10.7554/eLife.87115
DatabaseName	CrossRef ProQuest Central (Corporate) Health & Medical Collection ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) Science Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Journals Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Collection ProQuest Central Natural Science Collection ProQuest One Community College ProQuest Central Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student SciTech Premium ProQuest Health & Medical Complete (Alumni) Biological Sciences ProQuest Health & Medical Collection ProQuest Medical Database Science Database Biological Science Database ProQuest Central Premium ProQuest One Academic Publicly Available Content Database ProQuest Health & Medical Research Collection ProQuest One Academic Middle East (New) One Health & Nursing ProQuest One Academic Eastern Edition (DO NOT USE) One Applied & Life Sciences ProQuest One Academic (retired) ProQuest One Academic UKI Edition ProQuest Central Basic MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals
DatabaseTitle	CrossRef Publicly Available Content Database ProQuest Central Student ProQuest One Academic Middle East (New) ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest One Health & Nursing ProQuest Natural Science Collection ProQuest Central ProQuest One Applied & Life Sciences ProQuest Health & Medical Research Collection Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Health & Medical Research Collection Biological Science Collection ProQuest Central (New) ProQuest Medical Library (Alumni) ProQuest Science Journals (Alumni Edition) ProQuest Biological Science Collection ProQuest Central Basic ProQuest Science Journals ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest One Academic (New) ProQuest Central (Alumni) MEDLINE - Academic
DatabaseTitleList	MEDLINE - Academic CrossRef Publicly Available Content Database
Database_xml	– sequence: 1 dbid: DOA name: Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: PIMPY name: ProQuest Publicly Available Content url: http://search.proquest.com/publiccontent sourceTypes: Aggregation Database
DeliveryMethod	fulltext_linktorsrc
Discipline	Biology
EISSN	2050-084X
ExternalDocumentID	oai_doaj_org_article_2f4ea1420b75483d940eeb3406c239f4 PMC10581685 10_7554_eLife_87115
GrantInformation_xml	– fundername: ; grantid: 2021YFF1201500 – fundername: ; grantid: 81925015 – fundername: ; grantid: 32170653 – fundername: ; grantid: 2022YFC2702600 – fundername: ; grantid: 32270898 – fundername: ; grantid: 32230029
GroupedDBID	53G 5VS 7X7 88E 88I 8FE 8FH 8FI 8FJ AAFWJ AAKDD AAYXX ABUWG ACGFO ACGOD ACPRK ADBBV ADRAZ AENEX AFFHD AFKRA AFPKN ALMA_UNASSIGNED_HOLDINGS AOIJS AZQEC BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI CCPQU CITATION DIK DWQXO EMOBN FYUFA GNUQQ GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAO IEA IHR INH INR ISR ITC KQ8 LK8 M1P M2P M48 M7P M~E NQS OK1 PGMZT PHGZM PHGZT PIMPY PJZUB PPXIY PQGLB PQQKQ PROAC PSQYO RHI RNS RPM UKHRP 3V. 7XB 8FK K9. PKEHL PQEST PQUKI Q9U 7X8 PUEGO 5PM
ID	FETCH-LOGICAL-c453t-84ce0fdf1f2739230f1738b99bbb3943f51fe40a29db0d9d785fb3f7e46e13eb3
IEDL.DBID	DOA
ISICitedReferencesCount	9
ISICitedReferencesURI	http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=001134621600001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN	2050-084X
IngestDate	Fri Oct 03 12:32:27 EDT 2025 Tue Nov 04 02:06:12 EST 2025 Fri Sep 05 14:21:16 EDT 2025 Tue Oct 07 07:08:16 EDT 2025 Sat Nov 29 06:59:06 EST 2025 Tue Nov 18 21:16:58 EST 2025
IsDoiOpenAccess	true
IsOpenAccess	true
IsPeerReviewed	true
IsScholarly	true
Language	English
License	This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
LinkModel	DirectLink
MergedId	FETCHMERGED-LOGICAL-c453t-84ce0fdf1f2739230f1738b99bbb3943f51fe40a29db0d9d785fb3f7e46e13eb3
Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally to this work.
ORCID	0000-0001-9449-9321
OpenAccessLink	https://doaj.org/article/2f4ea1420b75483d940eeb3406c239f4
PMID	37847146
PQID	2884579335
PQPubID	2045579
ParticipantIDs	doaj_primary_oai_doaj_org_article_2f4ea1420b75483d940eeb3406c239f4 pubmedcentral_primary_oai_pubmedcentral_nih_gov_10581685 proquest_miscellaneous_2878292516 proquest_journals_2884579335 crossref_primary_10_7554_eLife_87115 crossref_citationtrail_10_7554_eLife_87115
PublicationCentury	2000
PublicationDate	2023-10-17
PublicationDateYYYYMMDD	2023-10-17
PublicationDate_xml	– month: 10 year: 2023 text: 2023-10-17 day: 17
PublicationDecade	2020
PublicationPlace	Cambridge
PublicationPlace_xml	– name: Cambridge
PublicationTitle	eLife
PublicationYear	2023
Publisher	eLife Sciences Publications Ltd eLife Sciences Publications, Ltd
Publisher_xml	– name: eLife Sciences Publications Ltd – name: eLife Sciences Publications, Ltd
References	Udugama (bib48) 2022; 50 Lange (bib18) 2016; 167 Ramírez (bib39) 2016; 44 Yuen (bib57) 2014; 141 Hayama (bib10) 2016; 83 Jensen-Seaman (bib13) 2004; 14 Prada-Luengo (bib37) 2019; 20 Shaha (bib41) 2010; 365 St John (bib46) 2016 Lu (bib21) 2021; 31 Chiu (bib4) 2020; 66 Lv (bib23) 2022; 12 Mehta (bib26) 2020; 15 Carroll (bib2) 1988; 8 Chen (bib3) 2021; 19 Van Roy (bib50) 2006; 45 Paulsen (bib36) 2021; 49 Zhang (bib58) 2008; 9 Henriksen (bib11) 2022; 82 Liu (bib20) 2017; 8 Wang (bib52) 2021; 599 Alleva (bib1) 2021; 9 Mann (bib24) 2022; 23 Møller (bib30) 2020; 12 Xi (bib55) 2010; 11 Mouakkad-Montoya (bib31) 2021; 118 Lachaud (bib17) 2004; 19 CNCB-NGDC Members and Partners (bib5) 2022; 50 Wang (bib53) 2021; 19 Paulsen (bib34) 2018; 34 Coquelle (bib6) 2002; 21 Hess (bib12) 2008; 636 Mohsen (bib27) 2016; 49 Danecek (bib7) 2021; 10 Zhang (bib59) 2021; 12 Wang (bib51) 2019; 10 Vacic (bib49) 2006; 22 Paulsen (bib35) 2019; 47 ROOSEN-RUNGE (bib40) 1962; 37 Sin (bib44) 2020; 117 Li (bib19) 2009; 25 Quinlan (bib38) 2010; 26 Shoshani (bib43) 2021; 591 Torres-Flores (bib47) 2020; 11 Matassov (bib25) 2004; 282 Lukaszewicz (bib22) 2021; 184 Singh (bib45) 2021; 9 Weinbauer (bib54) 2001; 64 Møller (bib28) 2015; 112 Møller (bib29) 2018; 9 Shibata (bib42) 2012; 336 Dillon (bib8) 2015; 11 Young (bib56) 2001; 64 Jung (bib15) 2019; 75 Kumar (bib16) 2017; 15 Noer (bib33) 2022; 38 Faust (bib9) 2014; 30 NjuChenlab (bib32) 2022 Jung (bib14) 2017; 18
References_xml	– volume: 19 start-page: 607 year: 2004 ident: bib17 article-title: Apoptosis and necrosis in human ejaculated spermatozoa publication-title: Human Reproduction doi: 10.1093/humrep/deh130 – volume: 184 start-page: 5970 year: 2021 ident: bib22 article-title: De novo deletions and duplications at recombination hotspots in mouse germlines publication-title: Cell doi: 10.1016/j.cell.2021.10.025 – volume: 9 year: 2021 ident: bib45 article-title: Heterogeneity in the Epigenetic Landscape of Murine Testis-Specific Histone Variants TH2A and TH2B Sharing the Same Bi-Directional Promoter publication-title: Frontiers in Cell and Developmental Biology doi: 10.3389/fcell.2021.755751 – volume: 112 start-page: E3114 year: 2015 ident: bib28 article-title: Extrachromosomal circular DNA is common in yeast publication-title: PNAS doi: 10.1073/pnas.1508825112 – volume: 64 start-page: 706 year: 2001 ident: bib56 article-title: Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris) publication-title: Biology of Reproduction doi: 10.1095/biolreprod64.2.706 – volume: 75 start-page: 154 year: 2019 ident: bib15 article-title: Maintenance of CTCF- and Transcription Factor-Mediated Interactions from the Gametes to the Early Mouse Embryo publication-title: Molecular Cell doi: 10.1016/j.molcel.2019.04.014 – volume: 10 year: 2019 ident: bib51 article-title: Essential role of Histone Replacement and Modifications in Male Fertility publication-title: Frontiers in Genetics doi: 10.3389/fgene.2019.00962 – volume: 282 start-page: 1 year: 2004 ident: bib25 article-title: Measurement of apoptosis by DNA fragmentation publication-title: Methods in Molecular Biology doi: 10.1385/1-59259-812-9:001 – volume: 38 start-page: 766 year: 2022 ident: bib33 article-title: Extrachromosomal circular DNA in cancer: history, current knowledge, and methods publication-title: Trends in Genetics doi: 10.1016/j.tig.2022.02.007 – volume: 9 year: 2018 ident: bib29 article-title: Circular DNA elements of chromosomal origin are common in healthy human somatic tissue publication-title: Nature Communications doi: 10.1038/s41467-018-03369-8 – volume: 83 start-page: 488 year: 2016 ident: bib10 article-title: Practical selection methods for rat and mouse round spermatids without DNA staining by flow cytometric cell sorting publication-title: Molecular Reproduction and Development doi: 10.1002/mrd.22644 – volume: 64 start-page: 120 year: 2001 ident: bib54 article-title: Quantitative analysis of spermatogenesis and apoptosis in the common marmoset (Callithrix jacchus) reveals high rates of spermatogonial turnover and high spermatogenic efficiency publication-title: Biology of Reproduction doi: 10.1095/biolreprod64.1.120 – volume: 117 start-page: 1658 year: 2020 ident: bib44 article-title: Identification and characterization of extrachromosomal circular DNA in maternal plasma publication-title: PNAS doi: 10.1073/pnas.1914949117 – volume: 8 start-page: 1525 year: 1988 ident: bib2 article-title: Double minute chromosomes can be produced from precursors derived from a chromosomal deletion publication-title: Molecular and Cellular Biology doi: 10.1128/mcb.8.4.1525-1533.1988 – volume-title: GitHub year: 2016 ident: bib46 article-title: Seqprep – volume: 45 start-page: 107 year: 2006 ident: bib50 article-title: Translocation-excision-deletion-amplification mechanism leading to nonsyntenic coamplification of MYC and ATBF1 publication-title: Genes, Chromosomes & Cancer doi: 10.1002/gcc.20272 – volume: 10 year: 2021 ident: bib7 article-title: Twelve years of SAMtools and BCFtools publication-title: GigaScience doi: 10.1093/gigascience/giab008 – volume: 118 year: 2021 ident: bib31 article-title: Quantitative assessment reveals the dominance of duplicated sequences in germline-derived extrachromosomal circular DNA publication-title: PNAS doi: 10.1073/pnas.2102842118 – volume: 11 year: 2020 ident: bib47 article-title: The interplay between replacement and Retention of Histones in the Sperm Genome publication-title: Frontiers in Genetics doi: 10.3389/fgene.2020.00780 – volume: 49 start-page: 2540 year: 2016 ident: bib27 article-title: The Discovery of Rolling Circle Amplification and Rolling Circle Transcription publication-title: Accounts of Chemical Research doi: 10.1021/acs.accounts.6b00417 – volume: 47 start-page: 4586 year: 2019 ident: bib35 article-title: Small extrachromosomal circular DNAs, microDNA, produce short regulatory RNAs that suppress gene expression independent of canonical promoters publication-title: Nucleic Acids Research doi: 10.1093/nar/gkz155 – volume: 82 start-page: 209 year: 2022 ident: bib11 article-title: Circular DNA in the human germline and its association with recombination publication-title: Molecular Cell doi: 10.1016/j.molcel.2021.11.027 – volume: 167 start-page: 695 year: 2016 ident: bib18 article-title: The Landscape of Mouse Meiotic Double-Strand Break Formation, Processing, and Repair publication-title: Cell doi: 10.1016/j.cell.2016.09.035 – volume: 12 start-page: 3762 year: 2020 ident: bib30 article-title: Near-Random Distribution of Chromosome-Derived Circular DNA in the Condensed Genome of Pigeons and the Larger, More Repeat-Rich Human Genome publication-title: Genome Biology and Evolution doi: 10.1093/gbe/evz281 – volume-title: GitHub year: 2022 ident: bib32 article-title: Eccdna_Detector_Tools – volume: 15 start-page: 1673 year: 2020 ident: bib26 article-title: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq publication-title: Nature Protocols doi: 10.1038/s41596-020-0301-0 – volume: 591 start-page: 137 year: 2021 ident: bib43 article-title: Chromothripsis drives the evolution of gene amplification in cancer publication-title: Nature doi: 10.1038/s41586-020-03064-z – volume: 11 year: 2010 ident: bib55 article-title: Predicting nucleosome positioning using a duration Hidden Markov Model publication-title: BMC Bioinformatics doi: 10.1186/1471-2105-11-346 – volume: 9 year: 2021 ident: bib1 article-title: Cataloging Human PRDM9 Allelic variation using long-read sequencing reveals PRDM9 Population specificity and two distinct groupings of related Alleles publication-title: Frontiers in Cell and Developmental Biology doi: 10.3389/fcell.2021.675286 – volume: 20 year: 2019 ident: bib37 article-title: Sensitive detection of circular DNAs at single-nucleotide resolution using guided realignment of partially aligned reads publication-title: BMC Bioinformatics doi: 10.1186/s12859-019-3160-3 – volume: 19 start-page: 578 year: 2021 ident: bib3 article-title: The Genome Sequence Archive Family: toward explosive data Growth and diverse data types publication-title: Genomics, Proteomics & Bioinformatics doi: 10.1016/j.gpb.2021.08.001 – volume: 49 start-page: 11787 year: 2021 ident: bib36 article-title: MicroDNA levels are dependent on MMEJ, repressed by c-NHEJ pathway, and stimulated by DNA damage publication-title: Nucleic Acids Research doi: 10.1093/nar/gkab984 – volume: 23 year: 2022 ident: bib24 article-title: ECCsplorer: a pipeline to detect extrachromosomal circular DNA (eccDNA) from next-generation sequencing data publication-title: BMC Bioinformatics doi: 10.1186/s12859-021-04545-2 – volume: 50 start-page: D27 year: 2022 ident: bib5 article-title: Database Resources of the National Genomics Data Center, China National Center for Bioinformation in 2022 publication-title: Nucleic Acids Research doi: 10.1093/nar/gkab951 – volume: 12 year: 2021 ident: bib59 article-title: ecc_finder: a robust and accurate tool for detecting extrachromosomal circular DNA from sequencing data publication-title: Frontiers in Plant Science doi: 10.3389/fpls.2021.743742 – volume: 9 year: 2008 ident: bib58 article-title: Model-based analysis of ChIP-Seq (MACS) publication-title: Genome Biology doi: 10.1186/gb-2008-9-9-r137 – volume: 11 start-page: 1749 year: 2015 ident: bib8 article-title: Production of Extrachromosomal MicroDNAs is linked to mismatch repair Pathways and Transcriptional Activity publication-title: Cell Reports doi: 10.1016/j.celrep.2015.05.020 – volume: 26 start-page: 841 year: 2010 ident: bib38 article-title: BEDTools: a flexible suite of utilities for comparing genomic features publication-title: Bioinformatics doi: 10.1093/bioinformatics/btq033 – volume: 636 start-page: 1 year: 2008 ident: bib12 article-title: Spermatogenesis and cycle of the seminiferous epithelium publication-title: Advances in Experimental Medicine and Biology doi: 10.1007/978-0-387-09597-4_1 – volume: 22 start-page: 1536 year: 2006 ident: bib49 article-title: Two Sample Logo: a graphical representation of the differences between two sets of sequence alignments publication-title: Bioinformatics doi: 10.1093/bioinformatics/btl151 – volume: 44 start-page: W160 year: 2016 ident: bib39 article-title: deepTools2: a next generation web server for deep-sequencing data analysis publication-title: Nucleic Acids Research doi: 10.1093/nar/gkw257 – volume: 365 start-page: 1501 year: 2010 ident: bib41 article-title: Male germ cell apoptosis: regulation and biology publication-title: Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences doi: 10.1098/rstb.2009.0124 – volume: 21 start-page: 7671 year: 2002 ident: bib6 article-title: Induction of multiple double-strand breaks within an hsr by meganucleaseI-SceI expression or fragile site activation leads to formation of double minutes and other chromosomal rearrangements publication-title: Oncogene doi: 10.1038/sj.onc.1205880 – volume: 50 start-page: 4500 year: 2022 ident: bib48 article-title: Histone H3.3 phosphorylation promotes heterochromatin formation by inhibiting H3K9/K36 histone demethylase publication-title: Nucleic Acids Research doi: 10.1093/nar/gkac259 – volume: 66 start-page: 754 year: 2020 ident: bib4 article-title: What is extrachromosomal circular DNA and What Does It Do? publication-title: Clinical Chemistry doi: 10.1093/clinchem/hvaa096 – volume: 12 year: 2022 ident: bib23 article-title: Circle-Seq reveals genomic and disease-specific hallmarks in urinary cell-free extrachromosomal circular DNAs publication-title: Clinical and Translational Medicine doi: 10.1002/ctm2.817 – volume: 19 year: 2021 ident: bib53 article-title: Extrachromosomal circular DNA: a new potential role in cancer progression publication-title: Journal of Translational Medicine doi: 10.1186/s12967-021-02927-x – volume: 599 start-page: 308 year: 2021 ident: bib52 article-title: eccDNAs are apoptotic products with high innate immunostimulatory activity publication-title: Nature doi: 10.1038/s41586-021-04009-w – volume: 141 start-page: 3483 year: 2014 ident: bib57 article-title: Histone H3.3 regulates dynamic chromatin states during spermatogenesis publication-title: Development doi: 10.1242/dev.106450 – volume: 25 start-page: 1754 year: 2009 ident: bib19 article-title: Fast and accurate short read alignment with Burrows-Wheeler transform publication-title: Bioinformatics doi: 10.1093/bioinformatics/btp324 – volume: 336 start-page: 82 year: 2012 ident: bib42 article-title: Extrachromosomal microDNAs and chromosomal microdeletions in normal tissues publication-title: Science doi: 10.1126/science.1213307 – volume: 15 start-page: 1197 year: 2017 ident: bib16 article-title: Normal and Cancerous Tissues Release Extrachromosomal Circular DNA (eccDNA) into the Circulation publication-title: Molecular Cancer Research doi: 10.1158/1541-7786.MCR-17-0095 – volume: 37 start-page: 343 year: 1962 ident: bib40 article-title: The process of spermatogenesis in mammals publication-title: Biological Reviews of the Cambridge Philosophical Society doi: 10.1111/j.1469-185x.1962.tb01616.x – volume: 31 start-page: 613 year: 2021 ident: bib21 article-title: Homotypic clustering of L1 and B1/Alu repeats compartmentalizes the 3D genome publication-title: Cell Research doi: 10.1038/s41422-020-00466-6 – volume: 14 start-page: 528 year: 2004 ident: bib13 article-title: Comparative recombination rates in the rat, mouse, and human genomes publication-title: Genome Research doi: 10.1101/gr.1970304 – volume: 34 start-page: 270 year: 2018 ident: bib34 article-title: Discoveries of Extrachromosomal Circles of DNA in Normal and Tumor Cells publication-title: Trends in Genetics doi: 10.1016/j.tig.2017.12.010 – volume: 30 start-page: 2503 year: 2014 ident: bib9 article-title: SAMBLASTER: fast duplicate marking and structural variant read extraction publication-title: Bioinformatics doi: 10.1093/bioinformatics/btu314 – volume: 8 year: 2017 ident: bib20 article-title: Molecular and Cellular Mechanisms of Apoptosis during Dissociated Spermatogenesis publication-title: Frontiers in Physiology doi: 10.3389/fphys.2017.00188 – volume: 18 start-page: 1366 year: 2017 ident: bib14 article-title: Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes publication-title: Cell Reports doi: 10.1016/j.celrep.2017.01.034
SSID	ssj0000748819
Score	2.4100516
Snippet	The landscape of extrachromosomal circular DNA (eccDNA) during mammalian spermatogenesis, as well as the biogenesis mechanism, remains to be explored. Here, we...
SourceID	doaj pubmedcentral proquest crossref
SourceType	Open Website Open Access Repository Aggregation Database Enrichment Source Index Database
SubjectTerms	Bioinformatics Biosynthesis Cell death Circular DNA Developmental Biology DNA fragmentation Euchromatin extrachromosomal circular DNA Genetics and Genomics Genomes Heterochromatin Meiosis microhomology Mitochondrial DNA Morphology Quality control Recombination hot spots Sperm Spermatogenesis
SummonAdditionalLinks	– databaseName: Biological Science Database dbid: M7P link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lb9QwELaggMSl5VWRUlCQekIKjWNnbZ9QKVQcyqoHkHqL4tc2UhuXZIvUf98ZJxsaCXHhEinxJLE0tucbe2Y-Qg64AhRSujpbaLhwakSmnSszA2jDWiFy4SJryalYLuX5uTobN9z6MaxysybGhdoGg3vkh4WUvITBxMpP178yZI3C09WRQuMheYRVElgM3Tub9ljAPEqweENangDDeehOG-8-gpOANLj3DFGs1z8DmfMQyXs252Tnf3v7jGyPaDM9GobHc_LAtS_Ik4F_8vYlsd8xHO8iXMX7LGaRAAJNTdPF8NT0y_IondIbU0xFScNlswotVkEOfbiCj_uuXsU8uXRIeUyx9ji8EVa4jDb9K_Lz5OuP42_ZSLuQGV6ydSa5cbm3nnqANoD_ck8Fk1oprTVTnPmSesfzulBW51ZZIUuvmReOLxxl4Jzvkq02tO41SQX1nhkrHeAWXpuizmuj7YJSK73Ruk7Ih40OKjPWJEdqjMsKfBNUWBUVVkWFJeRgEr4eSnH8XewzKnMSwfrZ8UHoVtU4HavCc1dTXuRagMvGrOK5g54DujEFU54nZH-j12qc1H31R6kJeT81w3TEM5a6deEGZQByKQCNi4TI2RCadWje0jYXsbA3YF2kQSn3_v33N-Qpkt6jBaVin2ytuxv3ljw2v9dN372LU-AOmBMXeQ priority: 102 providerName: ProQuest
Title	Microhomology-mediated circular DNA formation from oligonucleosomal fragments during spermatogenesis
URI	https://www.proquest.com/docview/2884579335 https://www.proquest.com/docview/2878292516 https://pubmed.ncbi.nlm.nih.gov/PMC10581685 https://doaj.org/article/2f4ea1420b75483d940eeb3406c239f4
Volume	12
WOSCitedRecordID	wos001134621600001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText	1
inHoldings	1
isFullTextHit
isPrint
journalDatabaseRights	– providerCode: PRVAON databaseName: Directory of Open Access Journals customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: DOA dateStart: 20130101 isFulltext: true titleUrlDefault: https://www.doaj.org/ providerName: Directory of Open Access Journals – providerCode: PRVHPJ databaseName: ROAD: Directory of Open Access Scholarly Resources customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: M~E dateStart: 20120101 isFulltext: true titleUrlDefault: https://road.issn.org providerName: ISSN International Centre – providerCode: PRVPQU databaseName: Biological Science Database customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: M7P dateStart: 20120101 isFulltext: true titleUrlDefault: http://search.proquest.com/biologicalscijournals providerName: ProQuest – providerCode: PRVPQU databaseName: Health & Medical Collection customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: 7X7 dateStart: 20120101 isFulltext: true titleUrlDefault: https://search.proquest.com/healthcomplete providerName: ProQuest – providerCode: PRVPQU databaseName: ProQuest Central customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: BENPR dateStart: 20120101 isFulltext: true titleUrlDefault: https://www.proquest.com/central providerName: ProQuest – providerCode: PRVPQU databaseName: ProQuest Publicly Available Content customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: PIMPY dateStart: 20120101 isFulltext: true titleUrlDefault: http://search.proquest.com/publiccontent providerName: ProQuest – providerCode: PRVPQU databaseName: Science Database customDbUrl: eissn: 2050-084X dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000748819 issn: 2050-084X databaseCode: M2P dateStart: 20120101 isFulltext: true titleUrlDefault: https://search.proquest.com/sciencejournals providerName: ProQuest
link	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3di9QwEB_0TsEX8RNXzyXCPQn1mibdJI93eofC7VJEYX0q-dwr3LWyuyf43ztJe8sWBF98GWiTtulkmvkNzfwG4JgrRCGl19nMoODUisx4X2YW0YZzQuTCp6oll2KxkMulqvZKfcU9YT09cK-4kyJwrykvciMQXDOneO4xAEQ_ZAumQmICRdSzF0ylNVigYVLVJ-QJdJkn_rIJ_gOGB7EA7p4LSkz9I3g53hy5520unsDjASaS0354T-Geb5_Bw75w5O_n4OZxH91Vd5OOs5T-gdCR2Gad9pWST4tTsstLJDGHhHTXzaprI31xt-lu8OZhrVcpwY30uYokkobjFd0qrn_N5gV8vzj_9vFzNtRLyCwv2TaT3Po8uEADYhIEbnmggkmjlDGGKc5CSYPnuS6UM7lTTsgyGBaE5zNPGSr1JRy0XetfARE0BGad9Ag4uLaFzrU1bkapk8Eaoyfw_k6FtR3IxGNNi-sag4qo7zrpu076nsDxrvPPnkPj793O4lzsukTi63QCzaEezKH-lzlM4OhuJuvha9zUhZS8xIWI4TPe7ZrxO4o_R3Tru9vYB7GSQrQ3m4AcWcBoQOOWtrlKjNwIUmP9kvL1_3iFN_Ao1rSPDpKKIzjYrm_9W3hgf22bzXoK98VSJCmncHh2vqi-TpPto5wXVZQC5WH1ZV79-AOOkA-G
linkProvider	Directory of Open Access Journals
linkToHtml	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1Lb9QwEB6VLQguvBGBAkEqF6TQOHHWzgGhQqm66u5qD0UqpxC_tpHapGS3oP4pfiNj50EjIW49cImUxHn688w3iWc-gG2aIgtJdB6MBS4okSwQWieBRLahFGMh0061ZMrmc358nC424FeXC2OnVXY20RlqVUn7jXwn4pwmCKY4-XD-PbCqUfbvaieh0cDiUF_-xJBt9X6yh_37Jor2Px99OghaVYFA0iReB5xKHRpliEHPjfQmNITFXKSpECJOaWwSYjQN8yhVIlSpYjwxIjZM07EmMcaeeN4bsEkR7HwEm4vJbPG1_6qDDpmjj20SARm66h09LYx-h2GJFd694vqcQsCA1g4nZV7xcvv3_rf3cx_utnza320GwAPY0OVDuNUobF4-AjWzEw5PqjO3Hrg8GeTYvixqNwHX35vv-n0Cp2-TbfzqtFhWpa3zXK2qMzy5qfOlywT0m6RO31ZXxyOqpXUUxeoxfLmWR3wCo7Iq9VPwGTEmloprZGY0l1Ee5lKoMSGKGylE7sHbrs8z2VZdt-IfpxlGXxYgmQNI5gDiwXbf-LwpNvL3Zh8tePomtkK421DVy6w1OFlkqM4JjULBMCiNVUpDjXeO_E1GcWqoB1sdjrLWbK2yPyDy4HW_Gw2O_YuUl7q6sG2QVKZIi8ce8AFkBzc03FMWJ650ObJ5K_SSPPv31V_B7YOj2TSbTuaHz-FOhMTS8gXCtmC0ri_0C7gpf6yLVf2yHYA-fLtuTP8GVXh25A
linkToPdf	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V3JbtRAEC2FsIgLO8IQwEjhguSM225Ptw8IBYYRUYbRHEDKzbi3iaXEDvYElF_j66huL8QS4pYDF0u22_tz1Su7qh7ALk2RhSQ6D6YCJ5RIFgitk0Ai21CKsZBpp1qyYMslPzpKV1vwq6-FsWmVvU10hlpV0n4jn0Sc0wTBFCcT06VFrGbzd2ffA6sgZf-09nIaLUQO9cVPDN-atwczfNavo2j-8cuHT0GnMBBImsSbgFOpQ6MMMejFkeqEhrCYizQVQsQpjU1CjKZhHqVKhCpVjCdGxIZpOtUkxjgU93sNrjPbtNylDa6G7zvomjl627YkkKHTnuhFYfQeBihWgveSE3RaASOCO07PvOTv5nf_5zt1D-50LNvfb1-L-7Clywdws9XdvHgI6rNNQzyuTt184KpnkHn7sqhdWq4_W-77Q1mnb0tw_OqkWFel7f5cNdUp7tzU-drVB_ptqadve67jFtXauo-ieQRfr-QSH8N2WZX6CfiMGBNLxTXyNZrLKA9zKdSUEMWNFCL34E3__DPZ9WK3kiAnGcZkFiyZA0vmwOLB7jD4rG1B8vdh7y2QhiG2b7hbUNXrrDNDWWSozgmNQsEwVI1VSkONZ46sTkZxaqgHOz2mss6YNdkfQHnwaliNZsj-W8pLXZ3bMUg1UyTLUw_4CL6jExqvKYtj19AcOb6Vf0me_vvoL-EWAjlbHCwPn8HtCNmmJRGE7cD2pj7Xz-GG_LEpmvqFexN9-HbVgP4Njwx-Iw
openUrl	ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Microhomology-mediated+circular+DNA+formation+from+oligonucleosomal+fragments+during+spermatogenesis&rft.jtitle=eLife&rft.au=Hu%2C+Jun&rft.au=Zhang%2C+Zhe&rft.au=Xiao%2C+Sai&rft.au=Cao%2C+Yalei&rft.date=2023-10-17&rft.issn=2050-084X&rft.eissn=2050-084X&rft.volume=12&rft_id=info:doi/10.7554%2FeLife.87115&rft.externalDBID=n%2Fa&rft.externalDocID=10_7554_eLife_87115
thumbnail_l	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2050-084X&client=summon
thumbnail_m	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2050-084X&client=summon
thumbnail_s	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2050-084X&client=summon