Mettl3-/Mettl14-mediated mRNA N6-methyladenosine modulates murine spermatogenesis
Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells （SSCs） produce hap- loid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine （m6A...
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| Published in | Cell research Vol. 27; no. 10; pp. 1216 - 1230 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.10.2017
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells （SSCs） produce hap- loid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine （m6A）, an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6A mRNA methylomes of mouse spermatogenic cells from five developmental stages： undifferentiated spermatogonia, type At spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactiva- tion of the m6A RNA methyltransferase Mettl3 or Mettll4 with Vasa-Cre causes loss of m6A and depletion of SSCs. m6A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Com- bined deletion of Mettl3 and Mettll4 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettll4 in advanced germ cells show normal spermatogenesis. The sper- matids from d6uble-mutant mice exhibit impaired translation of haploid-specific genes that are esseritial for spermio- genesis. This study highlights crucial roles of mRNA m6A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. |
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| AbstractList | Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells (SSCs) produce haploid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that
N
6
-methyladenosine (m
6
A), an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m
6
A mRNA methylomes of mouse spermatogenic cells from five developmental stages: undifferentiated spermatogonia, type A
1
spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactivation of the m
6
A RNA methyltransferase
Mettl3
or
Mettl14
with
V
asa
-Cre
causes loss of m
6
A and depletion of SSCs. m
6
A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Combined deletion of
Mettl3
and
Mettl14
in advanced germ cells with
Stra8-GFPCre
disrupts spermiogenesis, whereas mice with single deletion of either
Mettl3
or
Mettl14
in advanced germ cells show normal spermatogenesis. The spermatids from double-mutant mice exhibit impaired translation of haploid-specific genes that are essential for spermiogenesis. This study highlights crucial roles of mRNA m
6
A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells （SSCs） produce hap- loid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine （m6A）, an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6A mRNA methylomes of mouse spermatogenic cells from five developmental stages： undifferentiated spermatogonia, type At spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactiva- tion of the m6A RNA methyltransferase Mettl3 or Mettll4 with Vasa-Cre causes loss of m6A and depletion of SSCs. m6A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Com- bined deletion of Mettl3 and Mettll4 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettll4 in advanced germ cells show normal spermatogenesis. The sper- matids from d6uble-mutant mice exhibit impaired translation of haploid-specific genes that are esseritial for spermio- genesis. This study highlights crucial roles of mRNA m6A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells (SSCs) produce haploid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine (m6A), an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6A mRNA methylomes of mouse spermatogenic cells from five developmental stages: undifferentiated spermatogonia, type A1 spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactivation of the m6A RNA methyltransferase Mettl3 or Mettl14 with Vasa-Cre causes loss of m6A and depletion of SSCs. m6A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Combined deletion of Mettl3 and Mettl14 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettl14 in advanced germ cells show normal spermatogenesis. The spermatids from double-mutant mice exhibit impaired translation of haploid-specific genes that are essential for spermiogenesis. This study highlights crucial roles of mRNA m6A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis.Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells (SSCs) produce haploid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine (m6A), an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6A mRNA methylomes of mouse spermatogenic cells from five developmental stages: undifferentiated spermatogonia, type A1 spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactivation of the m6A RNA methyltransferase Mettl3 or Mettl14 with Vasa-Cre causes loss of m6A and depletion of SSCs. m6A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Combined deletion of Mettl3 and Mettl14 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettl14 in advanced germ cells show normal spermatogenesis. The spermatids from double-mutant mice exhibit impaired translation of haploid-specific genes that are essential for spermiogenesis. This study highlights crucial roles of mRNA m6A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells (SSCs) produce haploid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6 -methyladenosine (m6 A), an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6 A mRNA methylomes of mouse spermatogenic cells from five developmental stages: undifferentiated spermatogonia, type A1 spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactivation of the m6 A RNA methyltransferase Mettl3 or Mettl14 with Vasa-Cre causes loss of m6 A and depletion of SSCs. m6 A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Combined deletion of Mettl3 and Mettl14 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettl14 in advanced germ cells show normal spermatogenesis. The spermatids from double-mutant mice exhibit impaired translation of haploid-specific genes that are essential for spermiogenesis. This study highlights crucial roles of mRNA m6 A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. |
| Author | Zhen Lin;Phillip J Hsu;Xudong Xing;Jianhuo Fang;Zhike Lu;Qin Zou;Ke-Jia Zhang;Xiao Zhang;Yuchuan Zhou;Teng Zhang;Youcheng Zhang;Wanlu Song;Guifang Jia;Xuerui Yang;Chuan He;Ming-Han Tong |
| AuthorAffiliation | State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, China;Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, Howard Hughes Medical Institute, The University of Chicago, 929 East 57th Street, Chica- go, IL 60637, USA;MOE Key Laboratory of Bioinformatics, Center for Synthetic ＆ Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing 100084, China;Synthetic and Functional Biomolecules Center, Beo＇ing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Min- istry of Education, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, China |
| Author_xml | – sequence: 1 givenname: Zhen surname: Lin fullname: Lin, Zhen organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 2 givenname: Phillip J surname: Hsu fullname: Hsu, Phillip J organization: Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, Howard Hughes Medical Institute, The University of Chicago – sequence: 3 givenname: Xudong surname: Xing fullname: Xing, Xudong organization: MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University – sequence: 4 givenname: Jianhuo surname: Fang fullname: Fang, Jianhuo organization: MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University – sequence: 5 givenname: Zhike surname: Lu fullname: Lu, Zhike organization: Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, Howard Hughes Medical Institute, The University of Chicago – sequence: 6 givenname: Qin surname: Zou fullname: Zou, Qin organization: MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University – sequence: 7 givenname: Ke-Jia surname: Zhang fullname: Zhang, Ke-Jia organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 8 givenname: Xiao surname: Zhang fullname: Zhang, Xiao organization: Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University – sequence: 9 givenname: Yuchuan surname: Zhou fullname: Zhou, Yuchuan organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 10 givenname: Teng surname: Zhang fullname: Zhang, Teng organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 11 givenname: Youcheng surname: Zhang fullname: Zhang, Youcheng organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 12 givenname: Wanlu surname: Song fullname: Song, Wanlu organization: MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University – sequence: 13 givenname: Guifang surname: Jia fullname: Jia, Guifang organization: Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University – sequence: 14 givenname: Xuerui surname: Yang fullname: Yang, Xuerui email: yangxuerui@tsinghua.edu.cn organization: MOE Key Laboratory of Bioinformatics, Center for Synthetic & Systems Biology, THU-PKU Center for Life Sciences, School of Life Sciences, Tsinghua University – sequence: 15 givenname: Chuan surname: He fullname: He, Chuan email: chuanhe@uchicago.edu organization: Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, Howard Hughes Medical Institute, The University of Chicago, Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University – sequence: 16 givenname: Ming-Han surname: Tong fullname: Tong, Ming-Han email: minghan@sibcb.ac.cn organization: State Key Laboratory of Molecular Biology Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences |
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| ContentType | Journal Article |
| Copyright | Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences 2017 Copyright Nature Publishing Group Oct 2017 Copyright © 2017 Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences 2017 Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences |
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| DOI | 10.1038/cr.2017.117 |
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| DocumentTitleAlternate | Mettl3-/Mettl14-mediated mRNA N6-methyladenosine modulates murine spermatogenesis mRNA m6A modification regulates male germ cell development |
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| Keywords | A RNA modification spermatogonial stem cell spermiogenesis Mettl3 Mettl14 m |
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| Notes | Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells （SSCs） produce hap- loid spermatozoa. This highly specialized process is precisely controlled at the transcriptional, posttranscriptional, and translational levels. Here we report that N6-methyladenosine （m6A）, an epitranscriptomic mark regulating gene expression, plays essential roles during spermatogenesis. We present comprehensive m6A mRNA methylomes of mouse spermatogenic cells from five developmental stages： undifferentiated spermatogonia, type At spermatogonia, preleptotene spermatocytes, pachytene/diplotene spermatocytes, and round spermatids. Germ cell-specific inactiva- tion of the m6A RNA methyltransferase Mettl3 or Mettll4 with Vasa-Cre causes loss of m6A and depletion of SSCs. m6A depletion dysregulates translation of transcripts that are required for SSC proliferation/differentiation. Com- bined deletion of Mettl3 and Mettll4 in advanced germ cells with Stra8-GFPCre disrupts spermiogenesis, whereas mice with single deletion of either Mettl3 or Mettll4 in advanced germ cells show normal spermatogenesis. The sper- matids from d6uble-mutant mice exhibit impaired translation of haploid-specific genes that are esseritial for spermio- genesis. This study highlights crucial roles of mRNA m6A modification in germline development, potentially ensuring coordinated translation at different stages of spermatogenesis. 31-1568 m6A RNA modification; Mettl3; Mettll4; spermatogonial stem cell; spermiogenesis ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These two authors contributed equally to this work. |
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| PublicationTitle | Cell research |
| PublicationTitleAbbrev | Cell Res |
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| PublicationYear | 2017 |
| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| Snippet | Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells （SSCs） produce hap- loid spermatozoa. This highly specialized... Spermatogenesis is a differentiation process during which diploid spermatogonial stem cells (SSCs) produce haploid spermatozoa. This highly specialized process... |
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| SubjectTerms | 631/136/2434/1822 631/337/574 631/80/86 Biomedical and Life Sciences Cell Biology Cell proliferation Clonal deletion Deactivation Depletion Developmental stages Differentiation Gene expression Germ cells Inactivation Life Sciences Mice mRNA N6-methyladenosine Original original-article Pachytene Post-transcription Ribonucleic acid RNA RNA modification Rodents Spermatids Spermatocytes Spermatogenesis Spermatogonia Spermatozoa Spermiogenesis SSCS Stem cell transplantation Stem cells Transcription Translation 分化过程 基因表达调控 生殖细胞 突变小鼠 精原细胞 精子发生过程 |
| Title | Mettl3-/Mettl14-mediated mRNA N6-methyladenosine modulates murine spermatogenesis |
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