m6A Modification Prevents Formation of Endogenous Double-Stranded RNAs and Deleterious Innate Immune Responses during Hematopoietic Development
N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m6A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3...
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| Published in | Immunity (Cambridge, Mass.) Vol. 52; no. 6; pp. 1007 - 1021.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier Inc
16.06.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m6A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3 and m6A activated an aberrant innate immune response, mediated by the formation of endogenous double-stranded RNAs (dsRNAs). The aberrantly formed dsRNAs were long, highly m6A modified in their native state, characterized by low folding energies, and predominantly protein coding. We identified coinciding activation of pattern recognition receptor pathways normally tasked with the detection of foreign dsRNAs. Disruption of the aberrant immune response via abrogation of downstream Mavs or Rnasel signaling partially rescued the observed hematopoietic defects in METTL3-deficient cells in vitro and in vivo. Our results suggest that m6A modification protects against endogenous dsRNA formation and a deleterious innate immune response during mammalian hematopoietic development.
[Display omitted]
•Loss of METTL3 inhibits proliferation and differentiation of hematopoietic stem cells•Depletion of m6A results in aberrant dsRNA formation of long m6A-modified transcripts•Loss of METTL3 induces deleterious innate immune responses in hematopoiesis•Mavs and Rnasel depletion partially rescue defects in Vav-Cre+-Mettl3fl/fl mice
Little is known about the role of N6-methyladenosine (m6A) modifications in mammalian hematopoietic development. Gao et al. find that m6A modification of endogenous transcripts preserves their recognition as self by preventing aberrant formation of double-stranded RNA. Deletion of m6A writer Mettl3 and loss of m6A activates pattern recognition receptor pathways, culminating in a deleterious innate immune response and hematopoietic failure. |
|---|---|
| AbstractList | N
6
methyladenosine (m
6
A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m
6
A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3 and m
6
A activated an aberrant innate immune response, mediated by the formation of endogenous double-stranded RNAs (dsRNAs). The aberrantly formed dsRNAs were long, highly m
6
A modified in their native state, characterized by low folding energies, and predominantly protein-coding. We identified coinciding activation of pattern recognition receptor pathways normally tasked with the detection of foreign dsRNAs. Disruption of the aberrant immune response via abrogation of downstream
Mavs
or
Rnasel
signaling partially rescued the observed hematopoietic defects in METTL3-deficient cells
in vitro
and
in vivo
. Our results suggest that m
6
A modification protects against endogenous dsRNA formation and a deleterious innate immune response during mammalian hematopoietic development.
Little is known about the role of
N
6
-methyladenosine (m
6
A) modifications in mammalian hematopoietic development, Gao et al. find that m
6
A modification of endogenous transcripts preserves their recognition as self by preventing aberrant formation of double-stranded RNA. Deletion of m
6
A writer
Mettl3
and loss of m
6
A activates pattern recognition receptor pathways, culminating in a deleterious innate immune response and hematopoietic failure. N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m6A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3 and m6A activated an aberrant innate immune response, mediated by the formation of endogenous double-stranded RNAs (dsRNAs). The aberrantly formed dsRNAs were long, highly m6A modified in their native state, characterized by low folding energies, and predominantly protein coding. We identified coinciding activation of pattern recognition receptor pathways normally tasked with the detection of foreign dsRNAs. Disruption of the aberrant immune response via abrogation of downstream Mavs or Rnasel signaling partially rescued the observed hematopoietic defects in METTL3-deficient cells in vitro and in vivo. Our results suggest that m6A modification protects against endogenous dsRNA formation and a deleterious innate immune response during mammalian hematopoietic development.N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m6A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3 and m6A activated an aberrant innate immune response, mediated by the formation of endogenous double-stranded RNAs (dsRNAs). The aberrantly formed dsRNAs were long, highly m6A modified in their native state, characterized by low folding energies, and predominantly protein coding. We identified coinciding activation of pattern recognition receptor pathways normally tasked with the detection of foreign dsRNAs. Disruption of the aberrant immune response via abrogation of downstream Mavs or Rnasel signaling partially rescued the observed hematopoietic defects in METTL3-deficient cells in vitro and in vivo. Our results suggest that m6A modification protects against endogenous dsRNA formation and a deleterious innate immune response during mammalian hematopoietic development. N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that conditional deletion of the m6A writer METTL3 in murine fetal liver resulted in hematopoietic failure and perinatal lethality. Loss of METTL3 and m6A activated an aberrant innate immune response, mediated by the formation of endogenous double-stranded RNAs (dsRNAs). The aberrantly formed dsRNAs were long, highly m6A modified in their native state, characterized by low folding energies, and predominantly protein coding. We identified coinciding activation of pattern recognition receptor pathways normally tasked with the detection of foreign dsRNAs. Disruption of the aberrant immune response via abrogation of downstream Mavs or Rnasel signaling partially rescued the observed hematopoietic defects in METTL3-deficient cells in vitro and in vivo. Our results suggest that m6A modification protects against endogenous dsRNA formation and a deleterious innate immune response during mammalian hematopoietic development. [Display omitted] •Loss of METTL3 inhibits proliferation and differentiation of hematopoietic stem cells•Depletion of m6A results in aberrant dsRNA formation of long m6A-modified transcripts•Loss of METTL3 induces deleterious innate immune responses in hematopoiesis•Mavs and Rnasel depletion partially rescue defects in Vav-Cre+-Mettl3fl/fl mice Little is known about the role of N6-methyladenosine (m6A) modifications in mammalian hematopoietic development. Gao et al. find that m6A modification of endogenous transcripts preserves their recognition as self by preventing aberrant formation of double-stranded RNA. Deletion of m6A writer Mettl3 and loss of m6A activates pattern recognition receptor pathways, culminating in a deleterious innate immune response and hematopoietic failure. |
| Author | Xiao, Andrew Song, Yuanbin Joshi, Poorval Biancon, Giulia Fan, Rong Teng, Rhea Dura, Burak Liu, Chengyang Fu, Xiaoying Gbyli, Rana Iwasaki, Akiko Liu, Wei Flavell, Richard A. Ardasheva, Anastasia Gao, Yimeng Kudo, Eriko Li, Hua-Bing Lee, Veronica Viero, Gabriella Tebaldi, Toma Vasic, Radovan Lobben, Kirsten Wang, Xiaman Halene, Stephanie Nelakanti, Raman |
| AuthorAffiliation | 7 Institute of Biophysics, CNR Unit at Trento, Via Sommarive 18, Povo Trento 38123, Italy 11 These authors contributed equally 8 Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA 2 Yale Stem Cell Center and Yale RNA Center, Yale University School of Medicine, New Haven, CT 06520, USA 10 Shanghai Jiao Tong University School of Medicine-Yale Institute for Immune Metabolism, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China 1 Section of Hematology, Yale Cancer Center and Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520, USA 4 Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA 5 Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520, USA 6 Department of Biomedical Engineering and Yale Cancer Center, Yale University, New Haven, Connecticut 06520, USA 9 Yale Institute for Immune Metabolism, Shanghai Jiao Tong University Sc |
| AuthorAffiliation_xml | – name: 1 Section of Hematology, Yale Cancer Center and Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520, USA – name: 12 Lead contact – name: 11 These authors contributed equally – name: 7 Institute of Biophysics, CNR Unit at Trento, Via Sommarive 18, Povo Trento 38123, Italy – name: 4 Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA – name: 5 Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520, USA – name: 6 Department of Biomedical Engineering and Yale Cancer Center, Yale University, New Haven, Connecticut 06520, USA – name: 9 Yale Institute for Immune Metabolism, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China – name: 10 Shanghai Jiao Tong University School of Medicine-Yale Institute for Immune Metabolism, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China – name: 2 Yale Stem Cell Center and Yale RNA Center, Yale University School of Medicine, New Haven, CT 06520, USA – name: 3 Department of Genetics and Yale Stem Cell Center, Yale University School of Medicine, New Haven, Connecticut 06520, USA – name: 8 Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA |
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Iwasaki, Akiko organization: Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520, USA – sequence: 20 givenname: Rong surname: Fan fullname: Fan, Rong organization: Yale Stem Cell Center and Yale RNA Center, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 21 givenname: Andrew surname: Xiao fullname: Xiao, Andrew organization: Department of Genetics and Yale Stem Cell Center, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 22 givenname: Richard A. surname: Flavell fullname: Flavell, Richard A. email: richard.flavell@yale.edu organization: Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 23 givenname: Hua-Bing surname: Li fullname: Li, Hua-Bing email: huabing.li@shsmu.edu.cn organization: Shanghai Institute of Immunology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China – sequence: 24 givenname: Toma surname: Tebaldi fullname: Tebaldi, Toma email: toma.tebaldi@yale.edu organization: Section of Hematology, Yale Cancer Center and Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 25 givenname: Stephanie orcidid: 0000-0002-2737-9810 surname: Halene fullname: Halene, Stephanie email: stephanie.halene@yale.edu organization: Section of Hematology, Yale Cancer Center and Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520, USA |
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| Keywords | dsRNA RNA modification hematopoietic development hematopoiesis innate immune response METTL3 m6A N6-methyladenosine epitranscriptome double-stranded RNA |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contribution Conceptualization, S.H., R.A.F., H.-B.L., Y.G. and R.V.; Methodology, S.H., H.-B.L., A.X., R.F., Y.G. and R.V.; Investigation, Y.G., R.V., Y.S., R.T., C.L., R.G., K.L., and V.L.; Data analysis, Y.G., R.V., Y.S.; Bioinformatics, T.T. and G.B.; Validation, Y.G., R.V., R.G., R.N., C.L., E.K., K.L., W.L., A.A., X.F., X.W., B.D., G.V., and A.I.; Writing – Original Draft, S.H., Y.G., R.V. and T.T.; Writing – Review & Editing, S.H., H.-B.L., Y.G., R.V. and T.T.; Funding Acquisition, S.H.; Resources, R.G., A.A. and P.J.; Project Administration, S.H., R.A.F.; Supervision, S.H., H.-B.L. and T.T.. |
| ORCID | 0000-0002-2737-9810 |
| OpenAccessLink | http://www.cell.com/article/S1074761320301849/pdf |
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| PublicationDate | 20200616 |
| PublicationDateYYYYMMDD | 2020-06-16 |
| PublicationDate_xml | – month: 06 year: 2020 text: 20200616 day: 16 |
| PublicationDecade | 2020 |
| PublicationTitle | Immunity (Cambridge, Mass.) |
| PublicationYear | 2020 |
| Publisher | Elsevier Inc |
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| Snippet | N6-methyladenosine (m6A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show that... N 6 methyladenosine (m 6 A) is the most abundant RNA modification, but little is known about its role in mammalian hematopoietic development. Here, we show... |
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| SubjectTerms | double-stranded RNA dsRNA epitranscriptome hematopoiesis hematopoietic development innate immune response m6A METTL3 N6-methyladenosine RNA modification |
| Title | m6A Modification Prevents Formation of Endogenous Double-Stranded RNAs and Deleterious Innate Immune Responses during Hematopoietic Development |
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