Small-molecule inhibition of the METTL3/METTL14 complex suppresses neuroblastoma tumor growth and promotes differentiation
The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult c...
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| Published in: | Cell reports (Cambridge) Vol. 43; no. 5; p. 114165 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
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| Language: | English |
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| Abstract | The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m6A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m6A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma.
[Display omitted]
•Expression of RNA methyltransferases METTL3/14 correlates with survival in neuroblastoma•Inhibition of METTL3/14 decreases cell survival and reduces tumor growth in xenograft models•METTL3/14 inhibition regulates RNA stability by mediating site-specific m6A loss•METTL3/14 inhibition up-regulates differentiation-associated transcriptional networks
Pomaville et al. show that the catalytic activity of the METTL3/14 complex is critical for neuroblastoma growth. Pharmacological inhibition of METTL3/14 promoted neuroblastoma differentiation and suppressed tumor xenograft growth. Inhibitor treatment mediated m6A loss at sites specific for neuronal differentiation, increasing transcript stability and the expression of neuronal differentiation networks. |
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| AbstractList | The
N
6
-methyladenosine (m
6
A) RNA modification is an important regulator of gene expression. m
6
A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m
6
A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m
6
A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors
in vivo
. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma.
Pomaville et al. show that the catalytic activity of the METTL3/14 complex is critical for neuroblastoma growth. Pharmacological inhibition of METTL3/14 promoted neuroblastoma differentiation and suppressed tumor xenograft growth. Inhibitor treatment mediated m
6
A loss at sites specific for neuronal differentiation, increasing transcript stability and the expression of neuronal differentiation networks. The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m6A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m6A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma. The N -methyladenosine (m A) RNA modification is an important regulator of gene expression. m A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma. The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m6A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m6A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma.The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m6A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m6A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma. The N6-methyladenosine (m6A) RNA modification is an important regulator of gene expression. m6A is deposited by a methyltransferase complex that includes methyltransferase-like 3 (METTL3) and methyltransferase-like 14 (METTL14). High levels of METTL3/METTL14 drive the growth of many types of adult cancer, and METTL3/METTL14 inhibitors are emerging as new anticancer agents. However, little is known about the m6A epitranscriptome or the role of the METTL3/METTL14 complex in neuroblastoma, a common pediatric cancer. Here, we show that METTL3 knockdown or pharmacologic inhibition with the small molecule STM2457 leads to reduced neuroblastoma cell proliferation and increased differentiation. These changes in neuroblastoma phenotype are associated with decreased m6A deposition on transcripts involved in nervous system development and neuronal differentiation, with increased stability of target mRNAs. In preclinical studies, STM2457 treatment suppresses the growth of neuroblastoma tumors in vivo. Together, these results support the potential of METTL3/METTL14 complex inhibition as a therapeutic strategy against neuroblastoma. [Display omitted] •Expression of RNA methyltransferases METTL3/14 correlates with survival in neuroblastoma•Inhibition of METTL3/14 decreases cell survival and reduces tumor growth in xenograft models•METTL3/14 inhibition regulates RNA stability by mediating site-specific m6A loss•METTL3/14 inhibition up-regulates differentiation-associated transcriptional networks Pomaville et al. show that the catalytic activity of the METTL3/14 complex is critical for neuroblastoma growth. Pharmacological inhibition of METTL3/14 promoted neuroblastoma differentiation and suppressed tumor xenograft growth. Inhibitor treatment mediated m6A loss at sites specific for neuronal differentiation, increasing transcript stability and the expression of neuronal differentiation networks. |
| ArticleNumber | 114165 |
| Author | Krajewska, Malgorzata Sun, Hui-Lung Moore, Kelley He, Chuan Chlenski, Alexandre Ren, Peizhe Cohn, Susan L. Brodnik, Mallory Zhong, Yuhao Chennakesavalu, Mohansrinivas Wang, Pingluan Ge, Ruiqi Zhu, Zhongyu Jiang, Zhiwei Ye, Chang Gupta, Varsha Salwen, Helen George, Rani E. Applebaum, Mark A. Pomaville, Monica Borchert, Ryan |
| AuthorAffiliation | 2 Department of Chemistry, University of Chicago, Chicago, IL 60637, USA 3 Department of Pediatric Hematology/Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA 1 Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA 7 Present address: Department of Pediatric Oncology, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA 4 School of Biochemistry and Cell Biology, Biosciences Institute, University College Cork, Cork, Ireland 6 These authors contributed equally 8 Lead contact 5 Howard Hughes Medical Institute, University of Chicago, Chicago, Il 60637 USA |
| AuthorAffiliation_xml | – name: 2 Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – name: 1 Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – name: 5 Howard Hughes Medical Institute, University of Chicago, Chicago, Il 60637 USA – name: 7 Present address: Department of Pediatric Oncology, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA – name: 4 School of Biochemistry and Cell Biology, Biosciences Institute, University College Cork, Cork, Ireland – name: 6 These authors contributed equally – name: 3 Department of Pediatric Hematology/Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 8 Lead contact |
| Author_xml | – sequence: 1 givenname: Monica orcidid: 0009-0008-0498-5544 surname: Pomaville fullname: Pomaville, Monica organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 2 givenname: Mohansrinivas surname: Chennakesavalu fullname: Chennakesavalu, Mohansrinivas organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 3 givenname: Pingluan surname: Wang fullname: Wang, Pingluan organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 4 givenname: Zhiwei surname: Jiang fullname: Jiang, Zhiwei organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 5 givenname: Hui-Lung surname: Sun fullname: Sun, Hui-Lung organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 6 givenname: Peizhe surname: Ren fullname: Ren, Peizhe organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 7 givenname: Ryan surname: Borchert fullname: Borchert, Ryan organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 8 givenname: Varsha surname: Gupta fullname: Gupta, Varsha organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 9 givenname: Chang surname: Ye fullname: Ye, Chang organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 10 givenname: Ruiqi surname: Ge fullname: Ge, Ruiqi organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 11 givenname: Zhongyu surname: Zhu fullname: Zhu, Zhongyu organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 12 givenname: Mallory surname: Brodnik fullname: Brodnik, Mallory organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 13 givenname: Yuhao surname: Zhong fullname: Zhong, Yuhao organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 14 givenname: Kelley surname: Moore fullname: Moore, Kelley organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 15 givenname: Helen surname: Salwen fullname: Salwen, Helen organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 16 givenname: Rani E. surname: George fullname: George, Rani E. organization: Department of Pediatric Hematology/Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 17 givenname: Malgorzata surname: Krajewska fullname: Krajewska, Malgorzata organization: School of Biochemistry and Cell Biology, Biosciences Institute, University College Cork, Cork, Ireland – sequence: 18 givenname: Alexandre surname: Chlenski fullname: Chlenski, Alexandre organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 19 givenname: Mark A. surname: Applebaum fullname: Applebaum, Mark A. organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA – sequence: 20 givenname: Chuan surname: He fullname: He, Chuan organization: Department of Chemistry, University of Chicago, Chicago, IL 60637, USA – sequence: 21 givenname: Susan L. orcidid: 0000-0001-5749-7650 surname: Cohn fullname: Cohn, Susan L. email: scohn@bsd.uchicago.edu organization: Department of Pediatrics, University of Chicago Comer Children’s Hospital, Chicago, IL 60637, USA |
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| Issue | 5 |
| Keywords | gene expression regulation differentiation CP: Cancer neuroblastoma m6A tumor growth epitranscriptome therapeutic target mA |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, M.P., S.L.C., C.H., R.E.G., and M.K.; investigation, M.P., Z.J., P.W., M.C., H.-L.S., P.R., R.B., V.G., A.C., C.Y., R.G., Z.Z., M.B., Y.Z., K.M., and H.S.; writing – original draft, M.P. and S.L.C.; writing – review & editing, H.S., A.C., R.E.G., M.A.A., C.H., and S.L.C., visualization, M.P. and M.C.; supervision, M.A.A., C.H., and S.L.C.; funding acquisition, C.H. and S.L.C. |
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| SubjectTerms | Adenosine - analogs & derivatives Adenosine - metabolism Adenosine - pharmacology Animals Cell Differentiation - drug effects Cell Line, Tumor Cell Proliferation - drug effects CP: Cancer differentiation epitranscriptome gene expression regulation Gene Expression Regulation, Neoplastic - drug effects Humans m6A Methyltransferases - antagonists & inhibitors Methyltransferases - metabolism Mice neuroblastoma Neuroblastoma - drug therapy Neuroblastoma - genetics Neuroblastoma - metabolism Neuroblastoma - pathology therapeutic target tumor growth |
| Title | Small-molecule inhibition of the METTL3/METTL14 complex suppresses neuroblastoma tumor growth and promotes differentiation |
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