Post-transcriptional regulation of mouse neurogenesis by Pumilio proteins
Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the p...
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| Published in | Genes & development Vol. 31; no. 13; pp. 1354 - 1369 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Cold Spring Harbor Laboratory Press
01.07.2017
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| Abstract | Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory. Consistently, the mutant DG neurospheres generated fewer NSCs with defects in proliferation, survival, and differentiation, supporting a major role of Pum1 and Pum2 in hippocampal neurogenesis and function. Cross-linking immunoprecipitation revealed that Pum1 and Pum2 bind to thousands of mRNAs, with at least 694 common targets in multiple neurogenic pathways. Depleting Pum1 and/or Pum2 did not change the abundance of most target mRNAs but up-regulated their proteins, indicating that Pum1 and Pum2 regulate the translation of their target mRNAs. Moreover, Pum1 and Pum2 display RNA-dependent interaction with fragile X mental retardation protein (FMRP) and bind to one another's mRNA. This indicates that Pum proteins might form collaborative networks with FMRP and possibly other post-transcriptional regulators to regulate neurogenesis. |
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| AbstractList | Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory. Consistently, the mutant DG neurospheres generated fewer NSCs with defects in proliferation, survival, and differentiation, supporting a major role of Pum1 and Pum2 in hippocampal neurogenesis and function. Cross-linking immunoprecipitation revealed that Pum1 and Pum2 bind to thousands of mRNAs, with at least 694 common targets in multiple neurogenic pathways. Depleting Pum1 and/or Pum2 did not change the abundance of most target mRNAs but up-regulated their proteins, indicating that Pum1 and Pum2 regulate the translation of their target mRNAs. Moreover, Pum1 and Pum2 display RNA-dependent interaction with fragile X mental retardation protein (FMRP) and bind to one another's mRNA. This indicates that Pum proteins might form collaborative networks with FMRP and possibly other post-transcriptional regulators to regulate neurogenesis. Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory. Consistently, the mutant DG neurospheres generated fewer NSCs with defects in proliferation, survival, and differentiation, supporting a major role of Pum1 and Pum2 in hippocampal neurogenesis and function. Cross-linking immunoprecipitation revealed that Pum1 and Pum2 bind to thousands of mRNAs, with at least 694 common targets in multiple neurogenic pathways. Depleting Pum1 and/or Pum2 did not change the abundance of most target mRNAs but up-regulated their proteins, indicating that Pum1 and Pum2 regulate the translation of their target mRNAs. Moreover, Pum1 and Pum2 display RNA-dependent interaction with fragile X mental retardation protein (FMRP) and bind to one another's mRNA. This indicates that Pum proteins might form collaborative networks with FMRP and possibly other post-transcriptional regulators to regulate neurogenesis.Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory. Consistently, the mutant DG neurospheres generated fewer NSCs with defects in proliferation, survival, and differentiation, supporting a major role of Pum1 and Pum2 in hippocampal neurogenesis and function. Cross-linking immunoprecipitation revealed that Pum1 and Pum2 bind to thousands of mRNAs, with at least 694 common targets in multiple neurogenic pathways. Depleting Pum1 and/or Pum2 did not change the abundance of most target mRNAs but up-regulated their proteins, indicating that Pum1 and Pum2 regulate the translation of their target mRNAs. Moreover, Pum1 and Pum2 display RNA-dependent interaction with fragile X mental retardation protein (FMRP) and bind to one another's mRNA. This indicates that Pum proteins might form collaborative networks with FMRP and possibly other post-transcriptional regulators to regulate neurogenesis. In this study, Zhang et al. investigated post-transcriptional regulation during mammalian neurogenesis. They demonstrate that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory, and their data further suggest that PUM2 facilitates FMRP function and that Pum1 and Pum2 have different roles in neurogenesis. Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific inactivation of two murine post-transcriptional regulators, Pumilio 1 (Pum1) and Pum2, severely reduced the number of neural stem cells (NSCs) in the postnatal dentate gyrus (DG), drastically increased perinatal apoptosis, altered DG cell composition, and impaired learning and memory. Consistently, the mutant DG neurospheres generated fewer NSCs with defects in proliferation, survival, and differentiation, supporting a major role of Pum1 and Pum2 in hippocampal neurogenesis and function. Cross-linking immunoprecipitation revealed that Pum1 and Pum2 bind to thousands of mRNAs, with at least 694 common targets in multiple neurogenic pathways. Depleting Pum1 and/or Pum2 did not change the abundance of most target mRNAs but up-regulated their proteins, indicating that Pum1 and Pum2 regulate the translation of their target mRNAs. Moreover, Pum1 and Pum2 display RNA-dependent interaction with fragile X mental retardation protein (FMRP) and bind to one another's mRNA. This indicates that Pum proteins might form collaborative networks with FMRP and possibly other post-transcriptional regulators to regulate neurogenesis. |
| Author | Han, Wenqi Chen, Dong Lin, Haifan Xia, Jing Sestan, Nenad Zhang, Meng Hermes, Gretchen Neuenkirchen, Nils Cui, Xiekui |
| AuthorAffiliation | 3 Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, Connecticut 06536, USA 4 Department of Neuroscience, Yale School of Medicine, New Haven, Connecticut 06510, USA 2 Department of Cell Biology, Yale School of Medicine, New Haven, Connecticut 06520, USA 9 Department of Obstetrics and Gynecology, Yale School of Medicine, New Haven, Connecticut 06520, USA 5 Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut 06511, USA 7 Section of Comparative Medicine, Program in Cellular Neuroscience, Neurodegeneration, and Repair, Yale School of Medicine, New Haven, Connecticut 06520, USA 1 Yale Stem Cell Center, Yale School of Medicine, New Haven, Connecticut 06520, USA 8 Yale Child Study Center, Yale School of Medicine, New Haven, Connecticut 06519, USA 6 Department of Genetics, Yale School of Medicine, New Haven, Connecticut 06520, USA |
| AuthorAffiliation_xml | – name: 9 Department of Obstetrics and Gynecology, Yale School of Medicine, New Haven, Connecticut 06520, USA – name: 6 Department of Genetics, Yale School of Medicine, New Haven, Connecticut 06520, USA – name: 5 Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut 06511, USA – name: 2 Department of Cell Biology, Yale School of Medicine, New Haven, Connecticut 06520, USA – name: 4 Department of Neuroscience, Yale School of Medicine, New Haven, Connecticut 06510, USA – name: 8 Yale Child Study Center, Yale School of Medicine, New Haven, Connecticut 06519, USA – name: 1 Yale Stem Cell Center, Yale School of Medicine, New Haven, Connecticut 06520, USA – name: 3 Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, Connecticut 06536, USA – name: 7 Section of Comparative Medicine, Program in Cellular Neuroscience, Neurodegeneration, and Repair, Yale School of Medicine, New Haven, Connecticut 06520, USA |
| Author_xml | – sequence: 1 givenname: Meng surname: Zhang fullname: Zhang, Meng – sequence: 2 givenname: Dong surname: Chen fullname: Chen, Dong – sequence: 3 givenname: Jing surname: Xia fullname: Xia, Jing – sequence: 4 givenname: Wenqi surname: Han fullname: Han, Wenqi – sequence: 5 givenname: Xiekui surname: Cui fullname: Cui, Xiekui – sequence: 6 givenname: Nils surname: Neuenkirchen fullname: Neuenkirchen, Nils – sequence: 7 givenname: Gretchen surname: Hermes fullname: Hermes, Gretchen – sequence: 8 givenname: Nenad surname: Sestan fullname: Sestan, Nenad – sequence: 9 givenname: Haifan surname: Lin fullname: Lin, Haifan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28794184$$D View this record in MEDLINE/PubMed |
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| Keywords | mouse neural stem cell hippocampus FMRP post-transcriptional regulation mRNA Pumilio |
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| Snippet | Despite extensive studies on mammalian neurogenesis, its post-transcriptional regulation remains under-explored. Here we report that neural-specific... In this study, Zhang et al. investigated post-transcriptional regulation during mammalian neurogenesis. They demonstrate that neural-specific inactivation of... |
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| Title | Post-transcriptional regulation of mouse neurogenesis by Pumilio proteins |
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