Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis

Mi-Hyeon Jang; Michael A Bonaguidi; Yasuji Kitabatake; Jiaqi Sun; Juan Song; Eunchai Kang; Heechul Jun; Chun Zhong; Yijing Su; Junjie U Guo; Marie Xun Wang; Kurt A Sailor; Ju-Young Kim; Yuan Gao; Kimberly M Christian; Guo-li Ming; Hongjun Song

doi:10.1016/j.stem.2012.11.021

Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis

Mi-Hyeon Jang^* (Corresponding Author), Michael A Bonaguidi, Yasuji Kitabatake, Jiaqi Sun, Juan Song, Eunchai Kang, Heechul Jun, Chun Zhong, Yijing Su, Junjie U Guo, Marie Xun Wang, Kurt A Sailor, Ju-Young Kim, Yuan Gao, Kimberly M Christian, Guo-li Ming, Hongjun Song

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

154 Citations (Scopus)

Abstract

Adult neurogenesis, the process of generating mature neurons from adult neural stem cells, proceeds concurrently with ongoing neuronal circuit activity and is modulated by various physiological and pathological stimuli. The niche mechanism underlying the activity-dependent regulation of the sequential steps of adult neurogenesis remains largely unknown. Here, we report that neuronal activity decreases the expression of secreted frizzled-related protein 3 (sFRP3), a naturally secreted Wnt inhibitor highly expressed by adult dentate gyrus granule neurons. Sfrp3 deletion activates quiescent radial neural stem cells and promotes newborn neuron maturation, dendritic growth, and dendritic spine formation in the adult mouse hippocampus. Furthermore, sfrp3 reduction is essential for activity-induced adult neural progenitor proliferation and the acceleration of new neuron development. Our study identifies sFRP3 as an inhibitory niche factor from local mature dentate granule neurons that regulates multiple phases of adult hippocampal neurogenesis and suggests an interesting activity-dependent mechanism governing adult neurogenesis via the acute release of tonic inhibition.

Original language	English
Pages (from-to)	215-223
Number of pages	9
Journal	Cell Stem Cell
Volume	12
Issue number	2
DOIs	https://doi.org/10.1016/j.stem.2012.11.021
Publication status	Published - 7 Feb 2013
Externally published	Yes

Bibliographical note

ACKNOWLEDGMENTS
We thank Drs. D. Ginty, S. Jessberger, X. He, and members of the Song and Ming laboratories for their suggestions, A. Rattner and J. Nathans for generating sfrp3 KO mice, J.H. Shin and B. Xie for help with RNA-seq, and P. Worley for Arc antibodies and initial help with ECS. This work was supported by the NIH (NS047344, MH087874, and ES021957 to H.S; NS048271 and HD069184 to G.M.; MH090115 to M.-H.J.; and NS080913 to M.A.B) and NARSAD (Independent Investigator awards to H.S. and G.-l.M., and a Young Investigator award to M.-H.J.) and by postdoctoral fellowship awards from MSCRF to J.S., E.K., Y.S., and K.C.
Copyright © 2013 Elsevier Inc. All rights reserved.

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Jang, M.-H., Bonaguidi, M. A., Kitabatake, Y., Sun, J., Song, J., Kang, E., Jun, H., Zhong, C., Su, Y., Guo, J. U., Wang, M. X., Sailor, K. A., Kim, J.-Y., Gao, Y., Christian, K. M., Ming, G., & Song, H. (2013). Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell, 12(2), 215-223. https://doi.org/10.1016/j.stem.2012.11.021

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title = "Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis",

abstract = "Adult neurogenesis, the process of generating mature neurons from adult neural stem cells, proceeds concurrently with ongoing neuronal circuit activity and is modulated by various physiological and pathological stimuli. The niche mechanism underlying the activity-dependent regulation of the sequential steps of adult neurogenesis remains largely unknown. Here, we report that neuronal activity decreases the expression of secreted frizzled-related protein 3 (sFRP3), a naturally secreted Wnt inhibitor highly expressed by adult dentate gyrus granule neurons. Sfrp3 deletion activates quiescent radial neural stem cells and promotes newborn neuron maturation, dendritic growth, and dendritic spine formation in the adult mouse hippocampus. Furthermore, sfrp3 reduction is essential for activity-induced adult neural progenitor proliferation and the acceleration of new neuron development. Our study identifies sFRP3 as an inhibitory niche factor from local mature dentate granule neurons that regulates multiple phases of adult hippocampal neurogenesis and suggests an interesting activity-dependent mechanism governing adult neurogenesis via the acute release of tonic inhibition.",

author = "Mi-Hyeon Jang and Bonaguidi, {Michael A} and Yasuji Kitabatake and Jiaqi Sun and Juan Song and Eunchai Kang and Heechul Jun and Chun Zhong and Yijing Su and Guo, {Junjie U} and Wang, {Marie Xun} and Sailor, {Kurt A} and Ju-Young Kim and Yuan Gao and Christian, {Kimberly M} and Guo-li Ming and Hongjun Song",

note = "ACKNOWLEDGMENTS We thank Drs. D. Ginty, S. Jessberger, X. He, and members of the Song and Ming laboratories for their suggestions, A. Rattner and J. Nathans for generating sfrp3 KO mice, J.H. Shin and B. Xie for help with RNA-seq, and P. Worley for Arc antibodies and initial help with ECS. This work was supported by the NIH (NS047344, MH087874, and ES021957 to H.S; NS048271 and HD069184 to G.M.; MH090115 to M.-H.J.; and NS080913 to M.A.B) and NARSAD (Independent Investigator awards to H.S. and G.-l.M., and a Young Investigator award to M.-H.J.) and by postdoctoral fellowship awards from MSCRF to J.S., E.K., Y.S., and K.C. Copyright {\textcopyright} 2013 Elsevier Inc. All rights reserved.",

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AU - Jang, Mi-Hyeon

AU - Bonaguidi, Michael A

AU - Kitabatake, Yasuji

AU - Sun, Jiaqi

AU - Song, Juan

AU - Kang, Eunchai

AU - Jun, Heechul

AU - Zhong, Chun

AU - Su, Yijing

AU - Guo, Junjie U

AU - Wang, Marie Xun

AU - Sailor, Kurt A

AU - Kim, Ju-Young

AU - Gao, Yuan

AU - Christian, Kimberly M

AU - Ming, Guo-li

AU - Song, Hongjun

N1 - ACKNOWLEDGMENTS We thank Drs. D. Ginty, S. Jessberger, X. He, and members of the Song and Ming laboratories for their suggestions, A. Rattner and J. Nathans for generating sfrp3 KO mice, J.H. Shin and B. Xie for help with RNA-seq, and P. Worley for Arc antibodies and initial help with ECS. This work was supported by the NIH (NS047344, MH087874, and ES021957 to H.S; NS048271 and HD069184 to G.M.; MH090115 to M.-H.J.; and NS080913 to M.A.B) and NARSAD (Independent Investigator awards to H.S. and G.-l.M., and a Young Investigator award to M.-H.J.) and by postdoctoral fellowship awards from MSCRF to J.S., E.K., Y.S., and K.C. Copyright © 2013 Elsevier Inc. All rights reserved.

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N2 - Adult neurogenesis, the process of generating mature neurons from adult neural stem cells, proceeds concurrently with ongoing neuronal circuit activity and is modulated by various physiological and pathological stimuli. The niche mechanism underlying the activity-dependent regulation of the sequential steps of adult neurogenesis remains largely unknown. Here, we report that neuronal activity decreases the expression of secreted frizzled-related protein 3 (sFRP3), a naturally secreted Wnt inhibitor highly expressed by adult dentate gyrus granule neurons. Sfrp3 deletion activates quiescent radial neural stem cells and promotes newborn neuron maturation, dendritic growth, and dendritic spine formation in the adult mouse hippocampus. Furthermore, sfrp3 reduction is essential for activity-induced adult neural progenitor proliferation and the acceleration of new neuron development. Our study identifies sFRP3 as an inhibitory niche factor from local mature dentate granule neurons that regulates multiple phases of adult hippocampal neurogenesis and suggests an interesting activity-dependent mechanism governing adult neurogenesis via the acute release of tonic inhibition.

AB - Adult neurogenesis, the process of generating mature neurons from adult neural stem cells, proceeds concurrently with ongoing neuronal circuit activity and is modulated by various physiological and pathological stimuli. The niche mechanism underlying the activity-dependent regulation of the sequential steps of adult neurogenesis remains largely unknown. Here, we report that neuronal activity decreases the expression of secreted frizzled-related protein 3 (sFRP3), a naturally secreted Wnt inhibitor highly expressed by adult dentate gyrus granule neurons. Sfrp3 deletion activates quiescent radial neural stem cells and promotes newborn neuron maturation, dendritic growth, and dendritic spine formation in the adult mouse hippocampus. Furthermore, sfrp3 reduction is essential for activity-induced adult neural progenitor proliferation and the acceleration of new neuron development. Our study identifies sFRP3 as an inhibitory niche factor from local mature dentate granule neurons that regulates multiple phases of adult hippocampal neurogenesis and suggests an interesting activity-dependent mechanism governing adult neurogenesis via the acute release of tonic inhibition.

U2 - 10.1016/j.stem.2012.11.021

DO - 10.1016/j.stem.2012.11.021

M3 - Article

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SN - 1934-5909

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EP - 223

JO - Cell Stem Cell

JF - Cell Stem Cell

IS - 2

ER -

Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis

Abstract

Bibliographical note

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