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

Research output: Contribution to journalArticle

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 languageEnglish (US)
Pages (from-to)215-223
Number of pages9
JournalCell Stem Cell
Volume12
Issue number2
DOIs
StatePublished - Feb 7 2013

Fingerprint

Neurogenesis
Neurons
Neural Stem Cells
Dendritic Spines
Adult Stem Cells
Dentate Gyrus
Hippocampus
frizzled related protein-3
Growth

ASJC Scopus subject areas

  • Cell Biology
  • Molecular Medicine
  • Genetics

Cite this

Jang, M. H., Bonaguidi, M. A., Kitabatake, Y., Sun, J., Song, J., Kang, E., ... 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

Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. / Jang, Mi Hyeon; Bonaguidi, Michael A.; Kitabatake, Yasuji; Sun, Jiaqi; Song, Juan; Kang, Eunchai; Jun, Heechul; Zhong, Chun; Su, Yijing; Guo, Junjie U.; Wang, Marie Xun; Sailor, Kurt A.; Kim, Ju Young; Gao, Yuan; Christian, Kimberly M.; Ming, Guo Li; Song, Hongjun.

In: Cell Stem Cell, Vol. 12, No. 2, 07.02.2013, p. 215-223.

Research output: Contribution to journalArticle

Jang, MH, Bonaguidi, MA, Kitabatake, Y, Sun, J, Song, J, Kang, E, Jun, H, Zhong, C, Su, Y, Guo, JU, Wang, MX, Sailor, KA, Kim, JY, Gao, Y, Christian, KM, Ming, GL & Song, H 2013, 'Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis', Cell Stem Cell, vol. 12, no. 2, pp. 215-223. https://doi.org/10.1016/j.stem.2012.11.021
Jang, Mi Hyeon ; Bonaguidi, Michael A. ; Kitabatake, Yasuji ; Sun, Jiaqi ; Song, Juan ; Kang, Eunchai ; Jun, Heechul ; Zhong, Chun ; Su, Yijing ; Guo, Junjie U. ; Wang, Marie Xun ; Sailor, Kurt A. ; Kim, Ju Young ; Gao, Yuan ; Christian, Kimberly M. ; Ming, Guo Li ; Song, Hongjun. / Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. In: Cell Stem Cell. 2013 ; Vol. 12, No. 2. pp. 215-223.
@article{963999e11ae9499096012639b8d3e26f,
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 = "Jang, {Mi Hyeon} 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 Kim, {Ju Young} and Yuan Gao and Christian, {Kimberly M.} and Ming, {Guo Li} and Hongjun Song",
year = "2013",
month = "2",
day = "7",
doi = "10.1016/j.stem.2012.11.021",
language = "English (US)",
volume = "12",
pages = "215--223",
journal = "Cell Stem Cell",
issn = "1934-5909",
publisher = "Cell Press",
number = "2",

}

TY - JOUR

T1 - Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis

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

PY - 2013/2/7

Y1 - 2013/2/7

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.

UR - http://www.scopus.com/inward/record.url?scp=84873577692&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84873577692&partnerID=8YFLogxK

U2 - 10.1016/j.stem.2012.11.021

DO - 10.1016/j.stem.2012.11.021

M3 - Article

C2 - 23395446

AN - SCOPUS:84873577692

VL - 12

SP - 215

EP - 223

JO - Cell Stem Cell

JF - Cell Stem Cell

SN - 1934-5909

IS - 2

ER -