SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action

Yong Seok Oh; Pu Gao; Ko Woon Lee; Ilaria Ceglia; Ji Seon Seo; Xiaozhu Zhang; Jung Hyuck Ahn; Brian T. Chait; Dinshaw J. Patel; Yong Kim; Paul Greengard

doi:10.1016/j.cell.2013.01.014

SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action

Yong Seok Oh, Pu Gao, Ko Woon Lee, Ilaria Ceglia, Ji Seon Seo, Xiaozhu Zhang, Jung Hyuck Ahn, Brian T. Chait, Dinshaw J. Patel, Yong Kim, Paul Greengard

Department of Biochemistry

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

93 Scopus citations

Abstract

p11, through unknown mechanisms, is required for behavioral and cellular responses to selective serotonin reuptake inhibitors (SSRIs). We show that SMARCA3, a chromatin-remodeling factor, is a target for the p11/annexin A2 heterotetrameric complex. Determination of the crystal structure indicates that SMARCA3 peptide binds to a hydrophobic pocket in the heterotetramer. Formation of this complex increases the DNA-binding affinity of SMARCA3 and its localization to the nuclear matrix fraction. In the dentate gyrus, both p11 and SMARCA3 are highly enriched in hilar mossy cells and basket cells. The SSRI fluoxetine induces expression of p11 in both cell types and increases the amount of the ternary complex of p11/annexin A2/SMARCA3. SSRI-induced neurogenesis and behavioral responses are abolished by constitutive knockout of SMARCA3. Our studies indicate a central role for a chromatin-remodeling factor in the SSRI/p11 signaling pathway and suggest an approach to the development of improved antidepressant therapies. PaperClip:

Original language	English
Pages (from-to)	831-843
Number of pages	13
Journal	Cell
Volume	152
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2013.01.014
State	Published - 14 Feb 2013

Bibliographical note

Funding Information:
This work was supported by DOD/USAMRAA Grant W81XWH-09-1-0392 to Y.K.; DOD/USAMRAA Grant W81XWH-09-1-0402 to P. Greengard; the JPB Foundation to P. Greengard; the Fisher Center Foundation to P. Greengard; NIH grants (MH090963, DA10044, and AG09464) to Y.K. and P. Greengard; and the Maloris Foundation and the Abby Rockefeller Mauze Trust to D.J.P. We thank the staff at beamline 24ID-C of the Advanced Photon Source at the Argonne National Laboratory and beamline X29 of the National Synchrotron Light Source at the Brookhaven National Laboratory for assistance with data collection. We thank Daesoo Kim, Eric Schmidt, Jennifer Wagner-Schmidt, and Yotam Sagi for their helpful advice and discussion, and Elisabeth Griggs for technical assistance. We would like to thank Ji-Eun Kim for the mass spectrometry analysis. Finally, we would like to acknowledge Rada Norinsky and the Rockefeller University Transgenics Services Laboratory for their excellent IVF services; and Henry Zebroski III and Nagarajan Chandramouli from The Rockefeller University Proteomics Resource Center.

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title = "SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action",

abstract = "p11, through unknown mechanisms, is required for behavioral and cellular responses to selective serotonin reuptake inhibitors (SSRIs). We show that SMARCA3, a chromatin-remodeling factor, is a target for the p11/annexin A2 heterotetrameric complex. Determination of the crystal structure indicates that SMARCA3 peptide binds to a hydrophobic pocket in the heterotetramer. Formation of this complex increases the DNA-binding affinity of SMARCA3 and its localization to the nuclear matrix fraction. In the dentate gyrus, both p11 and SMARCA3 are highly enriched in hilar mossy cells and basket cells. The SSRI fluoxetine induces expression of p11 in both cell types and increases the amount of the ternary complex of p11/annexin A2/SMARCA3. SSRI-induced neurogenesis and behavioral responses are abolished by constitutive knockout of SMARCA3. Our studies indicate a central role for a chromatin-remodeling factor in the SSRI/p11 signaling pathway and suggest an approach to the development of improved antidepressant therapies. PaperClip:",

author = "Oh, {Yong Seok} and Pu Gao and Lee, {Ko Woon} and Ilaria Ceglia and Seo, {Ji Seon} and Xiaozhu Zhang and Ahn, {Jung Hyuck} and Chait, {Brian T.} and Patel, {Dinshaw J.} and Yong Kim and Paul Greengard",

note = "Funding Information: This work was supported by DOD/USAMRAA Grant W81XWH-09-1-0392 to Y.K.; DOD/USAMRAA Grant W81XWH-09-1-0402 to P. Greengard; the JPB Foundation to P. Greengard; the Fisher Center Foundation to P. Greengard; NIH grants (MH090963, DA10044, and AG09464) to Y.K. and P. Greengard; and the Maloris Foundation and the Abby Rockefeller Mauze Trust to D.J.P. We thank the staff at beamline 24ID-C of the Advanced Photon Source at the Argonne National Laboratory and beamline X29 of the National Synchrotron Light Source at the Brookhaven National Laboratory for assistance with data collection. We thank Daesoo Kim, Eric Schmidt, Jennifer Wagner-Schmidt, and Yotam Sagi for their helpful advice and discussion, and Elisabeth Griggs for technical assistance. We would like to thank Ji-Eun Kim for the mass spectrometry analysis. Finally, we would like to acknowledge Rada Norinsky and the Rockefeller University Transgenics Services Laboratory for their excellent IVF services; and Henry Zebroski III and Nagarajan Chandramouli from The Rockefeller University Proteomics Resource Center. ",

year = "2013",

month = feb,

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doi = "10.1016/j.cell.2013.01.014",

language = "English",

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T1 - SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action

AU - Oh, Yong Seok

AU - Gao, Pu

AU - Lee, Ko Woon

AU - Ceglia, Ilaria

AU - Seo, Ji Seon

AU - Zhang, Xiaozhu

AU - Ahn, Jung Hyuck

AU - Chait, Brian T.

AU - Patel, Dinshaw J.

AU - Kim, Yong

AU - Greengard, Paul

N1 - Funding Information: This work was supported by DOD/USAMRAA Grant W81XWH-09-1-0392 to Y.K.; DOD/USAMRAA Grant W81XWH-09-1-0402 to P. Greengard; the JPB Foundation to P. Greengard; the Fisher Center Foundation to P. Greengard; NIH grants (MH090963, DA10044, and AG09464) to Y.K. and P. Greengard; and the Maloris Foundation and the Abby Rockefeller Mauze Trust to D.J.P. We thank the staff at beamline 24ID-C of the Advanced Photon Source at the Argonne National Laboratory and beamline X29 of the National Synchrotron Light Source at the Brookhaven National Laboratory for assistance with data collection. We thank Daesoo Kim, Eric Schmidt, Jennifer Wagner-Schmidt, and Yotam Sagi for their helpful advice and discussion, and Elisabeth Griggs for technical assistance. We would like to thank Ji-Eun Kim for the mass spectrometry analysis. Finally, we would like to acknowledge Rada Norinsky and the Rockefeller University Transgenics Services Laboratory for their excellent IVF services; and Henry Zebroski III and Nagarajan Chandramouli from The Rockefeller University Proteomics Resource Center.

PY - 2013/2/14

Y1 - 2013/2/14

N2 - p11, through unknown mechanisms, is required for behavioral and cellular responses to selective serotonin reuptake inhibitors (SSRIs). We show that SMARCA3, a chromatin-remodeling factor, is a target for the p11/annexin A2 heterotetrameric complex. Determination of the crystal structure indicates that SMARCA3 peptide binds to a hydrophobic pocket in the heterotetramer. Formation of this complex increases the DNA-binding affinity of SMARCA3 and its localization to the nuclear matrix fraction. In the dentate gyrus, both p11 and SMARCA3 are highly enriched in hilar mossy cells and basket cells. The SSRI fluoxetine induces expression of p11 in both cell types and increases the amount of the ternary complex of p11/annexin A2/SMARCA3. SSRI-induced neurogenesis and behavioral responses are abolished by constitutive knockout of SMARCA3. Our studies indicate a central role for a chromatin-remodeling factor in the SSRI/p11 signaling pathway and suggest an approach to the development of improved antidepressant therapies. PaperClip:

AB - p11, through unknown mechanisms, is required for behavioral and cellular responses to selective serotonin reuptake inhibitors (SSRIs). We show that SMARCA3, a chromatin-remodeling factor, is a target for the p11/annexin A2 heterotetrameric complex. Determination of the crystal structure indicates that SMARCA3 peptide binds to a hydrophobic pocket in the heterotetramer. Formation of this complex increases the DNA-binding affinity of SMARCA3 and its localization to the nuclear matrix fraction. In the dentate gyrus, both p11 and SMARCA3 are highly enriched in hilar mossy cells and basket cells. The SSRI fluoxetine induces expression of p11 in both cell types and increases the amount of the ternary complex of p11/annexin A2/SMARCA3. SSRI-induced neurogenesis and behavioral responses are abolished by constitutive knockout of SMARCA3. Our studies indicate a central role for a chromatin-remodeling factor in the SSRI/p11 signaling pathway and suggest an approach to the development of improved antidepressant therapies. PaperClip:

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U2 - 10.1016/j.cell.2013.01.014

DO - 10.1016/j.cell.2013.01.014

M3 - Article

C2 - 23415230

AN - SCOPUS:84874051985

SN - 0092-8674

VL - 152

SP - 831

EP - 843

JO - Cell

JF - Cell

IS - 4

ER -

SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action

Abstract

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