A high-resolution enhancer atlas of the developing telencephalon

Axel Visel; Leila Taher; Hani Girgis; Dalit May; Olga Golonzhka; Renee V. Hoch; Gabriel L. McKinsey; Kartik Pattabiraman; Shanni N. Silberberg; Matthew J. Blow; David V. Hansen; Alex S. Nord; Jennifer A. Akiyama; Amy Holt; Roya Hosseini; Sengthavy Phouanenavong; Ingrid Plajzer-Frick; Malak Shoukry; Veena Afzal; Tommy Kaplan; Arnold R. Kriegstein; Edward M. Rubin; Ivan Ovcharenko; Len A. Pennacchio; John L.R. Rubenstein

doi:10.1016/j.cell.2012.12.041

A high-resolution enhancer atlas of the developing telencephalon

Axel Visel^*, Leila Taher, Hani Girgis, Dalit May, Olga Golonzhka, Renee V. Hoch, Gabriel L. McKinsey, Kartik Pattabiraman, Shanni N. Silberberg, Matthew J. Blow, David V. Hansen, Alex S. Nord, Jennifer A. Akiyama, Amy Holt, Roya Hosseini, Sengthavy Phouanenavong, Ingrid Plajzer-Frick, Malak Shoukry, Veena Afzal, Tommy KaplanArnold R. Kriegstein, Edward M. Rubin, Ivan Ovcharenko, Len A. Pennacchio, John L.R. Rubenstein

^*Corresponding author for this work

The Rachel and Selim Benin School of Engineering and Computer Science

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

192 Scopus citations

Abstract

The mammalian telencephalon plays critical roles in cognition, motor function, and emotion. Though many of the genes required for its development have been identified, the distant-acting regulatory sequences orchestrating their in vivo expression are mostly unknown. Here, we describe a digital atlas of in vivo enhancers active in subregions of the developing telencephalon. We identified more than 4,600 candidate embryonic forebrain enhancers and studied the in vivo activity of 329 of these sequences in transgenic mouse embryos. We generated serial sets of histological brain sections for 145 reproducible forebrain enhancers, resulting in a publicly accessible web-based data collection comprising more than 32,000 sections. We also used epigenomic analysis of human and mouse cortex tissue to directly compare the genome-wide enhancer architecture in these species. These data provide a primary resource for investigating gene regulatory mechanisms of telencephalon development and enable studies of the role of distant-acting enhancers in neurodevelopmental disorders.

Original language	English
Pages (from-to)	895-908
Number of pages	14
Journal	Cell
Volume	152
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2012.12.041
State	Published - 14 Feb 2013

Bibliographical note

Funding Information:
The authors thank Julian Golder and Noah Efron for help with digital image acquisition and data processing; Bing Ren and Zirong Li for help with chromatin immunoprecipitation from embryonic mouse tissue; Inna Dubchak, Simon Minovitsky, and Alexandre Poliakov for website support; and staff at San Francisco General Hospital Women’s Options Center for their consideration in allowing us to access donated fetal tissue. A.V. and L.A.P. were supported by NINDS grant R01NS062859A and by NHGRI grant R01HG003988. J.L.R.R. was supported by the Nina Ireland, Weston Havens Foundation, NINDS grant R01NS34661, NIMH grant R01MH081880, and NIMH grant R37MH049428. J.L.R.R. and A.R.K. were supported by CIRM RB2-1602. G.M. and S.N.S. were supported by T32 GM007449, K.P. was supported by T32 GMO7618, R.H. was supported by F32 MH081431, and O.G. was supported by NARSAD. A.R.K. was supported by NINDS grant R01NS075998. I.O. was supported by the Intramural Research Program of the NIH, National Library of Medicine. Research was conducted at the E.O. Lawrence Berkeley National Laboratory and performed under Department of Energy Contract DE-AC02-05CH11231, University of California.

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Visel, A., Taher, L., Girgis, H., May, D., Golonzhka, O., Hoch, R. V., McKinsey, G. L., Pattabiraman, K., Silberberg, S. N., Blow, M. J., Hansen, D. V., Nord, A. S., Akiyama, J. A., Holt, A., Hosseini, R., Phouanenavong, S., Plajzer-Frick, I., Shoukry, M., Afzal, V., ... Rubenstein, J. L. R. (2013). A high-resolution enhancer atlas of the developing telencephalon. Cell, 152(4), 895-908. https://doi.org/10.1016/j.cell.2012.12.041

@article{272f563c57644917949ef2d4cb2ce373,

title = "A high-resolution enhancer atlas of the developing telencephalon",

abstract = "The mammalian telencephalon plays critical roles in cognition, motor function, and emotion. Though many of the genes required for its development have been identified, the distant-acting regulatory sequences orchestrating their in vivo expression are mostly unknown. Here, we describe a digital atlas of in vivo enhancers active in subregions of the developing telencephalon. We identified more than 4,600 candidate embryonic forebrain enhancers and studied the in vivo activity of 329 of these sequences in transgenic mouse embryos. We generated serial sets of histological brain sections for 145 reproducible forebrain enhancers, resulting in a publicly accessible web-based data collection comprising more than 32,000 sections. We also used epigenomic analysis of human and mouse cortex tissue to directly compare the genome-wide enhancer architecture in these species. These data provide a primary resource for investigating gene regulatory mechanisms of telencephalon development and enable studies of the role of distant-acting enhancers in neurodevelopmental disorders.",

author = "Axel Visel and Leila Taher and Hani Girgis and Dalit May and Olga Golonzhka and Hoch, {Renee V.} and McKinsey, {Gabriel L.} and Kartik Pattabiraman and Silberberg, {Shanni N.} and Blow, {Matthew J.} and Hansen, {David V.} and Nord, {Alex S.} and Akiyama, {Jennifer A.} and Amy Holt and Roya Hosseini and Sengthavy Phouanenavong and Ingrid Plajzer-Frick and Malak Shoukry and Veena Afzal and Tommy Kaplan and Kriegstein, {Arnold R.} and Rubin, {Edward M.} and Ivan Ovcharenko and Pennacchio, {Len A.} and Rubenstein, {John L.R.}",

note = "Funding Information: The authors thank Julian Golder and Noah Efron for help with digital image acquisition and data processing; Bing Ren and Zirong Li for help with chromatin immunoprecipitation from embryonic mouse tissue; Inna Dubchak, Simon Minovitsky, and Alexandre Poliakov for website support; and staff at San Francisco General Hospital Women{\textquoteright}s Options Center for their consideration in allowing us to access donated fetal tissue. A.V. and L.A.P. were supported by NINDS grant R01NS062859A and by NHGRI grant R01HG003988. J.L.R.R. was supported by the Nina Ireland, Weston Havens Foundation, NINDS grant R01NS34661, NIMH grant R01MH081880, and NIMH grant R37MH049428. J.L.R.R. and A.R.K. were supported by CIRM RB2-1602. G.M. and S.N.S. were supported by T32 GM007449, K.P. was supported by T32 GMO7618, R.H. was supported by F32 MH081431, and O.G. was supported by NARSAD. A.R.K. was supported by NINDS grant R01NS075998. I.O. was supported by the Intramural Research Program of the NIH, National Library of Medicine. Research was conducted at the E.O. Lawrence Berkeley National Laboratory and performed under Department of Energy Contract DE-AC02-05CH11231, University of California. ",

year = "2013",

month = feb,

day = "14",

doi = "10.1016/j.cell.2012.12.041",

language = "אנגלית",

volume = "152",

pages = "895--908",

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Visel, A, Taher, L, Girgis, H, May, D, Golonzhka, O, Hoch, RV, McKinsey, GL, Pattabiraman, K, Silberberg, SN, Blow, MJ, Hansen, DV, Nord, AS, Akiyama, JA, Holt, A, Hosseini, R, Phouanenavong, S, Plajzer-Frick, I, Shoukry, M, Afzal, V, Kaplan, T, Kriegstein, AR, Rubin, EM, Ovcharenko, I, Pennacchio, LA & Rubenstein, JLR 2013, 'A high-resolution enhancer atlas of the developing telencephalon', Cell, vol. 152, no. 4, pp. 895-908. https://doi.org/10.1016/j.cell.2012.12.041

TY - JOUR

T1 - A high-resolution enhancer atlas of the developing telencephalon

AU - Visel, Axel

AU - Taher, Leila

AU - Girgis, Hani

AU - May, Dalit

AU - Golonzhka, Olga

AU - Hoch, Renee V.

AU - McKinsey, Gabriel L.

AU - Pattabiraman, Kartik

AU - Silberberg, Shanni N.

AU - Blow, Matthew J.

AU - Hansen, David V.

AU - Nord, Alex S.

AU - Akiyama, Jennifer A.

AU - Holt, Amy

AU - Hosseini, Roya

AU - Phouanenavong, Sengthavy

AU - Plajzer-Frick, Ingrid

AU - Shoukry, Malak

AU - Afzal, Veena

AU - Kaplan, Tommy

AU - Kriegstein, Arnold R.

AU - Rubin, Edward M.

AU - Ovcharenko, Ivan

AU - Pennacchio, Len A.

AU - Rubenstein, John L.R.

N1 - Funding Information: The authors thank Julian Golder and Noah Efron for help with digital image acquisition and data processing; Bing Ren and Zirong Li for help with chromatin immunoprecipitation from embryonic mouse tissue; Inna Dubchak, Simon Minovitsky, and Alexandre Poliakov for website support; and staff at San Francisco General Hospital Women’s Options Center for their consideration in allowing us to access donated fetal tissue. A.V. and L.A.P. were supported by NINDS grant R01NS062859A and by NHGRI grant R01HG003988. J.L.R.R. was supported by the Nina Ireland, Weston Havens Foundation, NINDS grant R01NS34661, NIMH grant R01MH081880, and NIMH grant R37MH049428. J.L.R.R. and A.R.K. were supported by CIRM RB2-1602. G.M. and S.N.S. were supported by T32 GM007449, K.P. was supported by T32 GMO7618, R.H. was supported by F32 MH081431, and O.G. was supported by NARSAD. A.R.K. was supported by NINDS grant R01NS075998. I.O. was supported by the Intramural Research Program of the NIH, National Library of Medicine. Research was conducted at the E.O. Lawrence Berkeley National Laboratory and performed under Department of Energy Contract DE-AC02-05CH11231, University of California.

PY - 2013/2/14

Y1 - 2013/2/14

N2 - The mammalian telencephalon plays critical roles in cognition, motor function, and emotion. Though many of the genes required for its development have been identified, the distant-acting regulatory sequences orchestrating their in vivo expression are mostly unknown. Here, we describe a digital atlas of in vivo enhancers active in subregions of the developing telencephalon. We identified more than 4,600 candidate embryonic forebrain enhancers and studied the in vivo activity of 329 of these sequences in transgenic mouse embryos. We generated serial sets of histological brain sections for 145 reproducible forebrain enhancers, resulting in a publicly accessible web-based data collection comprising more than 32,000 sections. We also used epigenomic analysis of human and mouse cortex tissue to directly compare the genome-wide enhancer architecture in these species. These data provide a primary resource for investigating gene regulatory mechanisms of telencephalon development and enable studies of the role of distant-acting enhancers in neurodevelopmental disorders.

AB - The mammalian telencephalon plays critical roles in cognition, motor function, and emotion. Though many of the genes required for its development have been identified, the distant-acting regulatory sequences orchestrating their in vivo expression are mostly unknown. Here, we describe a digital atlas of in vivo enhancers active in subregions of the developing telencephalon. We identified more than 4,600 candidate embryonic forebrain enhancers and studied the in vivo activity of 329 of these sequences in transgenic mouse embryos. We generated serial sets of histological brain sections for 145 reproducible forebrain enhancers, resulting in a publicly accessible web-based data collection comprising more than 32,000 sections. We also used epigenomic analysis of human and mouse cortex tissue to directly compare the genome-wide enhancer architecture in these species. These data provide a primary resource for investigating gene regulatory mechanisms of telencephalon development and enable studies of the role of distant-acting enhancers in neurodevelopmental disorders.

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SN - 0092-8674

VL - 152

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JO - Cell

JF - Cell

IS - 4

ER -

A high-resolution enhancer atlas of the developing telencephalon

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