A comprehensive transcriptional map of primate brain development

Trygve E. Bakken, Jeremy A. Miller, Song Lin Ding, Susan M. Sunkin, Kimberly A. Smith, Lydia Ng, Aaron Szafer, Rachel A. Dalley, Joshua J. Royall, Tracy Lemon, Sheila Shapouri, Kaylynn Aiona, James Arnold, Jeffrey L. Bennett, Darren Bertagnolli, Kristopher Bickley, Andrew Boe, Krissy Brouner, Stephanie Butler, Emi ByrnesShiella Caldejon, Anita Carey, Shelby Cate, Mike Chapin, Jefferey Chen, Nick Dee, Tsega Desta, Tim A. Dolbeare, Nadia Dotson, Amanda Ebbert, Erich Fulfs, Garrett Gee, Terri L. Gilbert, Jeff Goldy, Lindsey Gourley, Ben Gregor, Guangyu Gu, Jon Hall, Zeb Haradon, David R. Haynor, Nika Hejazinia, Anna Hoerder-Suabedissen, Robert Howard, Jay Jochim, Marty Kinnunen, Ali Kriedberg, Chihchau L. Kuan, Christopher Lau, Chang Kyu Lee, Felix Lee, Lon Luong, Naveed Mastan, Ryan May, Jose Melchor, Nerick Mosqueda, Erika Mott, Kiet Ngo, Julie Nyhus, Aaron Oldre, Eric Olson, Jody Parente, Patrick D. Parker, Sheana Parry, Julie Pendergraft, Lydia Potekhina, Melissa Reding, Zackery L. Riley, Tyson Roberts, Brandon Rogers, Kate Roll, David Rosen, David Sandman, Melaine Sarreal, Nadiya Shapovalova, Shu Shi, Nathan Sjoquist, Andy J. Sodt, Robbie Townsend, Lissette Velasquez, Udi Wagley, Wayne B. Wakeman, Cassandra White, Crissa Bennett, Jennifer Wu, Rob Young, Brian L. Youngstrom, Paul Wohnoutka, Richard A. Gibbs, Jeffrey Rogers, John G. Hohmann, Michael J. Hawrylycz, Robert F. Hevner, Zoltán Molnár, John W. Phillips, Chinh Dang, Allan R. Jones, David G Amaral, Amy Bernard, Ed S. Lein

Research output: Contribution to journalArticle

114 Citations (Scopus)

Abstract

The transcriptional underpinnings of brain development remain poorly understood, particularly in humans and closely related non-human primates. We describe a high-resolution transcriptional atlas of rhesus monkey (Macaca mulatta) brain development that combines dense temporal sampling of prenatal and postnatal periods with fine anatomical division of cortical and subcortical regions associated with human neuropsychiatric disease. Gene expression changes more rapidly before birth, both in progenitor cells and maturing neurons. Cortical layers and areas acquire adult-like molecular profiles surprisingly late in postnatal development. Disparate cell populations exhibit distinct developmental timing of gene expression, but also unexpected synchrony of processes underlying neural circuit construction including cell projection and adhesion. Candidate risk genes for neurodevelopmental disorders including primary microcephaly, autism spectrum disorder, intellectual disability, and schizophrenia show disease-specific spatiotemporal enrichment within developing neocortex. Human developmental expression trajectories are more similar to monkey than rodent, although approximately 9% of genes show human-specific regulation with evidence for prolonged maturation or neoteny compared to monkey.

Original languageEnglish (US)
Pages (from-to)367-375
Number of pages9
JournalNature
Volume535
Issue number7612
DOIs
StatePublished - Jul 13 2016

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Primates
Brain
Macaca mulatta
Haplorhini
Developmental Genes
Gene Expression
Microcephaly
Atlases
Neocortex
Cell Adhesion
Intellectual Disability
Genes
Rodentia
Schizophrenia
Stem Cells
Parturition
Neurons
Population

ASJC Scopus subject areas

  • Medicine(all)
  • General

Cite this

Bakken, T. E., Miller, J. A., Ding, S. L., Sunkin, S. M., Smith, K. A., Ng, L., ... Lein, E. S. (2016). A comprehensive transcriptional map of primate brain development. Nature, 535(7612), 367-375. https://doi.org/10.1038/nature18637

A comprehensive transcriptional map of primate brain development. / Bakken, Trygve E.; Miller, Jeremy A.; Ding, Song Lin; Sunkin, Susan M.; Smith, Kimberly A.; Ng, Lydia; Szafer, Aaron; Dalley, Rachel A.; Royall, Joshua J.; Lemon, Tracy; Shapouri, Sheila; Aiona, Kaylynn; Arnold, James; Bennett, Jeffrey L.; Bertagnolli, Darren; Bickley, Kristopher; Boe, Andrew; Brouner, Krissy; Butler, Stephanie; Byrnes, Emi; Caldejon, Shiella; Carey, Anita; Cate, Shelby; Chapin, Mike; Chen, Jefferey; Dee, Nick; Desta, Tsega; Dolbeare, Tim A.; Dotson, Nadia; Ebbert, Amanda; Fulfs, Erich; Gee, Garrett; Gilbert, Terri L.; Goldy, Jeff; Gourley, Lindsey; Gregor, Ben; Gu, Guangyu; Hall, Jon; Haradon, Zeb; Haynor, David R.; Hejazinia, Nika; Hoerder-Suabedissen, Anna; Howard, Robert; Jochim, Jay; Kinnunen, Marty; Kriedberg, Ali; Kuan, Chihchau L.; Lau, Christopher; Lee, Chang Kyu; Lee, Felix; Luong, Lon; Mastan, Naveed; May, Ryan; Melchor, Jose; Mosqueda, Nerick; Mott, Erika; Ngo, Kiet; Nyhus, Julie; Oldre, Aaron; Olson, Eric; Parente, Jody; Parker, Patrick D.; Parry, Sheana; Pendergraft, Julie; Potekhina, Lydia; Reding, Melissa; Riley, Zackery L.; Roberts, Tyson; Rogers, Brandon; Roll, Kate; Rosen, David; Sandman, David; Sarreal, Melaine; Shapovalova, Nadiya; Shi, Shu; Sjoquist, Nathan; Sodt, Andy J.; Townsend, Robbie; Velasquez, Lissette; Wagley, Udi; Wakeman, Wayne B.; White, Cassandra; Bennett, Crissa; Wu, Jennifer; Young, Rob; Youngstrom, Brian L.; Wohnoutka, Paul; Gibbs, Richard A.; Rogers, Jeffrey; Hohmann, John G.; Hawrylycz, Michael J.; Hevner, Robert F.; Molnár, Zoltán; Phillips, John W.; Dang, Chinh; Jones, Allan R.; Amaral, David G; Bernard, Amy; Lein, Ed S.

In: Nature, Vol. 535, No. 7612, 13.07.2016, p. 367-375.

Research output: Contribution to journalArticle

Bakken, TE, Miller, JA, Ding, SL, Sunkin, SM, Smith, KA, Ng, L, Szafer, A, Dalley, RA, Royall, JJ, Lemon, T, Shapouri, S, Aiona, K, Arnold, J, Bennett, JL, Bertagnolli, D, Bickley, K, Boe, A, Brouner, K, Butler, S, Byrnes, E, Caldejon, S, Carey, A, Cate, S, Chapin, M, Chen, J, Dee, N, Desta, T, Dolbeare, TA, Dotson, N, Ebbert, A, Fulfs, E, Gee, G, Gilbert, TL, Goldy, J, Gourley, L, Gregor, B, Gu, G, Hall, J, Haradon, Z, Haynor, DR, Hejazinia, N, Hoerder-Suabedissen, A, Howard, R, Jochim, J, Kinnunen, M, Kriedberg, A, Kuan, CL, Lau, C, Lee, CK, Lee, F, Luong, L, Mastan, N, May, R, Melchor, J, Mosqueda, N, Mott, E, Ngo, K, Nyhus, J, Oldre, A, Olson, E, Parente, J, Parker, PD, Parry, S, Pendergraft, J, Potekhina, L, Reding, M, Riley, ZL, Roberts, T, Rogers, B, Roll, K, Rosen, D, Sandman, D, Sarreal, M, Shapovalova, N, Shi, S, Sjoquist, N, Sodt, AJ, Townsend, R, Velasquez, L, Wagley, U, Wakeman, WB, White, C, Bennett, C, Wu, J, Young, R, Youngstrom, BL, Wohnoutka, P, Gibbs, RA, Rogers, J, Hohmann, JG, Hawrylycz, MJ, Hevner, RF, Molnár, Z, Phillips, JW, Dang, C, Jones, AR, Amaral, DG, Bernard, A & Lein, ES 2016, 'A comprehensive transcriptional map of primate brain development', Nature, vol. 535, no. 7612, pp. 367-375. https://doi.org/10.1038/nature18637
Bakken TE, Miller JA, Ding SL, Sunkin SM, Smith KA, Ng L et al. A comprehensive transcriptional map of primate brain development. Nature. 2016 Jul 13;535(7612):367-375. https://doi.org/10.1038/nature18637
Bakken, Trygve E. ; Miller, Jeremy A. ; Ding, Song Lin ; Sunkin, Susan M. ; Smith, Kimberly A. ; Ng, Lydia ; Szafer, Aaron ; Dalley, Rachel A. ; Royall, Joshua J. ; Lemon, Tracy ; Shapouri, Sheila ; Aiona, Kaylynn ; Arnold, James ; Bennett, Jeffrey L. ; Bertagnolli, Darren ; Bickley, Kristopher ; Boe, Andrew ; Brouner, Krissy ; Butler, Stephanie ; Byrnes, Emi ; Caldejon, Shiella ; Carey, Anita ; Cate, Shelby ; Chapin, Mike ; Chen, Jefferey ; Dee, Nick ; Desta, Tsega ; Dolbeare, Tim A. ; Dotson, Nadia ; Ebbert, Amanda ; Fulfs, Erich ; Gee, Garrett ; Gilbert, Terri L. ; Goldy, Jeff ; Gourley, Lindsey ; Gregor, Ben ; Gu, Guangyu ; Hall, Jon ; Haradon, Zeb ; Haynor, David R. ; Hejazinia, Nika ; Hoerder-Suabedissen, Anna ; Howard, Robert ; Jochim, Jay ; Kinnunen, Marty ; Kriedberg, Ali ; Kuan, Chihchau L. ; Lau, Christopher ; Lee, Chang Kyu ; Lee, Felix ; Luong, Lon ; Mastan, Naveed ; May, Ryan ; Melchor, Jose ; Mosqueda, Nerick ; Mott, Erika ; Ngo, Kiet ; Nyhus, Julie ; Oldre, Aaron ; Olson, Eric ; Parente, Jody ; Parker, Patrick D. ; Parry, Sheana ; Pendergraft, Julie ; Potekhina, Lydia ; Reding, Melissa ; Riley, Zackery L. ; Roberts, Tyson ; Rogers, Brandon ; Roll, Kate ; Rosen, David ; Sandman, David ; Sarreal, Melaine ; Shapovalova, Nadiya ; Shi, Shu ; Sjoquist, Nathan ; Sodt, Andy J. ; Townsend, Robbie ; Velasquez, Lissette ; Wagley, Udi ; Wakeman, Wayne B. ; White, Cassandra ; Bennett, Crissa ; Wu, Jennifer ; Young, Rob ; Youngstrom, Brian L. ; Wohnoutka, Paul ; Gibbs, Richard A. ; Rogers, Jeffrey ; Hohmann, John G. ; Hawrylycz, Michael J. ; Hevner, Robert F. ; Molnár, Zoltán ; Phillips, John W. ; Dang, Chinh ; Jones, Allan R. ; Amaral, David G ; Bernard, Amy ; Lein, Ed S. / A comprehensive transcriptional map of primate brain development. In: Nature. 2016 ; Vol. 535, No. 7612. pp. 367-375.
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AU - Miller, Jeremy A.

AU - Ding, Song Lin

AU - Sunkin, Susan M.

AU - Smith, Kimberly A.

AU - Ng, Lydia

AU - Szafer, Aaron

AU - Dalley, Rachel A.

AU - Royall, Joshua J.

AU - Lemon, Tracy

AU - Shapouri, Sheila

AU - Aiona, Kaylynn

AU - Arnold, James

AU - Bennett, Jeffrey L.

AU - Bertagnolli, Darren

AU - Bickley, Kristopher

AU - Boe, Andrew

AU - Brouner, Krissy

AU - Butler, Stephanie

AU - Byrnes, Emi

AU - Caldejon, Shiella

AU - Carey, Anita

AU - Cate, Shelby

AU - Chapin, Mike

AU - Chen, Jefferey

AU - Dee, Nick

AU - Desta, Tsega

AU - Dolbeare, Tim A.

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AU - Ebbert, Amanda

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AU - Gilbert, Terri L.

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AU - Hoerder-Suabedissen, Anna

AU - Howard, Robert

AU - Jochim, Jay

AU - Kinnunen, Marty

AU - Kriedberg, Ali

AU - Kuan, Chihchau L.

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AU - Lee, Chang Kyu

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AU - Riley, Zackery L.

AU - Roberts, Tyson

AU - Rogers, Brandon

AU - Roll, Kate

AU - Rosen, David

AU - Sandman, David

AU - Sarreal, Melaine

AU - Shapovalova, Nadiya

AU - Shi, Shu

AU - Sjoquist, Nathan

AU - Sodt, Andy J.

AU - Townsend, Robbie

AU - Velasquez, Lissette

AU - Wagley, Udi

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AU - White, Cassandra

AU - Bennett, Crissa

AU - Wu, Jennifer

AU - Young, Rob

AU - Youngstrom, Brian L.

AU - Wohnoutka, Paul

AU - Gibbs, Richard A.

AU - Rogers, Jeffrey

AU - Hohmann, John G.

AU - Hawrylycz, Michael J.

AU - Hevner, Robert F.

AU - Molnár, Zoltán

AU - Phillips, John W.

AU - Dang, Chinh

AU - Jones, Allan R.

AU - Amaral, David G

AU - Bernard, Amy

AU - Lein, Ed S.

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