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A comprehensive transcriptional map of primate brain development

Author

Listed:
  • Trygve E. Bakken

    (Allen Institute for Brain Science)

  • Jeremy A. Miller

    (Allen Institute for Brain Science)

  • Song-Lin Ding

    (Allen Institute for Brain Science)

  • Susan M. Sunkin

    (Allen Institute for Brain Science)

  • Kimberly A. Smith

    (Allen Institute for Brain Science)

  • Lydia Ng

    (Allen Institute for Brain Science)

  • Aaron Szafer

    (Allen Institute for Brain Science)

  • Rachel A. Dalley

    (Allen Institute for Brain Science)

  • Joshua J. Royall

    (Allen Institute for Brain Science)

  • Tracy Lemon

    (Allen Institute for Brain Science)

  • Sheila Shapouri

    (Allen Institute for Brain Science)

  • Kaylynn Aiona

    (Allen Institute for Brain Science)

  • James Arnold

    (Allen Institute for Brain Science)

  • Jeffrey L. Bennett

    (California National Primate Research Center, The M.I.N.D. Institute, University of California, Davis)

  • Darren Bertagnolli

    (Allen Institute for Brain Science)

  • Kristopher Bickley

    (Allen Institute for Brain Science)

  • Andrew Boe

    (Allen Institute for Brain Science)

  • Krissy Brouner

    (Allen Institute for Brain Science)

  • Stephanie Butler

    (Allen Institute for Brain Science)

  • Emi Byrnes

    (Allen Institute for Brain Science)

  • Shiella Caldejon

    (Allen Institute for Brain Science)

  • Anita Carey

    (Allen Institute for Brain Science)

  • Shelby Cate

    (Allen Institute for Brain Science)

  • Mike Chapin

    (Allen Institute for Brain Science)

  • Jefferey Chen

    (Allen Institute for Brain Science)

  • Nick Dee

    (Allen Institute for Brain Science)

  • Tsega Desta

    (Allen Institute for Brain Science)

  • Tim A. Dolbeare

    (Allen Institute for Brain Science)

  • Nadia Dotson

    (Allen Institute for Brain Science)

  • Amanda Ebbert

    (Allen Institute for Brain Science)

  • Erich Fulfs

    (Allen Institute for Brain Science)

  • Garrett Gee

    (Allen Institute for Brain Science)

  • Terri L. Gilbert

    (Allen Institute for Brain Science)

  • Jeff Goldy

    (Allen Institute for Brain Science)

  • Lindsey Gourley

    (Allen Institute for Brain Science)

  • Ben Gregor

    (Allen Institute for Brain Science)

  • Guangyu Gu

    (Allen Institute for Brain Science)

  • Jon Hall

    (Allen Institute for Brain Science)

  • Zeb Haradon

    (Allen Institute for Brain Science)

  • David R. Haynor

    (University of Washington, Seattle)

  • Nika Hejazinia

    (Allen Institute for Brain Science)

  • Anna Hoerder-Suabedissen

    (Anatomy and Genetics, University of Oxford)

  • Robert Howard

    (Allen Institute for Brain Science)

  • Jay Jochim

    (Allen Institute for Brain Science)

  • Marty Kinnunen

    (Allen Institute for Brain Science)

  • Ali Kriedberg

    (Allen Institute for Brain Science)

  • Chihchau L. Kuan

    (Allen Institute for Brain Science)

  • Christopher Lau

    (Allen Institute for Brain Science)

  • Chang-Kyu Lee

    (Allen Institute for Brain Science)

  • Felix Lee

    (Allen Institute for Brain Science)

  • Lon Luong

    (Allen Institute for Brain Science)

  • Naveed Mastan

    (Allen Institute for Brain Science)

  • Ryan May

    (Allen Institute for Brain Science)

  • Jose Melchor

    (Allen Institute for Brain Science)

  • Nerick Mosqueda

    (Allen Institute for Brain Science)

  • Erika Mott

    (Allen Institute for Brain Science)

  • Kiet Ngo

    (Allen Institute for Brain Science)

  • Julie Nyhus

    (Allen Institute for Brain Science)

  • Aaron Oldre

    (Allen Institute for Brain Science)

  • Eric Olson

    (Allen Institute for Brain Science)

  • Jody Parente

    (Allen Institute for Brain Science)

  • Patrick D. Parker

    (Allen Institute for Brain Science)

  • Sheana Parry

    (Allen Institute for Brain Science)

  • Julie Pendergraft

    (Allen Institute for Brain Science)

  • Lydia Potekhina

    (Allen Institute for Brain Science)

  • Melissa Reding

    (Allen Institute for Brain Science)

  • Zackery L. Riley

    (Allen Institute for Brain Science)

  • Tyson Roberts

    (Allen Institute for Brain Science)

  • Brandon Rogers

    (Allen Institute for Brain Science)

  • Kate Roll

    (Allen Institute for Brain Science)

  • David Rosen

    (Allen Institute for Brain Science)

  • David Sandman

    (Allen Institute for Brain Science)

  • Melaine Sarreal

    (Allen Institute for Brain Science)

  • Nadiya Shapovalova

    (Allen Institute for Brain Science)

  • Shu Shi

    (Allen Institute for Brain Science)

  • Nathan Sjoquist

    (Allen Institute for Brain Science)

  • Andy J. Sodt

    (Allen Institute for Brain Science)

  • Robbie Townsend

    (Allen Institute for Brain Science)

  • Lissette Velasquez

    (Allen Institute for Brain Science)

  • Udi Wagley

    (Allen Institute for Brain Science)

  • Wayne B. Wakeman

    (Allen Institute for Brain Science)

  • Cassandra White

    (Allen Institute for Brain Science)

  • Crissa Bennett

    (Allen Institute for Brain Science)

  • Jennifer Wu

    (Allen Institute for Brain Science)

  • Rob Young

    (Allen Institute for Brain Science)

  • Brian L. Youngstrom

    (Allen Institute for Brain Science)

  • Paul Wohnoutka

    (Allen Institute for Brain Science)

  • Richard A. Gibbs

    (Baylor College of Medicine)

  • Jeffrey Rogers

    (Baylor College of Medicine)

  • John G. Hohmann

    (Allen Institute for Brain Science)

  • Michael J. Hawrylycz

    (Allen Institute for Brain Science)

  • Robert F. Hevner

    (Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle)

  • Zoltán Molnár

    (Anatomy and Genetics, University of Oxford)

  • John W. Phillips

    (Allen Institute for Brain Science)

  • Chinh Dang

    (Allen Institute for Brain Science)

  • Allan R. Jones

    (Allen Institute for Brain Science)

  • David G. Amaral

    (California National Primate Research Center, The M.I.N.D. Institute, University of California, Davis)

  • Amy Bernard

    (Allen Institute for Brain Science)

  • Ed S. Lein

    (Allen Institute for Brain Science)

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.

Suggested Citation

  • 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 Aion, 2016. "A comprehensive transcriptional map of primate brain development," Nature, Nature, vol. 535(7612), pages 367-375, July.
  • Handle: RePEc:nat:nature:v:535:y:2016:i:7612:d:10.1038_nature18637
    DOI: 10.1038/nature18637
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    Cited by:

    1. Xuelong Yao & Zongyang Lu & Zhanying Feng & Lei Gao & Xin Zhou & Min Li & Suijuan Zhong & Qian Wu & Zhenbo Liu & Haofeng Zhang & Zeyuan Liu & Lizhi Yi & Tao Zhou & Xudong Zhao & Jun Zhang & Yong Wang , 2022. "Comparison of chromatin accessibility landscapes during early development of prefrontal cortex between rhesus macaque and human," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Jingnan Zhang & Chengye Li & Junhui Wang, 2023. "A stochastic block Ising model for multi‐layer networks with inter‐layer dependence," Biometrics, The International Biometric Society, vol. 79(4), pages 3564-3573, December.
    3. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    4. Jun Ding & Jian Ji & Zachary Rabow & Tong Shen & Jacob Folz & Christopher R. Brydges & Sili Fan & Xinchen Lu & Sajjan Mehta & Megan R. Showalter & Ying Zhang & Renee Araiza & Lynette R. Bower & K. C. , 2021. "A metabolome atlas of the aging mouse brain," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    5. Anna N. Bukiya, 2019. "Fetal Cerebral Artery Mitochondrion as Target of Prenatal Alcohol Exposure," IJERPH, MDPI, vol. 16(9), pages 1-16, May.
    6. Jingkuan Wei & Shaoxing Dai & Yaping Yan & Shulin Li & Pengpeng Yang & Ran Zhu & Tianzhuang Huang & Xi Li & Yanchao Duan & Zhengbo Wang & Weizhi Ji & Wei Si, 2023. "Spatiotemporal proteomic atlas of multiple brain regions across early fetal to neonatal stages in cynomolgus monkey," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Ying Lei & Mengnan Cheng & Zihao Li & Zhenkun Zhuang & Liang Wu & Yunong sun & Lei Han & Zhihao Huang & Yuzhou Wang & Zifei Wang & Liqin Xu & Yue Yuan & Shang Liu & Taotao Pan & Jiarui Xie & Chuanyu L, 2022. "Spatially resolved gene regulatory and disease-related vulnerability map of the adult Macaque cortex," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    9. Samuel S. Kim & Buu Truong & Karthik Jagadeesh & Kushal K. Dey & Amber Z. Shen & Soumya Raychaudhuri & Manolis Kellis & Alkes L. Price, 2024. "Leveraging single-cell ATAC-seq and RNA-seq to identify disease-critical fetal and adult brain cell types," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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