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Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys

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  • Tingting Bo

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Jie Li

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Ganlu Hu

    (ShanghaiTech University)

  • Ge Zhang

    (Henan Provincial People’s Hospital & the People’s Hospital of Zhengzhou University)

  • Wei Wang

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Qian Lv

    (Peking University)

  • Shaoling Zhao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Junjie Ma

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Meng Qin

    (Beijing University of Chemical Technology)

  • Xiaohui Yao

    (Harbin Engineering University
    Harbin Engineering University)

  • Meiyun Wang

    (Henan Provincial People’s Hospital & the People’s Hospital of Zhengzhou University)

  • Guang-Zhong Wang

    (University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Zheng Wang

    (Peking University
    Hainan University)

Abstract

Integrative analyses of transcriptomic and neuroimaging data have generated a wealth of information about biological pathways underlying regional variability in imaging-derived brain phenotypes in humans, but rarely in nonhuman primates due to the lack of a comprehensive anatomically-defined atlas of brain transcriptomics. Here we generate complementary bulk RNA-sequencing dataset of 819 samples from 110 brain regions and single-nucleus RNA-sequencing dataset, and neuroimaging data from 162 cynomolgus macaques, to examine the link between brain-wide gene expression and regional variation in morphometry. We not only observe global/regional expression profiles of macaque brain comparable to human but unravel a dorsolateral-ventromedial gradient of gene assemblies within the primate frontal lobe. Furthermore, we identify a set of 971 protein-coding and 34 non-coding genes consistently associated with cortical thickness, specially enriched for neurons and oligodendrocytes. These data provide a unique resource to investigate nonhuman primate models of human diseases and probe cross-species evolutionary mechanisms.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37246-w
    DOI: 10.1038/s41467-023-37246-w
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    as
    1. Michael J. Hawrylycz & Ed S. Lein & Angela L. Guillozet-Bongaarts & Elaine H. Shen & Lydia Ng & Jeremy A. Miller & Louie N. van de Lagemaat & Kimberly A. Smith & Amanda Ebbert & Zackery L. Riley & Chr, 2012. "An anatomically comprehensive atlas of the adult human brain transcriptome," Nature, Nature, vol. 489(7416), pages 391-399, September.
    2. Rebecca D. Hodge & Trygve E. Bakken & Jeremy A. Miller & Kimberly A. Smith & Eliza R. Barkan & Lucas T. Graybuck & Jennie L. Close & Brian Long & Nelson Johansen & Osnat Penn & Zizhen Yao & Jeroen Egg, 2019. "Conserved cell types with divergent features in human versus mouse cortex," Nature, Nature, vol. 573(7772), pages 61-68, September.
    3. Zhang Bin & Horvath Steve, 2005. "A General Framework for Weighted Gene Co-Expression Network Analysis," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 4(1), pages 1-45, August.
    4. 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.
    5. Trygve E. Bakken & Nikolas L. Jorstad & Qiwen Hu & Blue B. Lake & Wei Tian & Brian E. Kalmbach & Megan Crow & Rebecca D. Hodge & Fenna M. Krienen & Staci A. Sorensen & Jeroen Eggermont & Zizhen Yao & , 2021. "Comparative cellular analysis of motor cortex in human, marmoset and mouse," Nature, Nature, vol. 598(7879), pages 111-119, October.
    6. Ed S. Lein & Michael J. Hawrylycz & Nancy Ao & Mikael Ayres & Amy Bensinger & Amy Bernard & Andrew F. Boe & Mark S. Boguski & Kevin S. Brockway & Emi J. Byrnes & Lin Chen & Li Chen & Tsuey-Ming Chen &, 2007. "Genome-wide atlas of gene expression in the adult mouse brain," Nature, Nature, vol. 445(7124), pages 168-176, January.
    7. Suijuan Zhong & Shu Zhang & Xiaoying Fan & Qian Wu & Liying Yan & Ji Dong & Haofeng Zhang & Long Li & Le Sun & Na Pan & Xiaohui Xu & Fuchou Tang & Jun Zhang & Jie Qiao & Xiaoqun Wang, 2018. "A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex," Nature, Nature, vol. 555(7697), pages 524-528, March.
    8. Zhen Liu & Xiao Li & Jun-Tao Zhang & Yi-Jun Cai & Tian-Lin Cheng & Cheng Cheng & Yan Wang & Chen-Chen Zhang & Yan-Hong Nie & Zhi-Fang Chen & Wen-Jie Bian & Ling Zhang & Jianqiu Xiao & Bin Lu & Yue-Fan, 2016. "Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2," Nature, Nature, vol. 530(7588), pages 98-102, February.
    9. Lloyd T. Elliott & Kevin Sharp & Fidel Alfaro-Almagro & Sinan Shi & Karla L. Miller & Gwenaëlle Douaud & Jonathan Marchini & Stephen M. Smith, 2018. "Genome-wide association studies of brain imaging phenotypes in UK Biobank," Nature, Nature, vol. 562(7726), pages 210-216, October.
    10. Jeremy A. Miller & Song-Lin Ding & Susan M. Sunkin & Kimberly A. Smith & Lydia Ng & Aaron Szafer & Amanda Ebbert & Zackery L. Riley & Joshua J. Royall & Kaylynn Aiona & James M. Arnold & Crissa Bennet, 2014. "Transcriptional landscape of the prenatal human brain," Nature, Nature, vol. 508(7495), pages 199-206, April.
    11. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    12. Céline Amiez & Jérôme Sallet & William D. Hopkins & Adrien Meguerditchian & Fadila Hadj-Bouziane & Suliann Hamed & Charles R. E. Wilson & Emmanuel Procyk & Michael Petrides, 2019. "Sulcal organization in the medial frontal cortex provides insights into primate brain evolution," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    13. Hyo Jung Kang & Yuka Imamura Kawasawa & Feng Cheng & Ying Zhu & Xuming Xu & Mingfeng Li & André M. M. Sousa & Mihovil Pletikos & Kyle A. Meyer & Goran Sedmak & Tobias Guennel & Yurae Shin & Matthew B., 2011. "Spatio-temporal transcriptome of the human brain," Nature, Nature, vol. 478(7370), pages 483-489, October.
    14. Langfelder, Peter & Horvath, Steve, 2012. "Fast R Functions for Robust Correlations and Hierarchical Clustering," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 46(i11).
    15. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    16. 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.
    17. Lei Han & Xiaoyu Wei & Chuanyu Liu & Giacomo Volpe & Zhenkun Zhuang & Xuanxuan Zou & Zhifeng Wang & Taotao Pan & Yue Yuan & Xiao Zhang & Peng Fan & Pengcheng Guo & Yiwei Lai & Ying Lei & Xingyuan Liu , 2022. "Cell transcriptomic atlas of the non-human primate Macaca fascicularis," Nature, Nature, vol. 604(7907), pages 723-731, April.
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