IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39411-7.html
   My bibliography  Save this article

Spatiotemporal proteomic atlas of multiple brain regions across early fetal to neonatal stages in cynomolgus monkey

Author

Listed:
  • Jingkuan Wei

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Shaoxing Dai

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Yaping Yan

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Shulin Li

    (Kunming University of Science and Technology)

  • Pengpeng Yang

    (Kunming University of Science and Technology)

  • Ran Zhu

    (Kunming University of Science and Technology)

  • Tianzhuang Huang

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Xi Li

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Yanchao Duan

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Zhengbo Wang

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Weizhi Ji

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research
    Chinese Primate Biomedical Research Alliance (CPBRA))

  • Wei Si

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research
    Chinese Primate Biomedical Research Alliance (CPBRA))

Abstract

Fetal stages are critical periods for brain development. However, the protein molecular signature and dynamics of the human brain remain unclear due to sampling difficulty and ethical limitations. Non-human primates present similar developmental and neuropathological features to humans. This study constructed a spatiotemporal proteomic atlas of cynomolgus macaque brain development from early fetal to neonatal stages. Here we showed that (1) the variability across stages was greater than that among brain regions, and comparisons of cerebellum vs. cerebrum and cortical vs. subcortical regions revealed region-specific dynamics across early fetal to neonatal stages; (2) fluctuations in abundance of proteins associated with neural disease suggest the risk of nervous disorder at early fetal stages; (3) cross-species analysis (human, monkey, and mouse) and comparison between proteomic and transcriptomic data reveal the proteomic specificity and genes with mRNA/protein discrepancy. This study provides insight into fetal brain development in primates.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39411-7
    DOI: 10.1038/s41467-023-39411-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39411-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39411-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Velina Kozareva & Caroline Martin & Tomas Osorno & Stephanie Rudolph & Chong Guo & Charles Vanderburg & Naeem Nadaf & Aviv Regev & Wade G. Regehr & Evan Macosko, 2021. "A transcriptomic atlas of mouse cerebellar cortex comprehensively defines cell types," Nature, Nature, vol. 598(7879), pages 214-219, October.
    2. Senlin Yin & Keying Lu & Tao Tan & Jie Tang & Jingkuan Wei & Xu Liu & Xinlei Hu & Haisu Wan & Wei Huang & Yong Fan & Dan Xie & Yang Yu, 2020. "Transcriptomic and open chromatin atlas of high-resolution anatomical regions in the rhesus macaque brain," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    3. Marianne L. Seney & Kelly Cahill & John F. Enwright & Ryan W. Logan & Zhiguang Huo & Wei Zong & George Tseng & Colleen A. McClung, 2019. "Diurnal rhythms in gene expression in the prefrontal cortex in schizophrenia," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. 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.
    5. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. Jackson N. Cagle & Tiberio de Araujo & Kara A. Johnson & John Yu & Lauren Fanty & Filipe P. Sarmento & Simon Little & Michael S. Okun & Joshua K. Wong & Coralie de Hemptinne, 2024. "Chronic intracranial recordings in the globus pallidus reveal circadian rhythms in Parkinson’s disease," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    8. Leon D. Lotter & Amin Saberi & Justine Y. Hansen & Bratislav Misic & Casey Paquola & Gareth J. Barker & Arun L. W. Bokde & Sylvane Desrivières & Herta Flor & Antoine Grigis & Hugh Garavan & Penny Gowl, 2024. "Regional patterns of human cortex development correlate with underlying neurobiology," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    9. Jin Woo Oh & Michael A. Beer, 2024. "Gapped-kmer sequence modeling robustly identifies regulatory vocabularies and distal enhancers conserved between evolutionarily distant mammals," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Anna Pagliaro & Roxy Finger & Iris Zoutendijk & Saskia Bunschuh & Hans Clevers & Delilah Hendriks & Benedetta Artegiani, 2023. "Temporal morphogen gradient-driven neural induction shapes single expanded neuroepithelium brain organoids with enhanced cortical identity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Eva-Maria Stauffer & Richard A. I. Bethlehem & Lena Dorfschmidt & Hyejung Won & Varun Warrier & Edward T. Bullmore, 2023. "The genetic relationships between brain structure and schizophrenia," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Xiaomeng Wan & Jiashun Xiao & Sindy Sing Ting Tam & Mingxuan Cai & Ryohichi Sugimura & Yang Wang & Xiang Wan & Zhixiang Lin & Angela Ruohao Wu & Can Yang, 2023. "Integrating spatial and single-cell transcriptomics data using deep generative models with SpatialScope," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Sheng Wang & Belinda Wang & Vanessa Drury & Sam Drake & Nawei Sun & Hasan Alkhairo & Juan Arbelaez & Clif Duhn & Vanessa H. Bal & Kate Langley & Joanna Martin & Pieter J. Hoekstra & Andrea Dietrich & , 2023. "Rare X-linked variants carry predominantly male risk in autism, Tourette syndrome, and ADHD," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Tianqi Liu & Ming Yuan & Hongyu Zhao, 2022. "Characterizing Spatiotemporal Transcriptome of the Human Brain Via Low-Rank Tensor Decomposition," Statistics in Biosciences, Springer;International Chinese Statistical Association, vol. 14(3), pages 485-513, December.
    15. Hyosang Kim & Doyoun Kim & Yisul Cho & Kyungdeok Kim & Junyeop Daniel Roh & Yangsik Kim & Esther Yang & Seong Soon Kim & Sunjoo Ahn & Hyun Kim & Hyojin Kang & Yongchul Bae & Eunjoon Kim, 2022. "Early postnatal serotonin modulation prevents adult-stage deficits in Arid1b-deficient mice through synaptic transcriptional reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Elaine T. Lim & Yingleong Chan & Pepper Dawes & Xiaoge Guo & Serkan Erdin & Derek J. C. Tai & Songlei Liu & Julia M. Reichert & Mannix J. Burns & Ying Kai Chan & Jessica J. Chiang & Katharina Meyer & , 2022. "Orgo-Seq integrates single-cell and bulk transcriptomic data to identify cell type specific-driver genes associated with autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Md Tauhidul Islam & Lei Xing, 2023. "Cartography of Genomic Interactions Enables Deep Analysis of Single-Cell Expression Data," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Xinyuan Liang & Lianglong Sun & Xuhong Liao & Tianyuan Lei & Mingrui Xia & Dingna Duan & Zilong Zeng & Qiongling Li & Zhilei Xu & Weiwei Men & Yanpei Wang & Shuping Tan & Jia-Hong Gao & Shaozheng Qin , 2024. "Structural connectome architecture shapes the maturation of cortical morphology from childhood to adolescence," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. Marc P. Forrest & Marc Dos Santos & Nicolas H. Piguel & Yi-Zhi Wang & Nicole A. Hawkins & Vikram A. Bagchi & Leonardo E. Dionisio & Sehyoun Yoon & Dina Simkin & Maria Dolores Martin-de-Saavedra & Ruoq, 2023. "Rescue of neuropsychiatric phenotypes in a mouse model of 16p11.2 duplication syndrome by genetic correction of an epilepsy network hub," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    20. Norman L. Lehman & Nathalie Spassky & Müge Sak & Amy Webb & Cory T. Zumbar & Aisulu Usubalieva & Khaled J. Alkhateeb & Joseph P. McElroy & Kirsteen H. Maclean & Paolo Fadda & Tom Liu & Vineela Gangala, 2022. "Astroblastomas exhibit radial glia stem cell lineages and differential expression of imprinted and X-inactivation escape genes," Nature Communications, Nature, vol. 13(1), pages 1-20, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39411-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.