Noncoding transcripts are linked to brain resting-state activity in non-human primates

Wei Wang; Tingting Bo; Ge Zhang; Jie Li; Junjie Ma; Liangxiao Ma; Ganlu Hu; Huige Tong; Qian Lv; Daniel J Araujo; Dong Luo; Yuejun Chen; Meiyun Wang; Zheng Wang; Guang-Zhong Wang

doi:10.1016/j.celrep.2023.112652

Noncoding transcripts are linked to brain resting-state activity in non-human primates

Cell Rep. 2023 Jun 27;42(6):112652. doi: 10.1016/j.celrep.2023.112652. Epub 2023 Jun 18.

Authors

Wei Wang¹, Tingting Bo², Ge Zhang³, Jie Li¹, Junjie Ma¹, Liangxiao Ma¹, Ganlu Hu⁴, Huige Tong¹, Qian Lv⁵, Daniel J Araujo⁶, Dong Luo⁷, Yuejun Chen⁸, Meiyun Wang³, Zheng Wang⁹, Guang-Zhong Wang¹⁰

Affiliations

¹ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
² Department of Endocrine and Metabolic Diseases, Shanghai Institute of Endocrine and Metabolic Diseases, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Clinical Neuroscience Center, Ruijin Hospital Luwan Branch, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
³ Department of Medical Imaging, Henan Provincial People's Hospital & the People's Hospital of Zhengzhou University, No. 7 Weiwu Road, Zhengzhou, Henan, China.
⁴ Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, China.
⁵ School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, IDG/McGovern Institute for Brain Research, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China.
⁶ Center for Cancer Immunotherapy, La Jolla Institute for Immunology, La Jolla, CA, USA.
⁷ School of Biomedical Engineering, Hainan University, Haikou, Hainan, China.
⁸ Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Shanghai 201210, China.
⁹ School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, IDG/McGovern Institute for Brain Research, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China; School of Biomedical Engineering, Hainan University, Haikou, Hainan, China. Electronic address: zheng.wang@pku.edu.cn.
¹⁰ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Electronic address: guangzhong.wang@picb.ac.cn.

PMID: 37335775
DOI: 10.1016/j.celrep.2023.112652

Abstract

Brain-derived transcriptomes are known to correlate with resting-state brain activity in humans. Whether this association holds in nonhuman primates remains uncertain. Here, we search for such molecular correlates by integrating 757 transcriptomes derived from 100 macaque cortical regions with resting-state activity in separate conspecifics. We observe that 150 noncoding genes explain variations in resting-state activity at a comparable level with protein-coding genes. In-depth analysis of these noncoding genes reveals that they are connected to the function of nonneuronal cells such as oligodendrocytes. Co-expression network analysis finds that the modules of noncoding genes are linked to both autism and schizophrenia risk genes. Moreover, genes associated with resting-state noncoding genes are highly enriched in human resting-state functional genes and memory-effect genes, and their links with resting-state functional magnetic resonance imaging (fMRI) signals are altered in the brains of patients with autism. Our results highlight the potential for noncoding RNAs to explain resting-state activity in the nonhuman primate brain.

Keywords: CP: Neuroscience; autism; non-human primate; noncoding RNA; oligodendrocyte; resting-state activity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Autistic Disorder*
Brain / physiology
Brain Mapping / methods
Humans
Magnetic Resonance Imaging* / methods
Nerve Net / physiology
Primates / genetics