Transcriptomic and Open Chromatin Atlas of High-resolution Anatomical Regions in the Rhesus Macaque Brain

Overview

Journal Nat Commun

Specialty Biology

Date 2020 Jan 26

PMID 31980617

Citations 24

Authors

Senlin Yin

Keying Lu

Tao Tan

Jie Tang

Jingkuan Wei

Xu Liu

Xinlei Hu

Haisu Wan

Wei Huang

Yong Fan

Dan Xie

Yang Yu

Affiliations

Soon will be listed here.

Abstract

The rhesus macaque is a prime model animal in neuroscience. A comprehensive transcriptomic and open chromatin atlas of the rhesus macaque brain is key to a deeper understanding of the brain. Here we characterize the transcriptome of 416 brain samples from 52 regions of 8 rhesus macaque brains. We identify gene modules associated with specific brain regions like the cerebral cortex, pituitary, and thalamus. In addition, we discover 9703 novel intergenic transcripts, including 1701 coding transcripts and 2845 lncRNAs. Most of the novel transcripts are only expressed in specific brain regions or cortical regions of specific individuals. We further survey the open chromatin regions in the hippocampal CA1 and several cerebral cortical regions of the rhesus macaque brain using ATAC-seq, revealing CA1- and cortex-specific open chromatin regions. Our results add to the growing body of knowledge regarding the baseline transcriptomic and open chromatin profiles in the brain of the rhesus macaque.

Citing Articles

Single-nucleus multi-omics analyses reveal cellular and molecular innovations in the anterior cingulate cortex during primate evolution.

Yuan J, Dong K, Wu H, Zeng X, Liu X, Liu Y Cell Genom. 2024; 4(12):100703.

PMID: 39631404 PMC: 11701334. DOI: 10.1016/j.xgen.2024.100703.

Human-specific protein-coding and lncRNA genes cast sex-biased genes in the brain and their relationships with brain diseases.

He S, Zhang X, Zhu H Biol Sex Differ. 2024; 15(1):86.

PMID: 39472939 PMC: 11520681. DOI: 10.1186/s13293-024-00659-3.

Evolutionary and biomedical implications of sex differences in the primate brain transcriptome.

DeCasien A, Chiou K, Testard C, Mercer A, Negron-Del Valle J, Bauman Surratt S Cell Genom. 2024; 4(7):100589.

PMID: 38942023 PMC: 11293591. DOI: 10.1016/j.xgen.2024.100589.

Reciprocal negative feedback between Prrx1 and miR-140-3p regulates rapid chondrogenesis in the regenerating antler.

Hu P, Zhang G, Ba H, Ren J, Li J, Wang Z Cell Mol Biol Lett. 2024; 29(1):56.

PMID: 38643083 PMC: 11031908. DOI: 10.1186/s11658-024-00573-x.

Chromatin accessibility profiling methods.

Minnoye L, Marinov G, Krausgruber T, Pan L, Marand A, Secchia S Nat Rev Methods Primers. 2024; 1.

PMID: 38410680 PMC: 10895463. DOI: 10.1038/s43586-020-00008-9.

References

Hawrylycz M, Lein E, Guillozet-Bongaarts A, Shen E, Ng L, Miller J . An anatomically comprehensive atlas of the adult human brain transcriptome. Nature. 2012; 489(7416):391-399. PMC: 4243026. DOI: 10.1038/nature11405. View

Miller J, Ding S, Sunkin S, Smith K, Ng L, Szafer A . Transcriptional landscape of the prenatal human brain. Nature. 2014; 508(7495):199-206. PMC: 4105188. DOI: 10.1038/nature13185. View

Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R, Grenyer R . The delayed rise of present-day mammals. Nature. 2007; 446(7135):507-12. DOI: 10.1038/nature05634. View

Jennings C, Landman R, Zhou Y, Sharma J, Hyman J, Movshon J . Opportunities and challenges in modeling human brain disorders in transgenic primates. Nat Neurosci. 2016; 19(9):1123-30. DOI: 10.1038/nn.4362. View

Passingham R . How good is the macaque monkey model of the human brain?. Curr Opin Neurobiol. 2009; 19(1):6-11. PMC: 2706975. DOI: 10.1016/j.conb.2009.01.002. View

Bakken T, Miller J, Ding S, Sunkin S, Smith K, Ng L . A comprehensive transcriptional map of primate brain development. Nature. 2016; 535(7612):367-75. PMC: 5325728. DOI: 10.1038/nature18637. View

Kojima T, Higo N, Sato A, Oishi T, Nishimura Y, Yamamoto T . Functional annotation of genes differentially expressed between primary motor and prefrontal association cortices of macaque brain. Neurochem Res. 2012; 38(1):133-40. DOI: 10.1007/s11064-012-0900-4. View

Liu S, Wang Z, Chen D, Zhang B, Tian R, Wu J . Annotation and cluster analysis of spatiotemporal- and sex-related lncRNA expression in rhesus macaque brain. Genome Res. 2017; 27(9):1608-1620. PMC: 5580719. DOI: 10.1101/gr.217463.116. View

Zimin A, Cornish A, Maudhoo M, Gibbs R, Zhang X, Pandey S . A new rhesus macaque assembly and annotation for next-generation sequencing analyses. Biol Direct. 2014; 9(1):20. PMC: 4214606. DOI: 10.1186/1745-6150-9-20. View

10.

Zhu Y, Sousa A, Gao T, Skarica M, Li M, Santpere G . Spatiotemporal transcriptomic divergence across human and macaque brain development. Science. 2018; 362(6420). PMC: 6900982. DOI: 10.1126/science.aat8077. View

11.

Fullard J, Hauberg M, Bendl J, Egervari G, Cirnaru M, Reach S . An atlas of chromatin accessibility in the adult human brain. Genome Res. 2018; 28(8):1243-1252. PMC: 6071637. DOI: 10.1101/gr.232488.117. View

12.

Su Y, Shin J, Zhong C, Wang S, Roychowdhury P, Lim J . Neuronal activity modifies the chromatin accessibility landscape in the adult brain. Nat Neurosci. 2017; 20(3):476-483. PMC: 5325677. DOI: 10.1038/nn.4494. View

13.

Newman A, Liu C, Green M, Gentles A, Feng W, Xu Y . Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015; 12(5):453-7. PMC: 4739640. DOI: 10.1038/nmeth.3337. View

14.

Valerio-Gomes B, Guimaraes D, Szczupak D, Lent R . The Absolute Number of Oligodendrocytes in the Adult Mouse Brain. Front Neuroanat. 2018; 12:90. PMC: 6218541. DOI: 10.3389/fnana.2018.00090. View

15.

Baek S, Choi H, Kim J . Ebf3-miR218 regulation is involved in the development of dopaminergic neurons. Brain Res. 2014; 1587:23-32. DOI: 10.1016/j.brainres.2014.08.059. View

16.

Schliebs R, Arendt T . The cholinergic system in aging and neuronal degeneration. Behav Brain Res. 2010; 221(2):555-63. DOI: 10.1016/j.bbr.2010.11.058. View

17.

Xu C, Li Q, Efimova O, He L, Tatsumoto S, Stepanova V . Human-specific features of spatial gene expression and regulation in eight brain regions. Genome Res. 2018; 28(8):1097-1110. PMC: 6071643. DOI: 10.1101/gr.231357.117. View

18.

Jiang X, Zhang M, You Y, Liu F . The production of somatostatin interneurons in the olfactory bulb is regulated by the transcription factor sp8. PLoS One. 2013; 8(7):e70049. PMC: 3720950. DOI: 10.1371/journal.pone.0070049. View

19.

Guaza C, Borrell J . The Met-enkephalin analog D-Ala2-Met-enkephalinamide decreases the adrenocortical response to ACTH in dispersed rat adrenal cells. Peptides. 1984; 5(5):895-7. DOI: 10.1016/0196-9781(84)90113-x. View

20.

Faedo A, Ficara F, Ghiani M, Aiuti A, Rubenstein J, Bulfone A . Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis. Mech Dev. 2002; 116(1-2):157-60. DOI: 10.1016/s0925-4773(02)00114-4. View