Annotation and cluster analysis of spatiotemporal- and sex-related lncRNA expression in rhesus macaque brain
Open accessAbstract
Long noncoding RNAs (lncRNAs) mediate important epigenetic regulation in a wide range of biological processes and diseases. We applied comprehensive analyses of RNA-seq and CAGE-seq (cap analysis of gene expression and sequencing) to characterize the dynamic changes in lncRNA expression in rhesus macaque (Macaca mulatta) brain in four representative age groups. We identified 18 anatomically diverse lncRNA modules and 14 mRNA modules representing spatial, age, and sex specificities. Spatiotemporal- and sex-biased changes in lncRNA expression were generally higher than those observed in mRNA expression. A negative correlation between lncRNA and mRNA expression in cerebral cortex was observed and functionally validated. Our findings offer a fresh insight into spatial-, age-, and sex-biased changes in lncRNA expression in macaque brain and suggest that the changes represent a previously unappreciated regulatory system that potentially contributes to brain development and aging.
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lncMtDloop (AC027613.1) is a non-coding RNA encoded within the D-loop region of the mitochondrial genome.
“lncMtDloop, a non-coding RNA of unknown function encoded within the D-loop region of the mitochondrial genome”
From The mitochondrial long non-coding RNA lncMtloop regulates mitochondrial transcription and suppresses Alzheimer’s disease (2024) · cites this paper as Liu et al, 2017
The Abstract defines lncRNAs generally, and the Results discuss lncRNA expression in rhesus macaque brain, but neither identifies lncMtDloop (AC027613.1) or places it in the mitochondrial D-loop. Searches for the RNA’s name and for the D-loop region found no passage addressing that specific claim. (LLM, conf=0.76)
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BackgroundEvolutionary and biomedical implications of sex differences in the primate brain transcriptome
DeCasien, A. R., Chiou, K. L., Testard, C., Mercer, A., Valle, J. E. N.-D., Bauman, S. E., González, O., Stock, M. K., Ruiz-Lambides, A. V., Martínez, M. I., et al. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100589 · Cited by 16 · see citing works
Jin, Y., Zhang, B., Lu, J., Song, Y., Wang, W., Zhang, W., Shao, F., Gong, M., Wang, M., Liang, X., et al. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001297 · Cited by 17 · see citing works
“Interestingly, we found that the number of cerebellar-expressing lncRNAs are relatively higher and that their profiling is quite unique compared with the other tested brain areas [16,17], raising a possibility that these cerebellum highly expressed lncRNAs may be essential regulators of cerebellar function.”
BackgroundSelf-citationCheng, Y.-W., Xu, L.-J., Wang, J.-Y., Cao, X., Chen, D., Zhang, P., Yang, L., & Qin, L.-J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1026086 · Cited by 12
“To systematically analyze the lncRNA expression pattern, we used a pipeline for lncRNAs identification similar as previously reported (29), which was constructed based on the StringTie software (30).”
MethodSelf-citationWang, J., Yang, Q., Hu, Y., Xu, W., Yang, Y., Chen, S., & Wang, N. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.795525 · Cited by 11 · see citing works
Identification of drought-related co-expression modules and hub genes in potato roots based on WGCNA
Qin, T., Sun, C., Bi, Z., Liang, W., Li, P., Zhang, J., & Bai, J. (2020) · ACTA AGRONOMICA SINICA · doi:10.3724/sp.j.1006.2020.94130 · Cited by 13 · see citing works
“外界胁迫(生物胁迫和非生物胁迫)是农业生产 面临的主要问题之一, 了解胁迫对植物的影响以及 植物对胁迫信号的感知、传递和应答对解决和提高 作物产量具有重要的意义。马铃薯作为四大粮食作 物之一 , 在中国主要种植于年平均降水量小于 500 mm 的干旱和半干旱地区 , 长期的或季节性的 干旱胁迫会严重影响马铃薯的植株长势、块茎产量 和商品性 ([1-2])。马铃薯属浅根系作物 , 对干旱胁迫较 为敏感 , 因此抗旱性研究一直是马铃薯产业关注的 问题。研究人员从增大根系、减少蒸腾和提高水肥 利用率以提高马铃薯耐旱性开展了大量研究 , 也对 马铃薯的根系表型和抗逆相关生理生化指标对干 旱胁迫的响应情况进行了多种分析 , 但针对马铃薯 抗…”
Sui, B.-K., Chen, D., Liu, W., Tian, B., Lv, L., Pei, J., Wu, Q., Zhou, M., Fu, Z. F., Zhang, Y., et al. (2020) · Journal of General Virology · doi:10.1099/jgv.0.001538 · Cited by 11 · see citing works
Self-citationTranscriptomic study reveals changes of lncRNAs in PBMCs from HIV-1 patients before and after ART
Zhou, Y., Huang, Y., Chen, X.-P., Chen, T.-L., Hu, W.-J., Hou, W., Zhang, Q., & Xiong, Y. (2023) · Scientific Reports · doi:10.1038/s41598-023-49595-z · Cited by 10 · see citing works
“To systematically analyze the lncRNA expression pattern, we used a pipeline for lncRNA identification similar to that previously reported 39 , which was constructed based on cufflinks software 40 .”
MethodEpigenetic effects of silver nanoparticles and ionic silver in Tetrahymena thermophila.
Pan, Y.-B., Lin, S.-J., & Zhang, W.-J. (2021) · Science of the Total Environment · doi:10.1016/j.scitotenv.2020.144659 · Cited by 10
Bo, D.-D., Jiang, X.-P., Liu, G., Hu, R.-X., & Chong, Y.-Q. (2021) · Animals · doi:10.3390/ani11030625 · Cited by 10 · see citing works
“LincRNA tends to express in a temporal-specific manner [54].”
BackgroundResultChen, Y., Chen, D., Wang, J., Zhang, Y., Zhang, J., Chen, B., Chen, Y.-R., Zhang, Y., & Ma, C. (2021) · Technology in Cancer Research and Treatment · doi:10.1177/1533033821989711 · Cited by 10
“The following processes used to identify lncRNAs were as described by Liu et al.(44) Expression and DElncR analyses of lncRNAs were as described for DEGs.”
BackgroundMethodInfluentialSelf-citationShi, G.-L., Chen, L., Chen, G.-T., Zou, C., Li, J., Li, M., Fang, C.-C., & Li, C.-C. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00160 · Cited by 10
“Characterization of LincRNAs Previous studies found many differences between lincRNAs and protein-coding transcripts (Derrien et al., 2012; Liu et al., 2017).”
BackgroundSelf-citationNoncoding transcripts are linked to brain resting-state activity in non-human primates
Wang, W., Bo, T., Zhang, G., Li, J., Ma, J., Ma, L., Hu, G., Tong, H., Lv, Q., Araujo, D. J., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112652 · Cited by 11 · see citing works
Self-citationYang, N., Yang, J., He, X., Zhang, W., & Xing, Y. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2021.108915 · Cited by 9 · see citing works
Wang, J., Wu, X., Tu, Y., Dang, J.-Z., Cai, Z., Liao, W., Quan, W., & Wei, Y. (2021) · PeerJ · doi:10.7717/peerj.10668 · Cited by 9
“According to a previous study (Liu et al., 2017), we constructed a coexpression network between lncRNAs and mRNAs.”
BackgroundMethodInfluentialLong non-coding RNAs expression and regulation across different brain regions in primates
Navandar, M., Vennin, C., Lutz, B., & Gerber, S. (2024) · Scientific Data · doi:10.1038/s41597-024-03380-3 · Cited by 13 · see citing works
Long non-coding RNAs with essential roles in neurodegenerative disorders
Xiong, W., Lu, L., & Li, J.-L. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.385850 · Cited by 8 · see citing works
“This type of regulation can fine-tune gene expression and has been implicated in various biological processes, including cancer progression and immune response (Liu et al., 2017a; Zhang et al., 2020b, 2022; Hu et al., 2023).”
BackgroundSelf-citationCheng, Y.-W., Cao, X., Zhang, J.-G., Chen, D., Zhu, J., Xu, L.-J., & Qin, L.-J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.678256 · Cited by 8 · see citing works
Self-citationZhao, X., Zhao, F., Long, Y., Wu, J., Fang, Y., Wang, C., Xin, Z., & Yang, X. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-024-01510-4 · Cited by 6 · see citing works
“Referring to previous studies [33, 34], a pipeline for lncRNA identification was used to systematically analyze the dynamic expression patterns of lncRNAs.”
MethodSelf-citationLiu, Y., Yu, Y., Ao, H., Zhang, F., Zhao, X.-T., Liu, H.-T., Shi, Y., Xing, K., & Wang, C.-D. (2021) · Genes · doi:10.3390/genes12091374 · Cited by 7 · see citing works
“Studies have shown that the expression level of lncRNAs is usually lower than that of protein-coding genes [40], we found that the expression of lncRNA was much lower than that of the gene.”
BackgroundMidic, U., Vandevoort, C., & Latham, K. (2018) · Physiological Genomics · doi:10.1152/physiolgenomics.00001.2018 · Cited by 7
“Two series of libraries in Gene Expression Omnibus (GEO) were selected for the analysis and validation phase of the study for rhesus monkey samples (GSE85377 (9) and GSE96731 (7)).”
MethodWang, B.-B., Liu, X.-L., Li, C., & Yang, N. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.135131 · Cited by 6
Analysis of the aging-related biomarker in a nonhuman primate model using multilayer omics
Liu, Y., Lu, S., Yang, J., Yang, Y., Li, J., Hu, J., Li, Y., Yang, F., Pang, Y., Zhao, Y., et al. (2024) · BMC Genomics · doi:10.1186/s12864-024-10556-z · Cited by 7 · see citing works
“The average age of rhesus monkeys is approximately 20 years old, at the same time, we referred to the grouping situation of the age of rhesus monkeys in the article published by Liu et al. [26] and two reports about rhesus monkeys [80, 81].”
BackgroundMethodSikka, P., Singh, K. P., Singh, I., Mishra, D., Paul, S., Balhara, A., Andonissamy, J., Chaturvedi, K., Rao, A., & Rai, A. (2023) · Frontiers in Animal Science · doi:10.3389/fanim.2023.1135429 · Cited by 6 · see citing works
Identification of a hippocampal lncRNA-regulating network in a natural aging rat model
Qi, L., Li, X., Liu, S.-M., Jiao, D.-L., Hu, D., Ju, X.-Y., Zhao, S., Si, S.-H., Hu, L., Li, G.-N., et al. (2022) · BMC Neuroscience · doi:10.1186/s12868-022-00743-7 · Cited by 6
Self-citationScale Development-Related Genes Identified by Transcriptome Analysis
Zhang, Z., Ji, F.-Y., Jiang, S.-W., Wu, Z.-C., & Xu, Q.-H. (2022) · Fishes · doi:10.3390/fishes7020064 · Cited by 6
“WGCNA is an R package for weighted gene co-expression network analysis, which can simplify a large amount of complex gene data and quickly identify core genes related to target traits, and has been widely used in animal and plant research [18].”
MethodXie, T., Huang, Q.-M., Huang, Q.-L., Huang, Y.-T., Liu, S., Zeng, H.-X., & Liu, J.-P. (2024) · Stem cell research & therapeutics · doi:10.1186/s13287-023-03572-5 · Cited by 5 · see citing works
“To systematically analyse lncRNA expression patterns, a pipeline was used for lncRNA identification in a manner similar to that used in previous studies [31], which was constructed based on Cufflinks software [32].”
MethodSelf-citationLiu, Q.-Q., Yu, L., Zhang, Z., Chang, Y., Liu, Z.-H., & Xu, C.-Z. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043947 · Cited by 5
Genetic and Epigenetic Sexual Dimorphism of Brain Cells during Aging
Shirokova, O. M., Zaborskaya, O., Pchelin, P. V., Kozliaeva, E. V., Pershin, V. I., & Mukhina, I. V. (2023) · Brain Sciences · doi:10.3390/brainsci13020195 · Cited by 5 · see citing works
“Liu and coauthors (Liu et al., 2017) performed comprehensive RNA-seq and sex and age-biased analysis of lncRNA in rhesus macaque brain; they found a few sex and agebiased lncRNAs.”
Wang, M., Chen, D., Zheng, H., Zhao, L., Xue, X., Yu, F., Zhang, Y., Cheng, C., Niu, Q., Wang, S., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.690167 · Cited by 5 · see citing works
“Relative quantification was achieved by normalization to the amount of internal reference with the 2−11Ct method (Livak and Schmittgen, 2001).”
MethodSelf-citationLi, Y., Shen, Q. S., Peng, Q., Ding, W., Zhang, J., Zhong, X., An, N. A., Ji, M., Zhou, W., & Li, C. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab157 · Cited by 3 · see citing works
“CAGE-Seq data [11, 12] were analyzed by following the standard FANTOM pipeline [63].”
MethodXia, W., Shi, N., Li, C.-Q., & Tang, A. (2024) · Virulence · doi:10.1080/21505594.2024.2306795 · Cited by 3
“We used a pipeline for lncRNA identification similar to that previously reported [36] to systematically analyse the lncRNA expression pattern, which was constructed using StringTie 1.3.3 software [37].”
MethodInfluentialZhao, L., Xin, S.-M., Wu, Y.-F., Huang, S.-Y., Xu, K., Xu, Y., Ruan, D., Wu, B., Chen, D., & He, X.-J. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-08070-0 · Cited by 3
“Co-expression network analysis is widely used to explore the potential functions of lncRNAs [42, 43].”
BackgroundSelf-citationLópez‐Royo, T., Gascón, E., Moreno‐Martínez, L., Macías-Redondo, S., Zaragoza, P., Manzano, R., & Osta, R. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262412069 · Cited by 2 · see citing works
“Indeed, research in primates has demonstrated spatial, age, and sex-biassed changes in brain lncRNA expression, suggesting that these molecules may constitute a regulatory system that potentially contributes to brain development, ageing, and evolution [19,20].”
Ma, X., Chen, D., Li, C.-H., & Wu, W.-J. (2025) · Clinics · doi:10.1016/j.clinsp.2025.100732 · Cited by 2 · see citing works
Self-citationYu, M., Wu, G., Chang, Y., Cai, J., Wang, C., Zhang, D.-J., & Xu, C.-Z. (2025) · Biomolecules · doi:10.3390/biom15020180 · Cited by 2 · see citing works
“Among these techniques, constructing weighted gene co-expression network analysis (WGCNA) using differentially expressed genes (DEGs) obtained from RNA-seq efficiently identifies candidate genes closely associated with specific animal traits [23–26].”
Zhang, Y.-C., Tang, L., Wang, Y., Zhu, X.-Y., & Liu, L. (2023) · NeuroReport · doi:10.1097/wnr.0000000000001977 · Cited by 2 · see citing works
“This could be due to the variety of reported expression of lncRNA in different LPS treat-ment paradigms, different tissues and cells, compared to our results in brain tissue [28].”
ResultSelf-citationYang, N., Zhang, N.-Z., Wang, Z., Cao, W., He, X., Zhang, W., & Xing, Y.-Q. (2023) · BMC Genomics · doi:10.1186/s12864-023-09352-y · Cited by 2
“LncRNA prediction and direction identification To systematically analyze the lncRNA expression pattern, we used a pipeline for lncRNA identification similar to that previously reported [52], which was constructed based on the StringTie software [53].”
MethodSelf-citationWu, S.-L., Cheng, C., Zhu, W., Yang, J., He, B.-B., Li, S., Wang, X.-S., Guo, H., Chen, D., & Guo, Y.-M. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1152742 · Cited by 2
“To analyze lncRNA expression pattern, we used a pipeline to identify lncRNAs as previously reported (21).”
MethodSelf-citationA novel antiviral lncRNA EDAL shields a T309 O-GlcNAcylation site to promote EZH2 degradationPreprint
Sui, B.-K., Chen, D., Liu, W., Wu, Q., Tian, B., Hou, J., Li, Y.-Y., Liu, S., Xie, J., Jiang, H., et al. (2019) · bioRxiv · doi:10.1101/824813 · Cited by 2 · see citing works
Self-citationYilihamu, Y., Xu, R., Jia, W., Kukun, H., Aihemaiti, D., Chang, Y., Ding, S., & Wang, Y. (2024) · Gene · doi:10.1016/j.gene.2024.148694 · Cited by 1
Song, Y., Shen, T., Sun, H.-H., & Wang, X.-T. (2024) · Human Genetics · doi:10.1007/s00439-024-02653-6 · Cited by 1
“Including our previous works, several studies have demonstrated the widespread presence of AP phenomena in various physiological and pathological processes including cancer (Liu et al. 2017; Huang et al. 2021; Ushijima et al. 2017; Cui et al. 2021).”
Self-citationLei, L., Bai, Y.-H., Wang, J.-P., & Li, Y. (2022) · Asian Journal of Surgery · doi:10.1016/j.asjsur.2022.06.016 · Cited by 1
Fiselier, A., Byeon, B., Ilnytskyy, Y., Kovalchuk, I., & Kovalchuk, O. (2022) · Epigenomes · doi:10.3390/epigenomes6020011 · Cited by 1 · see citing works
“Sex-specific differences in the expression of microRNAs (miRNAs) [2–4] and long non-coding RNAs (lnc-RNAs) [5,6] in the brain of mammals in health and disease are also well-documented.”
BackgroundSui, B.-K., Zhao, J., Zheng, J., Zhou, M., Chen, H.-C., Fu, Z. F., & Zhao, L. (2022) · Journal of General Virology · doi:10.1099/jgv.0.001725 · Cited by 1
Non-Human Primates as a Comprehensive Model for Studying Epigenetic Markers of Aging
Petrova, V. M., Simoroz, E. V., Dudko, N. A., & Vasiļevska, J. (2026) · Genes · doi:10.3390/genes17080905
“The observed increase in lncRNA activity with age is also shown in the brains of rhesus macaques [49].”
Liu, J.-J., Li, Y.-Y., Tian, W.-L., Tang, Y.-H., Tan, J., Zhang, X.-Q., Liang, C.-E., Wu, J.-Q., Wang, J.-X., Xue, L., et al. (2026) · The FASEB Journal · doi:10.1096/fj.202503743r
Self-citationZhang, J., Huang, K., Zhou, J.-W., Liao, W., Li, F., Zhao, Z.-Z., & Wang, S. (2025) · Oncology Letters · doi:10.3892/ol.2025.15376
Yang, J.-Q., Yang, M., & Sheng, G.-T. (2023) · Open Medicine · doi:10.1515/med-2023-0657
“To systematically analyze the lncRNA expression pattern and methods, we used a previously reported lncRNA identification method based on cufflink software [20,21].”
MethodFiselier, A., Byeon, B., Ilnytskyy, Y., Kovalchuk, O., & Kovalchuk, I. (2022) · Epigenomes · doi:10.3390/epigenomes6040035 · Cited by 2 · see citing works
“The expression of lncRNAs in the brain is sex-specific [10].”
BackgroundXie, T., Huang, Q.-M., Huang, Q.-L., Zeng, H., & Liu, J.-P. (2021) · doi:10.21203/rs.3.rs-1073927/v1
Zhang, S.-C., Ahmad, S., Zhang, Y.-X., Hua, G., & Yi, J.-M. (2021) · Animals · doi:10.3390/ani11051268
Self-citationFang, Y., Yang, Y., Zhang, X.-L., Li, N., Yuan, B., Jin, L., Bao, S., Li, M., Zhao, D., Li, L., et al. (2021) · doi:10.21203/rs.3.rs-387093/v1
Brain transcriptomics of nonhuman primates: a review.
Pei, W., Fu, L., Li, S.-Q., & Yu, Y. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.135872
Sexual stage-induced long noncoding RNAs in the filamentous fungus Fusarium graminearum
Kim, W., Miguel-Rojas, C., Wang, J., Townsend, J., & Trail, F. (2018) · bioRxiv · doi:10.1101/270298
“More precise identification of lncRNAs, especially for those undergoing deadenylation by the RNA quality control machineries, should be accompanied by cap-analysis gene expression (CAGE)-seq (Bogu et al. 2016; Wery et al. 2016; Liu et al. 2017).”
Background
- Authors
- Liu, S., Wang, Z., Chen, D., Zhang, B., Tian, R.-R., Wu, J., Zhang, Y., Xu, K., Yang, L.-M., Cheng, C., Ma, J., Lv, L., Zheng, Y.-T., Hu, X., Zhang, Y., Wang, X., & Li, J.
- Affiliations
- Kunming Institute of Zoology (CN)
- University of Science and Technology of China (CN)
- ORCID
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2017-07-07
- Volume
- 27
- Issue
- 9
- Pages
- 1608-1620
- ISSN
- 1088-9051 (ISSN-L)
- 1549-5469
- PMC
- PMC5580719
- OpenAlex
- W2724845256
- Cited by
- 130
- References
- 49
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 29 · 2023: 16 · 2022: 15 · 2021: 29 · 2020: 16 · 2019: 11 · 2018: 7 · 2017: 1
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Chinese Academy of Sciences (Y406541141, 1100050210, KJ2070000031)
- Ministry of Science and Technology of China (2015CB755605)
- National Science Foundation of China (91649119, 91440108, 81471312)
- Strategic Priority Research Program
- CAS (XDB02020005)
- Appreciate the Beauty of Life, Inc. (ABL2015-02007)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- long non-coding RNA, lncRNA expression, rhesus monkeys, spatiotemporal gene expression, sex differences, brain aging, brain development, cerebral cortex
- MeSH terms
- Animals, Brain, Female, Gene Expression Regulation, Multigene Family, Humans, Macaca mulatta, Male, RNA, Messenger, Epigenesis, Genetic, Molecular Sequence Annotation, RNA, Long Noncoding
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