Novel Insights into the Circadian Rhythms Based on Long Noncoding and Circular RNA Profiling

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Jan 23

PMID 38256234

Authors

Xiaodong Tan

Jiawen Zhang

Jie Dong

Minjie Huang

Zhenzhen Zhou

Deqian Wang

Affiliations

Soon will be listed here.

Abstract

Circadian rhythm disorders pose major risks to human health and animal production activity, and the hypothalamus is the center of circadian rhythm regulation. However, the epigenetic regulation of circadian rhythm based on farm animal models has been poorly investigated. We collected chicken hypothalamus samples at seven time points in one light/dark cycle and performed long noncoding RNA (lncRNA), circular RNA (circRNA), and mRNA sequencing to detect biomarkers associated with circadian rhythm. We enhanced the comprehensive expression profiling of ncRNAs and mRNAs in the hypothalamus and found two gene sets (circadian rhythm and retinal metabolism) associated with the light/dark cycle. Noncoding RNA networks with circadian expression patterns were identified by differential expression and circadian analysis was provided that included 38 lncRNAs, 15 circRNAs, and 200 candidate genes. Three lncRNAs (ENSGALT00000098661, ENSGALT00000100816, and MSTRG.16980.1) and one circRNA (novel_circ_010168) in the ncRNA-mRNA regulatory network were identified as key molecules influencing circadian rhythm by regulating in retinal metabolism. These ncRNAs were predicted to be related to pernicious anemia, gonadal, eye disease and other disorders in humans. Together, the findings of this study provide insights into the epigenetic mechanisms of circadian rhythm and reveal as a promising target of circadian rhythm regulation.

References

Zhang Y, Li Y, Yuan Y, Wang J, Zhang S, Zhu R . Reducing light exposure enhances the circadian rhythm of the biological clock through interactions with the gut microbiota. Sci Total Environ. 2022; 858(Pt 3):160041. DOI: 10.1016/j.scitotenv.2022.160041. View

Si Y, Chen J, Shen Y, Kubra S, Mei B, Qin Z . Circadian rhythm sleep disorders and time-of-day-dependent memory deficiency in Presenilin1/2 conditional knockout mice with long noncoding RNA expression profiling changes. Sleep Med. 2023; 103:146-158. DOI: 10.1016/j.sleep.2023.02.007. View

You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G . Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci. 2015; 18(4):603-610. PMC: 4376664. DOI: 10.1038/nn.3975. View

Barna J, Csermely P, Vellai T . Roles of heat shock factor 1 beyond the heat shock response. Cell Mol Life Sci. 2018; 75(16):2897-2916. PMC: 11105406. DOI: 10.1007/s00018-018-2836-6. View

Kim D, Paggi J, Park C, Bennett C, Salzberg S . Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37(8):907-915. PMC: 7605509. DOI: 10.1038/s41587-019-0201-4. View

Zheng Y, Wang H, Guo H, Xie H, Zhang W, Han D . CircRNA-WNK2 Acts as a ceRNA for miR-328a-3p to Promote AANAT Expression in the Male Rat Pineal Gland. Endocrinology. 2021; 163(2). DOI: 10.1210/endocr/bqab255. View

McGlincy N, Valomon A, Chesham J, Maywood E, Hastings M, Ule J . Regulation of alternative splicing by the circadian clock and food related cues. Genome Biol. 2012; 13(6):R54. PMC: 3446320. DOI: 10.1186/gb-2012-13-6-r54. View

Wu G, Anafi R, Hughes M, Kornacker K, Hogenesch J . MetaCycle: an integrated R package to evaluate periodicity in large scale data. Bioinformatics. 2016; 32(21):3351-3353. PMC: 5079475. DOI: 10.1093/bioinformatics/btw405. View

Sun L, Luo H, Bu D, Zhao G, Yu K, Zhang C . Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res. 2013; 41(17):e166. PMC: 3783192. DOI: 10.1093/nar/gkt646. View

10.

Lincoln G, Messager S, Andersson H, Hazlerigg D . Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci U S A. 2002; 99(21):13890-5. PMC: 129793. DOI: 10.1073/pnas.212517599. View

11.

Liu L, Wang Z, Cao J, Dong Y, Chen Y . Effect of melatonin on monochromatic light-induced changes in clock gene circadian expression in the chick liver. J Photochem Photobiol B. 2019; 197:111537. DOI: 10.1016/j.jphotobiol.2019.111537. View

12.

Isobe Y, Hida H, Nishino H . Circadian rhythm of metabolic oscillation in suprachiasmatic nucleus depends on the mitochondrial oxidation state, reflected by cytochrome C oxidase and lactate dehydrogenase. J Neurosci Res. 2011; 89(6):929-35. DOI: 10.1002/jnr.22609. View

13.

Ivanov A, Memczak S, Wyler E, Torti F, Porath H, Orejuela M . Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 2015; 10(2):170-7. DOI: 10.1016/j.celrep.2014.12.019. View

14.

He X, Di R, Guo X, Cao X, Zhou M, Li X . Transcriptomic Changes of Photoperiodic Response in the Hypothalamus Were Identified in Ovariectomized and Estradiol-Treated Sheep. Front Mol Biosci. 2022; 9:848144. PMC: 9036065. DOI: 10.3389/fmolb.2022.848144. View

15.

Korf H . The pineal organ as a component of the biological clock. Phylogenetic and ontogenetic considerations. Ann N Y Acad Sci. 1994; 719:13-42. DOI: 10.1111/j.1749-6632.1994.tb56818.x. View

16.

Dudek M, Gossan N, Yang N, Im H, Ruckshanthi J, Yoshitane H . The chondrocyte clock gene Bmal1 controls cartilage homeostasis and integrity. J Clin Invest. 2015; 126(1):365-76. PMC: 4701559. DOI: 10.1172/JCI82755. View

17.

Sun L, Ma J, Chen J, Pan Z, Li L . Bioinformatics-Guided Analysis Uncovers AOX1 as an Osteogenic Differentiation-Relevant Gene of Human Mesenchymal Stem Cells. Front Mol Biosci. 2022; 9:800288. PMC: 8920545. DOI: 10.3389/fmolb.2022.800288. View

18.

Chun S, Fortin B, Fellows R, Habowski A, Verlande A, Song W . Disruption of the circadian clock drives loss of heterozygosity to accelerate colorectal cancer. Sci Adv. 2022; 8(32):eabo2389. PMC: 9365282. DOI: 10.1126/sciadv.abo2389. View

19.

Xue Z, Ye Q, Anson S, Yang J, Xiao G, Kowbel D . Transcriptional interference by antisense RNA is required for circadian clock function. Nature. 2014; 514(7524):650-3. PMC: 4214883. DOI: 10.1038/nature13671. View

20.

Love M, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. PMC: 4302049. DOI: 10.1186/s13059-014-0550-8. View