circRNA在猪脂肪沉积调控中的研究进展

doi:10.16431/j.cnki.1671-7236.2025.04.016

摘要/Abstract

摘要： 脂肪沉积能力是影响猪瘦肉率、屠宰率及肉品质的重要因素之一，而脂肪沉积的调控机制涉及复杂的生物学过程，其中非编码RNA (non-coding RNA，ncRNA)这类表观遗传调节因子扮演着关键角色。环状RNA (circular RNA,circRNA)是真核生物中存在的一种共价闭合的环状ncRNA，具有相对保守性和时空特异性，作用途径丰富多样，并广泛参与细胞增殖和凋亡、基因转录、癌症发生、神经系统疾病等各类生物学过程。近年来，越来越多的研究表明，circRNA对于猪皮下、肌内和内脏脂肪的沉积有着重要调控作用，但大部分研究还处于发现和鉴定的起步阶段，很多circRNA上、下游通路的具体机制尚不清晰。目前来看，circRNA主要通过miRNA的分子海绵机制来控制脂肪沉积相关基因的表达，影响脂质代谢，促进或抑制脂肪细胞的增殖分化，调控猪的脂肪沉积。作者在概述脂肪组织的分类与功能、调控脂肪沉积的关键基因、circRNA的生物发生及功能的基础上，系统回顾并总结了国内外circRNA调控猪脂肪沉积的研究进展，以期为进一步探究猪脂肪沉积的机制提供参考。

关键词: 猪; circRNA; 脂肪沉积

Abstract: Fat deposition ability is one of the important factors affecting the lean meat rate,slaughter rate and meat quality of pigs,and the regulatory mechanism of fat deposition involves complex biological processes,among which epigenetic regulators such as non-coding RNA (ncRNA) play a key role.Circular RNA (circRNA) is a covalently closed circular ncRNA existing in eukaryotes,it is relatively conservative and spatiotemporally specific,with rich and diverse action pathways,and is widely involved in various biological processes such as cell proliferation and apoptosis,gene transcription,cancer occurrence and nervous system diseases.In recent years,more and more studies have shown that circRNA plays an important regulatory role in the deposition of subcutaneous,intramuscular and visceral fat in pigs,but most studies are still in the initial stage of discovery and identification,and the specific mechanisms of many upstream and downstream pathways of circRNA are still unclear.At present,circRNA mainly controls the expression of fat deposition-related genes through the molecular sponge mechanism of miRNA,affects lipid metabolism,promotes or inhibits the proliferation and differentiation of adipocytes,and regulates fat deposition in pigs.Based on an overview of the classification and function of adipose tissue,key genes regulating fat deposition,and the biogenesis and function of circRNA,this paper systematically reviews and summarizes the research progress on circRNA regulating fat deposition of pigs at home and abroad,in order to provide a reference for further exploration of the mechanism of pig fat deposition.

Key words: pigs; circRNA; fat deposition

中图分类号:

S828
Q78

何晓菲, 雷宇航, 朱砺, 甘麦邻, 沈林園. circRNA在猪脂肪沉积调控中的研究进展[J]. 中国畜牧兽医, 2025, 52(4): 1627-1638.

HE Xiaofei, LEI Yuhang, ZHU Li, GAN Mailin, SHEN Linyuan. Research Progress on circRNA Regulating Fat Deposition in Pigs[J]. China Animal Husbandry and Veterinary Medicine, 2025, 52(4): 1627-1638.

参考文献

[1] MALGWI I H,HALAS V,GRVNVALD P,et al.Genes related to fat metabolism in pigs and intramuscular fat content of pork:A focus on nutrigenetics and nutrigenomics[J].Animals (Basel),2022,12(2):150.
[2] LI Y X,YAO L T,LU J.IL-35 inhibits adipogenesis via PPARγ-Wnt/β-catenin signaling pathway by targeting Axin2[J].International Immunopharmacology,2023,122:110615.
[3] LIU S,HUANG J,WANG X,et al.Transcription factors regulate adipocyte differentiation in beef cattle[J].Animal Genetics,2020,51(3):351-357.
[4] HU C L,FENG X,MA Y F,et al.circADAMTS16 inhibits differentiation and promotes proliferation of bovine adipocytes by targeting miR-10167-3p[J]. Cells,2023,12(1175):1175.
[5] ZHANG W N,ZHU H,MA Z W,et al.Subcutaneous adipose tissue alteration in aging process associated with thyroid hormone signaling[J].BMC Medical Genomics,2023,16(1):202.
[6] LIU Y J,LIU H T,LI Y,et al.Circular RNA SAMD4A controls adipogenesis in obesity through the miR-138-5p/EZH2 axis[J].Theranostics,2020,10(10):4705-4719.
[7] YU G L,YANG Z,PENG T H,et al.Circular RNAs:Rising stars in lipid metabolism and lipid disorders[J].Journal of Cellular Physiology,2021,236(7):4797-4806.
[8] WU J Y,ZHANG S L,YUE B L,et al.circRNA profiling reveals circPPARγ modulates adipogenic differentiation via sponging miR-92a-3p[J].Journal of Agricultural and Food Chemistry,2022,70(22):6698-6708.
[9] ZHANG P,ZHANG X O,JIANG T T,et al.Comprehensive identification of alternative back-splicing in human tissue transcriptomes[J].Nucleic Acids Research,2020,48(4):1779-1789.
[10] WU W Y,JI P F,ZHAO F Q.circAtlas:An integrated resource of one million highly accurate circular RNAs from 1070 vertebrate transcriptomes[J].Genome Biology,2020,21(1):101.
[11] SANGER H L,KLOTZ G,RIESNER D,et al.Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures[J].Proceedings of the National Academy of Sciences of the United States of America,1976,73(11):3852-3856.
[12] JECK W R,SORRENTINO J A,WANG K,et al.Circular RNAs are abundant,conserved,and associated with ALU repeats[J].RNA,2013,19(2):141-157.
[13] LU T T,CUI L L,ZHOU Y,et al.Transcriptome-wide investigation of circular RNAs in rice[J].RNA,2015,21(12):2076-2087.
[14] MEMCZAK S,JENS M,ELEFSINIOTI A,et al.Circular RNAs are a large class of animal RNAs with regulatory potency[J].Nature,2013,495(7441):333-338.
[15] KRISTENSEN L S,ANDERSEN M S,STAGSTED L V W,et al.The biogenesis,biology and characterization of circular RNAs[J].Nature Reviews Genetics,2019,20(11):675-691.
[16] YANG Z Z,XIE L,HAN L,et al.Circular RNAs:Regulators of cancer-related signaling pathways and potential diagnostic biomarkers for human cancers[J].Theranostics,2017,7(12):3106-3117.
[17] WANG Z Y,WEN Z J,XU H M,et al.Exosomal noncoding RNAs in central nervous system diseases:Biological functions and potential clinical applications[J].Frontiers in Molecular Neuroscience,2022,15:1004221.
[18] FANALE D,TAVERNA S,RUSSO A,et al.Circular RNA in exosomes[J].Advances in Experimental Medicine and Biology,2018,1087:109-117.
[19] RABE K,LEHRKE M,PARHOFER K G,et al.Adipokines and insulin resistance[J].Molecular Medicine,2008,14(11-12):741-751.
[20] MORIGNY P,BOUCHER J,ARNER P,et al.Lipid and glucose metabolism in white adipocytes:Pathways,dysfunction and therapeutics[J].Nature Reviews Endocrinology,2021,17(5):276-295.
[21] CZECH M P.Mechanisms of insulin resistance related to white,beige,and brown adipocytes[J].Molecular Metabolism,2020,34:27-42.
[22] ZHU X Q,ZENG C F,YU B P.White adipose tissue in metabolic associated fatty liver disease[J].Clinics and Research in Hepatology and Gastroenterology,2024,48(5):102336.
[23] SCHUMACHER M,DELCURTO-WYFFELS H,THOMSON J,et al.Fat deposition and fat effects on meat quality-A review[J].Animals (Basel),2022,12(12):1550.
[24] CHAIT A,DEN HARTIGH L J.Adipose tissue distribution,inflammation and its metabolic consequences,including diabetes and cardiovascular disease[J]. Frontiers in Cardiovascular Medicine,2020,7:22.
[25] GUGLIUCCI A.Biomarkers of dysfunctional visceral fat[J].Advances in Clinical Chemistry,2022,109:1-30.
[26] HAUSMAN G J,BASU U,DU M,et al.Intermuscular and intramuscular adipose tissues:Bad vs.good adipose tissues[J].Adipocyte,2014,3(4):242-255.
[27] HOCQUETTE J F,GONDRET F,BAÉZA E,et al.Intramuscular fat content in meat-producing animals:Development,genetic and nutritional control,and identification of putative markers[J].Animal,2010,4(2):303-319.
[28] XIAO C,WEI T,LIU L X,et al.Whole-transcriptome analysis of preadipocyte and adipocyte and cnstruction of regulatory networks to investigate lipid metabolism in sheep[J].Frontiers in Genetics,2021,12:662143.
[29] NEMATBAKHSH S,PEI PEI C,SELAMAT J,et al.Molecular regulation of lipogenesis,adipogenesis and fat deposition in chicken[J].Genes,2021,12(3):414.
[30] GÁLVEZ F,DOMÍNGUEZ R,PATEIRO M,et al.Effect of gender on breast and thigh turkey meat quality[J].British Poultry Science,2018,59(4):408-415.
[31] 韩丽,黄兴国,尹杰.营养调控对宁乡猪肉品质的影响及其分子机制研究[J].动物营养学报,2023,35(10):6164-6175.HAN L,HUANG X G,YIN J.Effects of nutrition regulation on meat quality of Ningxiang pigs and its molecular mechanism[J].Chinese Journal of Animal Nutrition,2023,35(10):6164-6175.(in Chinese)
[32] LAMBE N R,CLELLAND N,DRAPER J,et al.Prediction of intramuscular fat in lamb by visible and near-infrared spectroscopy in an abattoir environment[J].Meat Science,2021,171:108286.
[33] HÉRAULT F,DAMON M,CHEREL P,et al.Combined GWAS and LDLA approaches to improve genome-wide quantitative trait loci detection affecting carcass and meat quality traits in pig[J].Meat Science,2018,135:148-158.
[34] LEE J E,CHO Y W,DENG C X,et al.MLL3/MLL4-associated PAGR1 regulates adipogenesis by controlling induction of C/EBPβ and C/EBPδ[J].Molecular and Cellular Biology,2020,40(17):e00209-20.
[35] GERSTNER M,HELLER V,FECHNER J,et al.Prmt6 represses the pro-adipogenic PPAR-gamma-C/EBP-alpha transcription factor loop[J].Scientific Reports,2024,14(1):6656.
[36] AMBELE M A,DHANRAJ P,GILES R,et al.Adipogenesis:A complex interplay of multiple molecular determinants and pathways[J].International Journal of Molecular Sciences,2020,21(12):E4283.
[37] DONG P Y,MAI Y,ZHANG Z Y,et al.miR-15a/b promote adipogenesis in porcine pre-adipocyte via repressing FoxO1[J].Acta Biochimica et Biophysica Sinica,2014,46(7):565-571.
[38] GARIN-SHKOLNIK T,RUDICH A,HOTAMISLIGIL G S,et al.FABP4 attenuates PPARγ and adipogenesis and is inversely correlated with PPARγ in adipose tissues[J].Diabetes,2014,63(3):900-911.
[39] ZHANG Y,ZHENG Y,WANG X Y,et al.Bovine stearoyl-CoA desaturase 1 promotes adipogenesis by activating the PPARγ receptor[J].Journal of Agricultural and Food Chemistry,2020,68(43):12058-12066.
[40] LIU K L,LIN L Y,LI Q,et al.Scd1 controls de novo beige fat biogenesis through succinate-dependent regulation of mitochondrial complex Ⅱ[J].Proceedings of the National Academy of Sciences of the United States of America,2020,117(5):2462-2472.
[41] KERSTEN S.Role and mechanism of the action of angiopoietin-like protein ANGPTL4 in plasma lipid metabolism[J].Journal of Lipid Research,2021,62:100150.
[42] REN H,ZHANG H,HUA Z,et al.ACSL4 directs intramuscular adipogenesis and fatty acid composition in pigs[J].Animals (Basel),2022,12(1):119.
[43] GARCÍA-NIÑO W R,ZAZUETA C.New insights of Krüppel-like transcription factors in adipogenesis and the role of their regulatory neighbors[J].Life Sciences,2021,265:118763.
[44] YUCE K,OZKAN A I.The Krüppel-like factor (KLF) family,diseases,and physiological events[J].Gene,2024,895:148027.
[45] LI Y Y,XU Q,WANG Y,et al.Knockdown of KLF7 inhibits the differentiation of both intramuscular and subcutaneous preadipocytes in goat[J].Animal Biotechnology,2023,34(4):1072-1082.
[46] QU S B,YANG X S,LI X L,et al.Circular RNA:A new star of noncoding RNAs[J].Cancer Letters,2015,365(2):141-148.
[47] ZHANG J,ZHANG X L,LI C D,et al.Circular RNA profiling provides insights into their subcellular distribution and molecular characteristics in HepG2 cells[J].RNA Biology,2019,16(2):220-232.
[48] LI Z Y,HUANG C,BAO C,et al.Exon-intron circular RNAs regulate transcription in the nucleus[J].Nature Structural&Molecular Biology,2015,22(3):256-264.
[49] NGO L H,BERT A G,DREDGE B K,et al.Nuclear export of circular RNA[J].Nature,2024,627(8002):212-220.
[50] EBBESEN K K,HANSEN T B,KJEMS J.Insights into circular RNA biology[J]. RNA Biology,2017,14(8):1035-1045.
[51] MALVIYA A,BHUYAN R.The recent advancements in circRNA research:From biogenesis to therapeutic interventions[J].Pathology,Research and Practice,2023,248:154697.
[52] NI L,YAMADA T,NAKATANI K.Utility of oligonucleotide in upregulating circular RNA production in a cellular model[J].Scientific Reports,2024,14(1):8096.
[53] GONG Y R,LIN Z Z,WANG Y,et al.Research progress of non-coding RNAs regulation on intramuscular adipocytes in domestic animals[J].Gene,2023,860:147226.
[54] ZENG Y,ZOU Y T,GAO G F,et al.The biogenesis,function and clinical significance of circular RNAs in breast cancer[J].Cancer Biology&Medicine,2022,19(1):14-29.
[55] LIANG D M,WILUSZ J E.Short intronic repeat sequences facilitate circular RNA production[J].Genes&Development,2014,28(20):2233-2247.
[56] BARRETT S P,WANG P L,SALZMAN J.Circular RNA biogenesis can proceed through an exon-containing lariat precursor[J].eLife,2015,4:e07540.
[57] ZHANG Y,ZHANG X O,CHEN T,et al.Circular intronic long noncoding RNAs[J].Molecular Cell,2013,51(6):792-806.
[58] ROBIC A,DEMARS J,KVHN C.In-depth analysis reveals production of circular RNAs from non-coding sequences[J].Cells,2020,9(8):E1806.
[59] MONTAÑÉS-AGUDO P,VAN DER MADE I,AUFIERO S,et al.Quaking regulates circular RNA production in cardiomyocytes[J].Journal of Cell Science,2023,136(13):jcs261120.
[60] NI X Z,DUAN L,BAO Y D,et al.circ_005077 accelerates myocardial lipotoxicity induced by high-fat diet via CyPA/p47PHOX mediated ferroptosis[J].Cardiovascular Diabetology,2024,23(1):129.
[61] CHEN R X,CHEN X,XIA L P,et al.N6-methyladenosine modification of circNSUN2 facilitates cytoplasmic export and stabilizes HMGA2 to promote colorectal liver metastasis[J].Nature Communications,2019,10(1):4695.
[62] ASHWAL-FLUSS R,MEYER M,PAMUDURTI N R,et al.circRNA biogenesis competes with pre-mRNA splicing[J].Molecular Cell,2014,56(1):55-66.
[63] DU W W,YANG W,LIU E,et al.FoxO3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2[J].Nucleic Acids Research,2016,44(6):2846-2858.
[64] CHEN Q J J,WANG H B,LI Z,et al.Circular RNA ACTN4 promotes intrahepatic cholangiocarcinoma progression by recruiting YBX1 to initiate FZD7 transcription[J].Journal of Hepatology,2022,76(1):135-147.
[65] LIU S,GUO X Y,SHANG Q J,et al.The biogenesis,biological functions and modification of circular RNAs[J].Experimental and Molecular Pathology,2023,131:104861.
[66] ZHOU B,YANG H,YANG C,et al.Translation of noncoding RNAs and cancer[J].Cancer Letters,2021,497:89-99.
[67] YANG Y,FAN X J,MAO M W,et al.Extensive translation of circular RNAs driven by N6-methyladenosine[J].Cell Research,2017,27(5):626-641.
[68] ZHOU C,MOLINIE B,DANESHVAR K,et al.Genome-wide maps of m⁶A circRNAs identify widespread and cell-type-specific methylation patterns that are distinct from mRNAs[J].Cell Reports,2017,20(9):2262-2276.
[69] CHANG J,SHIN M K,PARK J,et al.An interaction between eIF4A3 and eIF3g drives the internal initiation of translation[J].Nucleic Acids Research, 2023,51(20):10950-10969.
[70] GARCÍA-MUSE T,AGUILERA A.R loops:From physiological to pathological roles[J].Cell,2019,179(3):604-618.
[71] LI X,ZHANG J L,LEI Y N,et al.Linking circular intronic RNA degradation and function in transcription by RNase H1[J].Science China (Life Sciences),2021,64(11):1795-1809.
[72] GU Y,WANG Y Y,HE L Y,et al.Circular RNA circIPO11 drives self-renewal of liver cancer initiating cells via Hedgehog signaling[J].Molecular Cancer,2021,20(1):132.
[73] LIU C X,CHEN L L.Circular RNAs:Characterization,cellular roles,and applications[J].Cell,2022,185(12):2016-2034.
[74] LI B,YANG J Z,HE J,et al.Spatiotemporal regulation and functional analysis of circular RNAs in skeletal muscle and subcutaneous fat during pig growth[J].Biology,2021,10(9):841.
[75] LIU X,LIU K,SHAN B,et al.A genome-wide landscape of mRNAs,lncRNAs,and circRNAs during subcutaneous adipogenesis in pigs[J].Journal of Animal Science and Biotechnology,2018,9(1):76.
[76] 李萌,李娇,张娜,等.猪脂肪组织circIDH2的鉴定及功能分析[J].中国畜牧杂志,2021,57(S1):136-142.LI M,LI J,ZHANG N,et al.Identification and functional analysis of circIDH2 in porcine adipose tissue[J].Chinese Journal of Animal Science,2021,57(S1):136-142.(in Chinese)
[77] 张晓,冉雪琴,牛熙,等.香猪3种组织环状RNA的表达及其功能分析[J].中国畜牧兽医,2020,47(12):3870-3881.ZHANG X,RAN X Q,NIU X,et al.Expression and function analysis of circular RNA in three tissues of Xiang pig[J].China Animal Husbandry&Veterinary Medicine,2020,47(12):3870-3881.(in Chinese)
[78] WEI X F,ZHAO X,SHAN X Y,et al.miR-107 regulates adipocyte differentiation and adipogenesis by targeting apolipoprotein C-2(APOC2) in bovine[J].Genes,2022,13(8):1467.
[79] AHONEN M A,HARIDAS P A N,MYSORE R,et al.miR-107 inhibits CDK6 expression,differentiation,and lipid storage in human adipocytes[J].Molecular and Cellular Endocrinology,2019,479(1):110-116.
[80] SHI X E,LI Y F,JIA L,et al.microRNA-199a-5p affects porcine preadipocyte proliferation and differentiation[J].International Journal of Molecular Sciences,2014,15(5):8526-8538.
[81] 李娇,赵天枝,王婕妤,等.circECH1通过充当miR-365-5p海绵抑制猪前体脂肪细胞增殖[J].中国生物化学与分子生物学报,2023,39(5):672-682.LI J,ZHAO T Z,WANG J Y,et al.circECH1 inhibits proliferation of porcine preadipocyte by sponging miR-365-5p[J].Chinese Journal of Biochemistry and Molecular Biology,2023,39(5):672-682.(in Chinese).
[82] LI M,LI J,JI M T,et al.circHOMER1 inhibits porcine adipogenesis via the miR-23b/SIRT1 axis[J].FASEB Journal,2023,37(3):e22828.
[83] LI A,HUANG W L,ZHANG X X,et al.Identification and characterization of circRNAs of two pig breeds as a new biomarker in metabolism-related diseases[J].Cellular Physiology&Biochemistry,2018,47(6):2458-2470.
[84] 董新星,刘金桥,李明丽,等.撒坝猪与大白猪背脂差异circRNA筛选与调控网络分析[J].中国畜牧杂志,2023,59(5):116-123.DONG X X,LIU J Q,LI M L,et al.Screening of differentially expressed circRNAs in back fat of Saba pigs and Large White pigs and analysis of their regulatory networks[J].Chinese Journal of Animal Science,2023,59(5):116-123.(in Chinese)
[85] LI Q W,WANG L Y,XING K,et al.Identification of circRNAs associated with adipogenesis based on RNA-Seq data in pigs[J].Genes,2022,13(11):2062.
[86] LIU X M,BAI Y,CUI R,et al.sus_circPAPPA2 regulates fat deposition in castrated pigs through the miR-2366/GK pathway[J].Biomolecules,2022,12(6):753.
[87] TAN L,CHEN Z,TENG M,et al.Genome-wide analysis of mRNAs,lncRNAs,and circRNAs during intramuscular adipogenesis in Chinese Guizhou Congjiang pigs[J].PLoS One,2022,17(1):e0261293.
[88] LI J X,ZHAO X Y,WANG Y P,et al.Comprehensive analysis of differentially expressed mRNAs,lncRNAs and circRNAs related to intramuscular fat deposition in Laiwu pigs[J].Genes,2022,13(8):1349.
[89] JIN Z,GAO H,FU Y,et al.Whole-transcriptome analysis sheds light on the biological contexts of intramuscular fat deposition in Ningxiang pigs[J].Genes,2024,15(5):642.
[90] QI K L,LIU Y K,LI C L,et al.Construction of circRNA-related ceRNA networks in longissimus dorsi muscle of Queshan Black and Large White pigs[J].Molecular Genetics&Genomics,2022,297(1):101-112.
[91] LIU Y K,DOU Y Q,QI K L,et al.circSETBP1 acts as a miR-149-5p sponge to promote intramuscular fat deposition by regulating CRTCs[J].Journal of Agricultural and Food Chemistry,2022,70(40):12841-12851.
[92] LI M,ZHANG N,ZHANG W F,et al.Comprehensive analysis of differentially expressed circRNAs and ceRNA regulatory network in porcine skeletal muscle[J].BMC Genomics,2021,22(1):320.
[93] WANG J,CHEN J F,MA Q,et al.Identification and characterization of circRNAs related to meat quality during embryonic development of the longissimus dorsi muscle in two pig breeds[J].Frontiers in Genetics,2022,13:1019687.
[94] DING Y Y,HOU Y H,LING Z J,et al.Identification of candidate genes and regulatory competitive endogenous RNA (ceRNA) networks underlying intramuscular fat content in Yorkshire pigs with extreme fat deposition phenotypes[J].International Journal of Molecular Sciences,2022,23(20):12596.
[95] RONG X Y,LI R X,GONG T Y,et al.circMEF2C (2,3) modulates proliferation and adipogenesis of porcine intramuscular preadipocytes by miR-383/671-3p/MEF2C axis[J].iScience,2024,27(5):109710.
[96] LI B J,HE Y,WU W J,et al.Circular RNA profiling identifies novel circPPARA that promotes intramuscular fat deposition in pigs[J].Journal of Agricultural and Food Chemistry,2022,70(13):4123-4137.
[97] 张娜.circIGF1R调控猪成脂和成肌分化的作用及机制研究[D].太谷:山西农业大学,2022.ZHANG N.Effect and mechanism of circIGF1R in regulating adipogenic and myogenic differentiation in pigs[D].Taigu:Shanxi Agricultural University,2022.(in Chinese)
[98] YOUSUF S,LI A,FENG H,et al.Genome-wide expression profiling and networking reveals an imperative role of IMF-associated novel circRNAs as ceRNA in pigs[J].Cells,2022,11(17):2638.
[99] WANG J,YANG Y B,XING B S,et al.Castration induced circRNA expressional changes in subcutaneous adipose tissue of male pigs[J].Animal Science Journal,2021,92(1):e13648.
[100] FENG H,YOUSUF S,LIU T Y,et al.The comprehensive detection of miRNA and circRNA in the regulation of intramuscular and subcutaneous adipose tissue of Laiwu pig[J].Scientific Reports,2022,12(1):16542.
[101] CHEN W W,MA H M,LI B,et al.Spatiotemporal regulation of circular RNA expression during liver development of Chinese indigenous Ningxiang pigs[J]. Genes,2022,13(5):746.