circRNA作为ceRNA调控畜禽重要经济性状的研究进展

doi:10.11843/j.issn.0366-6964.2023.06.001

摘要/Abstract

摘要： 竞争性内源RNA(competing endogenous RNA,ceRNA)机制指具有同种miRNA反应元件(microRNA response elements,MRE)的RNA分子,通过竞争性地结合该miRNA以在转录后水平调控基因的表达,进而影响细胞的生物学功能。ceRNA机制的有效性受细胞环境、miRNA活性及其与不同RNA分子间亲和力等因素的影响。虽然环状RNA(circular RNA,circRNA)和长链非编码RNA(long non-coding RNA,lncRNA)等均可作为ceRNA,但circRNA是相对更为有效的ceRNA分子,因为其在进化过程中稳定且保守,可使ceRNA信号在不同组织中传导。本文在探讨ceRNA调控机制影响因素的基础上,进一步综述了circRNA作为ceRNA调控畜禽肌肉发育、脂肪沉积、乳腺及卵泡发育等方面的研究进展,以期为深入研究畜禽重要经济性状中ceRNA调控网络提供新思路。

关键词: 竞争性内源RNA, 影响因素, 环状RNA, 经济性状, 调控机制

Abstract: Competing endogenous RNAs (ceRNA) refers to RNAs harboring the same microRNA response elements (MRE), competitively binding the miRNA to regulate gene expression post-transcriptionally. Eventually, the biological functions of cells are altered. The efficiency of ceRNA is affected by the cellular environment, miRNA activity, intermolecular affinity with RNAs, etc. Both circular RNA (circRNA) and long non-coding RNA (lncRNA) can act as ceRNA; circRNA is more effective based on its higher stability and conservation, enabling its transition into different tissues. This paper discussed the factors affecting the ceRNA mechanism, then reviewed the research progress of ceRNA-mediated regulation of circRNAs in muscle growth, fat deposition, mammary gland and follicular development in animals. In the hope of providing new insight for the in-depth study of the ceRNA regulatory network in the development of critical economic traits for animals.

Key words: competing endogenous RNAs, influence factor, circRNA, economic trait, regulatory mechanism

中图分类号:

S813

安宗麒, 占思远, 李利, 张红平. circRNA作为ceRNA调控畜禽重要经济性状的研究进展[J]. 畜牧兽医学报, 2023, 54(6): 2215-2222.

AN Zongqi, ZHAN Siyuan, LI Li, ZHANG Hongping. ceRNA-mediated Function of CircRNA on Critical Economic Traits in Animals[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(6): 2215-2222.

参考文献 67

[1]	CESANA M,CACCHIARELLI D,LEGNINI I,et al.A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA[J].Cell,2011,147(2):358-369.
[2]	SALMENA L,POLISENO L,TAY Y,et al.A ceRNA hypothesis:The Rosetta stone of a hidden RNA language?[J].Cell,2011,146(3):353-358.
[3]	KARRETH F A,TAY Y,PERNA D,et al.In vivo identification of tumor- suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma[J].Cell,2011,147(2):382-395.
[4]	CHIU H S,MARTÍNEZ M R,BANSAL M,et al.High-throughput validation of ceRNA regulatory networks[J].BMC Genomics,2017,18(1):418.
[5]	TAY Y,RINN J,PANDOLFI P P.The multilayered complexity of ceRNA crosstalk and competition[J].Nature,2014,505(7483):344-352.
[6]	LI J J,LIU Y,XIN X F,et al.Evidence for positive selection on a number of microRNA regulatory interactions during recent human evolution[J].PLoS Genet,2012,8(3):e1002578.
[7]	THOMAS M,LIEBERMAN J,LAL A.Desperately seeking microRNA targets[J].Nat Struct Mol Biol,2010,17(10):1169-1174.
[8]	SEITZ H.Redefining microRNA targets[J].Curr Biol,2009,19(10):870-873.
[9]	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.
[10]	ALA U,KARRETH F A,BOSIA C,et al.Integrated transcriptional and competitive endogenous RNA networks are cross-regulated in permissive molecular environments[J].Proc Natl Acad Sci U S A,2013,110(18):7154-7159.
[11]	KIMURA T,JIANG S W,YOSHIDA N,et al.Interferon-alpha competing endogenous RNA network antagonizes microRNA-1270[J].Cell Mol Life Sci,2015,72(14):2749-2761.
[12]	STAMOULAKATOU E,PINOLI P,CERI S,et al.Impact of mutational signatures on microRNA and their response elements[C]//Proceedings of the Pacific Symposium on Biocomputing 2020.Fairmont Orchid:World Scientific Publishing,2020:250-261.
[13]	GARCIA D M,BAEK D,SHIN C,et al.Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs[J].Nat Struct Mol Biol,2011,18(10):1139-1146.
[14]	FIGLIUZZI M,MARINARI E,DE MARTINO A.MicroRNAs as a selective channel of communication between competing RNAs:a steady-state theory[J].Biophys J,2013,104(5):1203-1213.
[15]	LI Y,ZHENG Q P,BAO C Y,et al.Circular RNA is enriched and stable in exosomes:A promising biomarker for cancer diagnosis[J].Cell Res,2015,25(8):981-984.
[16]	EBERT M S,SHARP P A.Emerging roles for natural microRNA sponges[J].Curr Biol,2010,20(19):R858-R861.
[17]	DENZLER R,AGARWAL V,STEFANO J,et al.Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance[J].Mol cell,2014,54(5):766-776.
[18]	BOSSON A D,ZAMUDIO J R,SHARP P A.Endogenous miRNA and target concentrations determine susceptibility to potential ceRNA competition[J].Mol Cell,2014,56(3):347-359.
[19]	QI X L,ZHANG D H,WU N,et al.CeRNA in cancer:Possible functions and clinical implications[J].J Med Genet,2015,52(10):710-718.
[20]	TAN C,LIU S,TAN S K,et al.Polymorphisms in microRNA target sites of forkhead box O genes are associated with hepatocellular carcinoma[J].PLoS One,2015,10(3):e0119210.
[21]	GRIMSON A,FARH K K H,JOHNSTON W K,et al.MicroRNA targeting specificity in mammals:Determinants beyond seed pairing[J].Mol Cell,2007,27(1):91-105.
[22]	EBERT M S,SHARP P A.MicroRNA sponges:progress and possibilities[J].RNA,2010,16(11):2043-2050.
[23]	RYBAK-WOLF A,STOTTMEISTER C,GLAŽAR P,et al.Circular RNAs in the mammalian brain are highly abundant,conserved,and dynamically expressed[J].Mol Cell,2015,58(5):870-885.
[24]	HANSEN T B,JENSEN T I,CLAUSEN B H,et al.Natural RNA circles function as efficient microRNA sponges[J].Nature,2013,495(7441):384-388.
[25]	ZHANG P P,CHAO Z,ZHANG R,et al.Circular RNA regulation of myogenesis[J].Cells,2019,8(8):885.
[26]	ZHOU Z Y,LI K Y,LIU J N,et al.Expression profile analysis to identify circular RNA expression signatures in muscle development of Wu'an goat Longissimus dorsi tissues[J].Front Vet Sci,2022,9:833946.
[27]	LIU R L,LIU X X,BAI X J,et al.Identification and characterization of circRNA in Longissimus dorsi of different breeds of cattle[J].Front Genet,2020,11:565085.
[28]	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.
[29]	QI A,RU W X,YANG H Y,et al.Circular RNA ACTA1 acts as a sponge for miR-199a-5p and miR-433 to regulate bovine myoblast development through the MAP3K11/MAP2k7/JNK pathway[J].J Agric Food Chem,2022,70(10):3357-3373.
[30]	ZHANG R M,PAN Y,ZOU C X,et al.CircUBE2Q2 promotes differentiation of cattle muscle stem cells and is a potential regulatory molecule of skeletal muscle development[J].BMC Genomics,2022,23(1):267.
[31]	LI H,YANG J M,WEI X F,et al.CircFUT10 reduces proliferation and facilitates differentiation of myoblasts by sponging miR-133a[J].J Cell Physiol,2018,233(6):4643-4651.
[32]	RU W X,QI A,SHEN X M,et al.The circular RNA circCPE regulates myoblast development by sponging miR-138[J].J Anim Sci Biotechnol,2021,12(1):102.
[33]	WANG X G,CAO X K,DONG D,et al.Circular RNA TTN acts as a miR-432 sponge to facilitate proliferation and differentiation of myoblasts via the IGF2/PI3K/AKT signaling pathway[J].Mol Ther Nucleic Acids,2019,18:966-980.
[34]	YUE B L,WANG J,RU W X,et al.The circular RNA circHUWE1 sponges the miR-29b-AKT3 axis to regulate myoblast development[J].Mol Ther Nucleic Acids,2020,19:1086-1097.
[35]	SHEN X M,TANG J,RU W X,et al.CircINSR regulates fetal bovine muscle and fat development[J].Front Cell Dev Biol,2021,8:615638.
[36]	SHEN X M,ZHANG X Y,RU W X,et al.circINSR promotes proliferation and reduces apoptosis of embryonic myoblasts by sponging miR-34a[J].Mol Ther Nucleic Acids,2020,19:986-999.
[37]	OUYANG H J,CHEN X L,LI W M,et al.Circular RNA circSVIL promotes myoblast proliferation and differentiation by sponging miR-203 in chicken[J].Front Genet,2018,9:172.
[38]	CHEN B,YU J,GUO L J,et al.Circular RNA circHIPK3 promotes the proliferation and differentiation of chicken myoblast cells by sponging miR-30a-3p[J].Cells,2019,8(2):177.
[39]	ZHAO J,ZHAO X Y,SHEN X X,et al.CircCCDC91 regulates chicken skeletal muscle development by sponging miR-15 family via activating IGF1-PI3K/AKT signaling pathway[J].Poult Sci,2022,101(5):101803.
[40]	SHEN X M,TANG J,JIANG R,et al.CircRILPL1 promotes muscle proliferation and differentiation via binding miR-145 to activate IGF1R/PI3K/AKT pathway[J].Cell Death Dis,2021,12(2):142.
[41]	CAI B L,MA M T,ZHOU Z,et al.CircPTPN4 regulates myogenesis via the miR-499-3p/NAMPT axis[J].J Anim Sci Biotechnol,2022,13(1):2.
[42]	WANG Z J,ZHANG M,LI K,et al.CircMGA depresses myoblast proliferation and promotes myotube formation through miR-144-5p/FAP signal[J].Animals (Basel),2022,12(7):873.
[43]	LI K,HUANG W C,WANG Z J,et al.CircTAF8 regulates myoblast development and associated carcass traits in chicken[J].Front Genet,2022,12:743757.
[44]	KYEI B,ODAME E,LI L,et al.Knockdown of CDR1as decreases differentiation of goat skeletal muscle satellite cells via upregulating mir-27a-3p to inhibit ANGPT1[J].Genes (Basel),2022,13(4):663.
[45]	ZHANG Z, FAN Y, DENG K, et al. Circular RNA circUSP13 sponges miR-29c to promote differentiation and inhibit apoptosis of goat myoblasts by targeting IGF1[J]. Faseb,2022,36(1):e22097.
[46]	CAO H G,LIU J M,DU T N,et al.Circular RNA screening identifies circMYLK4 as a regulator of fast/slow myofibers in porcine skeletal muscles[J].Mol Genet Genomics,2022,297(1):87-99.
[47]	JIN L,TANG Q Z,HU S L,et al.A pig bodymap transcriptome reveals diverse tissue physiologies and evolutionary dynamics of transcription[J].Nat Commun,2021,12(1):3715.
[48]	HUANG J P,ZHAO J H,ZHENG Q Z,et al.Characterization of circular RNAs in Chinese buffalo (Bubalus bubalis) adipose tissue:A focus on circular RNAs involved in fat deposition[J].Animals (Basel),2019,9(7):403.
[49]	WU J Y,ZHANG S L,YUE B L,et al.CircRNA profiling reveals circPPARγ modulates adipogenic differentiation via sponging miR-92a-3p[J].J Agric Food Chem,2022,70(22):6698-6708.
[50]	LI B J,HE Y,WU W J,et al.Circular RNA profiling identifies novel circPPARA that promotes intramuscular fat deposition in pigs[J].J Agric Food Chem,2022,70(13):4123-4137.
[51]	JIANG R,LI H,YANG J M,et al.CircRNA profiling reveals an abundant circFUT10 that promotes adipocyte proliferation and inhibits adipocyte differentiation via sponging let-7[J].Mol Ther Nucleic Acids,2020,20:491-501.
[52]	ZHANG P P,HAN Q,SHENG M X,et al.Identification of circular RNA expression profiles in white adipocytes and their roles in Adipogenesis[J].Front Physiol,2021,12:728208.
[53]	WANG L D,LIANG W S,WANG S S,et al.Circular RNA expression profiling reveals that circ-PLXNA1 functions in duck adipocyte differentiation[J].PLoS One,2020,15(7):e0236069.
[54]	HAO Z Y,ZHOU H T,HICKFORD J G H,et al.Identification and characterization of circular RNA in lactating mammary glands from two breeds of sheep with different milk production profiles using RNA-seq[J].Genomics,2020,112(3):2186-2193.
[55]	WANG J Q,ZHOU H T,HICKFORD J G H,et al.Identification and characterization of circular RNAs in mammary gland tissue from sheep at peak lactation and during the nonlactating period[J].J Dairy Sci,2021,104(2):2396-2409.
[56]	WANG D Y,CHEN Z J,ZHUANG X N,et al.Identification of circRNA-associated-ceRNA networks involved in milk fat metabolism under heat stress[J].Int J Mol Sci,2020,21(11):4162.
[57]	ZHANG M,MA L,LIU Y H,et al.CircRNA-006258 sponge-adsorbs miR-574-5p to regulate cell growth and milk synthesis via EVI5l in goat mammary epithelial cells[J].Genes (Basel),2020,11(7):718.
[58]	WANG D Y,ZHAO Z J,SHI Y R,et al.CircEZH2 regulates milk fat metabolism through miR-378b sponge activity[J].Animals (Basel),2022,12(6):718.
[59]	CLIFFORD R L,SINGER C A,JOHN A E.Epigenetics and miRNA emerge as key regulators of smooth muscle cell phenotype and function[J].Pulm Pharmacol Ther,2013,26(1):75-85.
[60]	LIU Y F,ZHOU Z Y,HE X Y,et al.Differentially expressed circular RNA profile signatures identified in prolificacy trait of Yunshang black goat ovary at estrus cycle[J].Front Physiol,2022,13:820459.
[61]	MA L,ZHANG M,CAO F J,et al.Effect of MiR-100-5p on proliferation and apoptosis of goat endometrial stromal cell in vitro and embryo implantation in vivo[J].J Cell Mol Med,2022,26(9):2543-2556.
[62]	LIU X R,ZHANG L,YANG L C,et al.miR-34a/c induce caprine endometrial epithelial cell apoptosis by regulating circ-8073/CEP55 via the RAS/RAF/MEK/ERK and PI3K/AKT/mTOR pathways[J].J Cell Physiol,2020,235(12):10051-10067.
[63]	LI X Y,GAO F L,FAN Y S,et al.A novel identified circ-ANKHD1 targets the miR-27a-3p/SFRP1 signaling pathway and modulates the apoptosis of granulosa cells[J].Environ Sci Pollut Res Int,2021,28(41):57459-57469.
[64]	GUO T Y,ZHANG J B,YAO W,et al.CircINHA resists granulosa cell apoptosis by upregulating CTGF as a ceRNA of miR-10a-5p in pig ovarian follicles[J].Biochim Biophys Acta Gene Regul Mech,2019,1862(10):194420.
[65]	WU Y,XIAO H W,PI J S,et al.The circular RNA aplacirc_13267 upregulates duck granulosa cell apoptosis by the apla-miR-1-13/THBS1 signaling pathway[J].J Cell Physiol,2020,235(7-8):5750-5763.
[66]	WANG H M,ZHANG Y,ZHANG J B,et al.CircSLC41A1 resists porcine granulosa cell apoptosis and follicular atresia by promoting SRSF1 through miR-9820-5p sponging[J].Int J Mol Sci,2022,23(3):1509.
[67]	CAO Z B,GAO D,XU T T,et al.Circular RNA profiling in the oocyte and cumulus cells reveals that circARMC4 is essential for porcine oocyte maturation[J].Aging,2019,11(18):8015-8034.