感染大肠杆菌F17湖羊羔羊脾脏中差异circRNA分析

doi:10.3864/j.issn.0578-1752.2019.06.012

Abstract

Abstract:

【Background】Sheep colibacillosis is an acute infectious disease by E. coli that is characterized by severe diarrhea and sepsis, which is one of the most common bacterial diseases in large-scale sheep farms. Especially the newborn lamb is infected by enterotoxin-producing Escherichia coli (ETEC), causing lamb diarrhea, also known as lamb white diarrhea. Sheep colibacillosis let the farm to suffer serious economic losses, but the traditional antibiotic treatment program has many defects. 【Objective】In this study, we obtained oral diarrhea and diarrhea lambs by oral administration of E. coli F17 strain, and screened out circRNAs that were differentially expressed in individuals with diarrhea and diarrhea after taking E. coli F17 pili, and then explored circRNA for sheep in anti-diarrhea to find candidate genes associated with resistance to E. coli disease traits. From the circRNA level, the understanding of sheep antagonizing E. coli F17 fimbriae was deepened, and the functional genes of sheep antagonizing E. coli F17 fimbriae were determined.【Method】We used CIRI software to predict circRNA from scratch, and firstly screened differentially expressed (DE) circRNA in spleen of Escherichia coli F17 fimbriae without diarrhea and diarrhea by using RNA-seq technology. Then we performed GO on differentially expressed transcripts, and its function was described in combination with GO annotation results. The number of differential transcripts included in each GO entry was counted and the significance of differential transcript enrichment in each GO entry was calculated by using Fisher's exact test. Then, 6 DE circRNAs were randomly selected, and the relative expression levels of the 6 DE circRNAs in the spleen of lambs without diarrhea and diarrhea were verified by q-PCR, and the miRNAs and miRNA target genes were predicted by Miranda software. The function of this part of circRNA was elucidated based on the functional annotation of the miRNA target gene, and the circRNA-miRNA-mRNA interaction was analyzed. Finally, the relative expression level of mRNA in the non-diarrhea group and the diarrhea group lamb was verified by q-PCR.【Result】After mapping the reference sequence, we identified 7730 circRNAs, and DE circRNA was compared with the GO database. A total of 60 circRNAs were annotated and classified into 297 functional subclasses. Using RNA-seq to screen 60 DE circRNAs in spleens of diarrhea-free and diarrhea lambs, 31 of which were up-regulated, and 29 of which were down-regulated. Relative expression levels of randomly selected 6 DE circRNAs in non-diarrhea and diarrhea lambs by q-PCR and found to be consistent with RNA-seq results. Using Miranda to analyze circRNA-miRNA-mRNA interactions, we found a certain target relationship between 6 circRNAs, 5 miRNAs and 8 mRNAs. q-PCR was used to verify the relative expression of mRNA in lambs without diarrhea and diarrhea, and the results were found to be consistent with RNA-seq results.【Conclusion】 This study explored the expression profile of circRNA in the spleen of lambs without diarrhea and diarrhea, and further understood its regulation in the process of disease resistance in sheep. The discovery of circRNA, which was differentially expressed in the spleen of lambs without diarrhea and diarrhea, could help to find out how the lambs resist the mechanism of diarrhea, and to provide a scientific basis for improving the lamb's ability to resist diarrhea.

Key words: Escherichia coli F17, circRNA, Lake sheep, circRNA-miRNA-mRNA interaction

ZOU ShuangXia,JIN ChengYan,BAO JianJun,WANG Yue,CHEN WeiHao,WU TianYi,WANG LiHong,LÜ XiaoYang,GAO Wen,WANG BuZhong,ZHU GuoQiang,DAI GuoJun,SHI DongFang,SUN Wei. Differential circRNA Analysis in the Spleen of Hu-sheep Lambs Infected with F17 Escherichia coli[J].Scientia Agricultura Sinica, 2019, 52(6): 1090-1101.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: https://www.chinaagrisci.com/EN/10.3864/j.issn.0578-1752.2019.06.012

https://www.chinaagrisci.com/EN/Y2019/V52/I6/1090

Figures/Tables 10

Table 1

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Fig. 6

Fig. 7

Fig. 8

Table 2

References 50

[1]	邓齐文, 许晔琼, 王书奎 . 长链非编码RNA 多态性与肿瘤相关性的研究. 医学研究生学报, 2014,27(3):303-306. doi: 10.3969/j.issn.1008-8199.2014.03.021
	DENG Q W, XU Y Q, WANG S K . Long-chain non-coding RNA polymorphism and tumor correlation study. Journal of Medical Postgraduate, 2014,27(3):303-306. (in Chinese) doi: 10.3969/j.issn.1008-8199.2014.03.021
[2]	SANGER H L, KLOTZ G, RIESNER D, GROSS H J, KLEISCHMIDT A K . VIROID are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proceedings of the National Academy of Sciences of the United States of America, 1976, 11:3852-3856. doi: 10.1073/pnas.73.11.3852 pmid: 1069269
[3]	MATSUMOTO Y, FISHEL R, WICKNER R . Circular single-stranded RNA replicon in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 1990, 87(19):7628-7632. doi: 10.1073/pnas.87.19.7628 pmid: 1699230
[4]	ARNBERG A C , VAN OMMEN G J B, GRIVELL L A, BRUGGEN E F J V, BORST P . Some yeast mitochondrial RNAs are circular. Cell, 1980,19(2):313-319. doi: 10.1016/0092-8674(80)90505-X pmid: 6986989
[5]	KOS A, DIJKEMA R, AMBERG A C, VAN P H, SCHELLEKENS H . The hepatitis delta (delta) virus possesses a circular RNA. Nature, 1986,323(6088):558-560. doi: 10.1038/323558a0
[6]	CAPEL B, SWAIN A, NICOLIS S, HACKER A, WALTER M, KOOPMAN P, GOODFELLOW P , LOVELL-badqeBADQE R. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell, 1993,7(5):1019-1030.
[7]	COCQUERELLE C, MASCREZ B, HETUIN D, BAILLEUL B . Mis-splicing yields circular RNA molecule. FASEB Journal, 1993,7(1):155-160. doi: 10.1006/excr.1993.1021 pmid: 7678559
[8]	LASDA E, PARKER R . Circular RNAs: diversity of form and function. RNA, 2014,20(12):1829-1842. doi: 10.1261/rna.047126.114 pmid: 25404635
[9]	SALZMAN J, GAWAD C, WANG P L, LACAYO N, BRWON P O . Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One, 2012,7(2):e30733. doi: 10.1371/journal.pone.0030733 pmid: 3270023
[10]	ASHWAL-FLUSS R, MEYER M, PAMUDURITI N R, LAVNOV A, BARTOK O. HANMAN M, EVANTAL N, MEMCZAK S, RAJEWSKY N , KADENER S . circRNA biogenesis competes with pre-mRNA splicing. Molecular Cell, 2014,56(1):55-66. doi: 10.1016/j.molcel.2014.08.019
[11]	STARKE S, JOST I, ROSSBACH O, SCHNEIDER T, SCHREINER S. HUNQ L H, BINDIREIF A . Exon circularization requires canonical splice signals. Cell Report, 2015,10(1):103-111. doi: 10.1016/j.celrep.2014.12.002 pmid: 25543144
[12]	徐兴文 . 羊大肠杆菌病防治. 中国畜禽种业, 2017,4:129-130. doi: 10.3969/j.issn.1673-4556.2017.04.109
	XU X W . Prevention and treatment of Escherichia Coli in sheep. China Animal and Poultry Industry, 2017,4:129-130. (in Chinese) doi: 10.3969/j.issn.1673-4556.2017.04.109
[13]	张文静 . 羊大肠杆菌病的防控措施. 畜牧兽医科技信息, 2017,6:76. doi: 10.3969/J.ISSN.1671-6027.2017.06.071
	ZHANG W J . Prevention and control measures for sheep colibacillosis. Herbivore, 2017,6:76. (in Chinese) doi: 10.3969/J.ISSN.1671-6027.2017.06.071
[14]	LEWIS S J, HEATON K W . Stool form as a useful guide to intestinal transit time. Scand J Gastroenterol. 1997,32:920-924.
[15]	P, G, P. P,and R. N, circBase: a database for circular RNAs. Rna-a Publication of the Rna Society, 2014. 20(11):1666-1670. doi: 10.1261/rna.043687.113
[16]	GAO Y, WANG J, ZHAO F , CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biology, 2015. 16:4. doi: 10.1186/s13059-014-0571-3 pmid: 25583365
[17]	ANDERS S. HUBER W . Differential expression of RNA-Seq data at the gene level - the DESeq package. European Molecular Biology Laboratory, 2013.
[18]	ROBINSON, M D, MCCARTHY D J , SMYTH G K . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 2010,26(1):139-140. doi: 10.1093/bioinformatics/btp616
[19]	KANEHISA M, ARAKI M, GOTO S, HATTORI M, HIRAKAWA M, ITOH M, KATAYAMA T, KAWASHIMA S, OKUDA S, TUKIMATSU T, YAMANISHI Y . KEGG for linking genomes to life and the environment. Nucleic Acids Research, 2008,36:480-484. doi: 10.1093/nar/gkm882 pmid: 2238879
[20]	JOHN B, ENRIGHT A J, ALEXIE A, THOMAS T, CHRIS S . Human MicroRNA targets. PLoS Biology, 2004. 2(11):e363. doi: 10.1371/journal.pbio.0020363
[21]	ENRIGH A, JOHN B, GAUL U, TUSCHL T, SANDER C, MARKS S . MicroRNA targets in Drosophila. Genome Biology, 2004,5(1):R1. doi: 10.1186/gb-2003-5-1-r1 pmid: 14709173
[22]	ABDELMOHSEN K, PANDA A C, DES, GRAMMITIKAKIS I, KIM J, DING J, NOH J H, KIM K M, MATTISON J A, DECABO R, COROSEP M . Circular RNAs in monkey muscle: age-dependent changes. Aging (Albany NY), 2015,7(11):903-910. doi: 10.18632/aging.100834 pmid: 26546448
[23]	BURD C E, JECK W R, LIU Y, SANOFF H K , WANG Z. SHARPLESS N E. Expression of linear and novel circular forms of an INK4/ARF-associated Non-coding RNA correlates with atherosclerosis Risk. PLoS Geneicst, 2010,6(12):e1001233. doi: 10.1371/journal.pgen.1001233 pmid: 2996334
[24]	SALZMAN J, CHEN R E, OLESN M N, WANG P L, BROWN P O . Cell-type specific features of circular RNA expression. PLoS Genetics, 2013,9(9):e1003777. doi: 10.1371/journal.pgen.1003777 pmid: 24039610
[25]	MEMCZAK S, JENS M, ELEFSINIOTI A, TORTI F, KRUEGER J, RYBAK A, MAIER L, MACKOWIAK S D, GREGEISEN L H, MUNSCHAUER M, LOERWER A, ZIEBOLD U, LANDTHALER M, KOCKS C, NOBEL F, RAJEWSKY N . Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013,495(7441):333-338. doi: 10.1038/nature11928
[26]	HANSEN T B, JENSEN T I, CLAUSEN B H, BRAMSEN J B, FINSEN B, DAMGAARD C K, KJEMS J . Natural RNA circles function as efficient microRNA sponges. Nature, 2013,495(7441):384-388. doi: 10.1038/nature11993 pmid: 23446346
[27]	ZHENG Q, BAO C, GUO W, LI S, CHEN J, CHEN B, LUO Y, LYU D, LI Y, SHI G, LIANG L, GU J, HE X, HUANG S . Circular RNA profiling reveals an abundant circHIPK3that regulates cell growth by sponging multiple miRNAs. Nature Communication, 2016,7:11215. doi: 10.1038/ncomms11215 pmid: 27050392
[28]	CHEN C Y, SARMOW P . Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science, 1995,268(5209):415-417. doi: 10.1126/science.7536344 pmid: 7536344
[29]	WANG Y, WANG Z . Efficient backsplicing produces translatable circular mRNAs. RNA, 2015,21(2):172-179. doi: 10.1261/rna.048272.114 pmid: 25449546
[30]	ZHANG Y, ZHANG X O, CHEN T, XIANG J F, XING Y H, YIN Q, ZHU S, YANG S, CHEN L L . Circular intronic long noncoding RNAs. Molecular Cell, 2013,51(6):792-806. doi: 10.1016/j.molcel.2013.08.017 pmid: 24035497
[31]	LI Z, HUANG C, BAO C, CHEN L, LIN M, WANG X, ZHONG G, YU B, HU W, DAI L, ZHU P, CHANG Z, WU Q, ZHAO Y, JIA Y, XU P, LIU P, SHAN G . Exon-intron circular RNAs regulate transcription in the nucleus. Nature Structural Molecular Biology, 2015,22(3):256-264. doi: 10.1038/nsmb.2959
[32]	LASDA E P, ARKER R . Circular RNAs: diversity of form and function. RNA, 2014,20(12):1829-1842. doi: 10.1261/rna.047126.114 pmid: 25404635
[33]	ASHWAL-FLUSS R, MEYER M, PAMUDURTI NR, LVANOV A, BARTOK O, HANAN M, EVANTAL N, MEMCZAK S, RAJEWSKY N , KADENER S . circRNA biogenesis competes with pre-mRNA splicing. Molecular Cell, 2014,56(1):55-66. doi: 10.1016/j.molcel.2014.08.019
[34]	YAMAZAKI T, GOYA I, GRAF D, CRAIG S, MARTIN-OROZCO N, DONG C . A Butyrophilin Family Member Critically Inhibits T Cell Activation. The Journal of Immunology, 2010,185(10):5907-5914. doi: 10.4049/jimmunol.1000835
[35]	NGUYEN T, LIU XK, ZHANG Y, DONG C . BTNL2, a butyrophilin-like molecule that functions to inhibit T cell activation. The Journal of Immunology, 2006,176:7354-7360. doi: 10.4049/jimmunol.176.12.7354 pmid: 1626526
[36]	ARNETT H A, ESCOBAR S S, GONZALEZSUAREZ E, BUDELSKY A L, STEFFEN L A, BOIABI N, ZHANG M, SIU G, BREWER A W, VINEY J L . BTNL2, a butyrophilin/B7-like molecule, is a negative costimulatory molecule modulated in intestinal inflammation. The Journal of Immunology, 2007,178:1523-1533. doi: 10.4049/jimmunol.178.3.1523 pmid: 17237401
[37]	SMITH I A, KNEZEVIC B R, AMMANN J U, RHODES D A, AW D, PALMER D B, MATHER I H, TROWSDALE J . BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T cell activation. The Journal of Immunology, 2010,184:3514-3525. doi: 10.4049/jimmunol.0900416 pmid: 20208008
[38]	BAS A, SWAMY M, ABELER-DORNER L, WILLIAMS G, PANG D J, BARBEE S D, HAYDAY A C, HAYDAY A C . Butyrophilin-like 1 encodes an enterocyte protein that selectively regulates functional interactions with T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(11):4376-4381. doi: 10.1073/pnas.1010647108
[39]	SHEPPERD J A, LIPKUS I M, SANDERSON S C, MCBRIDE C M , O’NEILL S C, DOCHERTY S . Testing different communication formats on responses to imagined risk of having versus missing the GSTM1 gene.Journal of Health Communication, 2013, 18:124-137. doi: 10.1080/10810730.2012.688245 pmid: 22888806
[40]	SINGH R, MANCHANDA P K, KESARWANI P, SRIVASTAVA A, MITTAL R D . Influence of genetic polymorphisms in GSTM1, GSTM3, GSTT1 and GSTP1 on allograft outcome in renal transplant recipients. Clinical Transplantation, 2009,23:490-498. doi: 10.1111/ctr.2009.23.issue-4
[41]	SOCHA A L, GUERINOT M L . Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Frontiers in Plant Science, 2014,5:106. doi: 10.3389/fpls.2014.00106 pmid: 3978347
[42]	MIYATA T, JADOUL M, KUROKAWA K, YDSC C , VAN . beta-2 microglobulin in renal disease. Journal of the American Society of Nephrology, 1998 (9):1723-1735. doi: 10.1038/sj.ijir.3900333 pmid: 9727382
[43]	WALLGREN-PETTERSSON C, SSEWRY C A, NONWAK K J, LAING N G , Nemaline myopathies. Semin. Pediatric Neurology, 2011,18(4):230-238. doi: 10.1016/j.spen.2011.10.004 pmid: 22172418
[44]	KUMAR S, KAO W H , HOWLEY P M. Physical interaction between specific E2 and Hect E3 enzymes determines functional cooperativity. Journal of Biology. Chemistry, 1997,272:13548-13554. doi: 10.1074/jbc.272.21.13548 pmid: 9153201
[45]	HAMANN J, AUGST G, ARAC D, ENGLE F B, FORMSTON C . International union of basic and clinical pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol Reviews, 2015; 67(2):338-367. doi: 10.1124/pr.114.009647 pmid: 25713288
[46]	VILBOUX T, MALICDAN M C, CHANG Y M, GUO J, ZERFAS P M, STEPHEN J, CULLINANE A R, BYANT J, FISHER R, BROOKS B P, ZEIN W M, WIGGS E A, ZELEWSKI C K, PORETTI A, BRYAN M M, VEMULAPALLI M, MULLIKIN J C, KIRBY M, ANDERSON S M, HUIZING M, TORO C, GAHL W A, GUNAY- AYQUN M . Cystic cerebellar dysplasia and biallelic LAMA1 mutations: a lamininopathy associated with tics, obsessive compulsive traits and myopia due to cell adhesion and migration defects. Cognitive and Behavioural Genetics, 2016,53(5):318-329.
[47]	FELIPE L O , JUNIOR W F D S, ARAUJO K C, FABRINO D L . Lactoferrin, chitosan and Melaleuca alternifolia-natural products that show promise in candidiasis treatment. Brazilian Journal Microbiology, 2017,49(2):212-219. doi: 10.1016/j.bjm.2017.05.008 pmid: 29132828
[48]	HASSANI Z, SALEH A, TURPAULT S, KHIATI S, MORELLE W, VIQNON J, HUQNOT J P, URO-COSTE E, LEQRAND P, DELAFORGE M, LOISEAU S, CLARION L, LECOUVEY M, VOLLE J N, VIRIEUX D, IRAT J L, DUFFAU H, BAKALARA N . Phostine PST3. 1a Targets MGAT5 and inhibits glioblastoma- initiating cell invasiveness and proliferation. Molecular Cancer Research, 2017,15(10):1376-1387. doi: 10.1158/1541-7786.MCR-17-0120
[49]	DEBRAND E, ELJAI Y, SPENCE L, BATE N, PRAEKELT U, PRITCHARD C A, MONKLEY S J, CRITCHLEY D R . Talin 2 is a large and complex gene encoding multiple transcripts and protein isoforms. FEBS Journal, 2009,276(6):1610-1628. doi: 10.1111/j.1742-4658.2009.06893.x pmid: 19220457
[50]	PORCELLI V, FIERMONTE G, LONGO A, PALMIERI F . The human gene SLC25A29, of solute carrier family 25, encodes a mitochondrial transporter of basic amino acids. Journal of Bioogylogy Chemistry, 2014,289(19):13374-13384. doi: 10.1074/jbc.M114.547448 pmid: 24652292

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Comments

Recommended 0

No Suggested Reading articles found!

	基因符号Gene symbol	引物序列Primer sequence	产物长度Length of product (bp)
差异表达的环状RNA的引物 Primers of DE circRNA	circRNA_2125	F:ATTGAATCACTTCTCTGTTGC	129
	circRNA_2125	R:TAGGTGCTCAAAATAGGAC	129
	circRNA_3832	F:AGCCTCTCATCTGTACAC	134
	circRNA_3832	R:CAGTAACTGCCTAGAGCA	134
	circRNA_7711	F:ACAAAGATTCCATTGACAG	101
	circRNA_7711	R:ACCAAGAGGCTAGCAAGAC	101
	circRNA_6710	F:CAGATTACAGCTATGGCGA	124
	circRNA_6710	R:CCCTCATGATCTCATAGG	124
	circRNA_6914	F:TTGGCTGTTACTATCATGAG	124
	circRNA_6914	R:CTGAACTCTTAACTTGCA	124
	circRNA_4030	F:TGATGCAGATATTAAACCTC	133
	circRNA_4030	R:CCAATCTCGGATAACTTCAC	133
差异表达的信使RNA的引物 Primers of DE mRNA	NEB	F:ATTACAGCTATCCACCCGAC	149
	NEB	R:TGCCTTTTCCATTTCTAAG	149
	UBE3B	F:TAAGATTGCCAGGAAACTGC	133
	UBE3B	R:AGCCAGGGACACGTACCAC	133
	ADGRF2	F:GGCGTTTACCTCTTTCTCG	103
	ADGRF2	R:CAAGCTGCAAATAGAAAC	103
	LAMA1	F:AAATGATCGAAAAGGCTAC	127
	LAMA1	R:AACCGCCTTTTCCGTAGGAC	127
	LTF	F:GAAAAGCGTATCCCAACCTG	103
	LTF	R:TTGAAGGCACCAGAATAAC	103
	MGAT5	F:CATCATCCACACCTACACG	111
	MGAT5	R:AACTGCAAGTCTCGTCCGC	111
	TLN2	F:ACGACGGTGGTTAAATAC	125
	TLN2	R:AGTTGCCCATAGTCACTGGTC	125
	ARHGAP30	F:TCTTCAACCTGGGTCGCTC	159
	ARHGAP30	R:GCAGCCCCTCTGGTTCATC	159
	SLC25A29	F:GCGTCCTGGCTCTCCACCT	125
	SLC25A29	R:CCCTGCCTCCCCGCGCTC	125
GAPDH引物 Primers of GAPDH	GAPDH-F	F:GTTCCACGGCACAGTCAAGG	127
GAPDH引物 Primers of GAPDH	GAPDH-F	R:ACTCAGCACCAGCATCACCC	127

环状RNA circRNA	最佳circRNA基因 Best gene of circRNA	P值 P vale	微小RNA miRNA	微小RNA的靶基因 Target gene of miRNA	靶标基因转录ID Transcription ID of target gene
circRNA_6577	LOC101111058 (Btnl 1)	0.000190825	oar-miR-381-5p
circRNA_7725		0.003873598	oar-miR-1193-5p	NEB	XM_012137591.2
				UBE3B	XM_004017436.3
circRNA_0309	LOC101108092 (GSTM1)	0.004205007	oar-miR-370-3p	ADGRF2	XM_004018870.3
circRNA_2125	LOC101115614 (NRAMP2)	0.004205007	oar-miR-370-3p	LAMA1	XM_012103553.2
circRNA_3832	B2M	0.004205007	oar-miR-370-3p	LTF	NM_001024862.1
circRNA_6577	LOC101111058 (Btnl 1)	0.004205007	oar-miR-370-3p	MGAT5	XM_012139230.2
circRNA_7711		0.004205007	oar-miR-370-3p	TLN2	XM_012181407.2
circRNA_6577	LOC101111058 (Btnl 1)	0.006550584	oar-miR-3956-3p	SLC25A29	XM_015102051.1
circRNA_6577	LOC101111058 (Btnl 1)	0.011765813	oar-miR-370-5p

Differential circRNA Analysis in the Spleen of Hu-sheep Lambs Infected with F17 Escherichia coli

RichHTML

PDF

Abstract

Cite this article

share this article

Figures/Tables 10

References 50

Related Articles 5

Metrics

Comments

Recommended 0

[1]	WU Yan,ZHANG Hao,LIANG ZhenHua,PAN AiLuan,SHEN Jie,PU YueJin,HUANG Tao,PI JinSong,DU JinPing. circ-13267 Regulates Egg Duck Granulosa Cells Apoptosis Through Let-7-19/ERBB4 Pathway [J]. Scientia Agricultura Sinica, 2022, 55(8): 1657-1666.
[2]	MA MengNan,WANG HuiMing,WANG MiaoMiao,YAO Wang,ZHANG JinBi,PAN ZengXiang. Identification of circINHBB During Follicular Atresia and Its Effect on Granulosa Cell Apoptosis [J]. Scientia Agricultura Sinica, 2021, 54(18): 3998-4007.
[3]	SHI TianPei,WANG XinYue,HOU HaoBin,ZHAO ZhiDa,SHANG MingYu,ZHANG Li. Analysis and Identification of circRNAs of Skeletal Muscle at Different Stages of Sheep Embryos Based on Whole Transcriptome Sequencing [J]. Scientia Agricultura Sinica, 2020, 53(3): 642-657.
[4]	DU Yu,FAN XiaoXue,JIANG HaiBin,WANG Jie,FAN YuanChan,ZHU ZhiWei,ZHOU DingDing,WAN JieQi,LU JiaXuan,XIONG CuiLing,ZHENG YanZhen,CHEN DaFu,GUO Rui. The Potential Role of MicroRNAs and MicroRNA-Mediated Competing Endogenous Networks During the Developmental Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2020, 53(12): 2512-2526.
[5]	GUO Rui,CHEN HuaZhi,XIONG CuiLing,ZHENG YanZhen,FU ZhongMin,XU GuoJun,DU Yu,WANG HaiPeng,GENG SiHai,ZHOU DingDing,LIU SiYa,CHEN DaFu. Analysis of Differentially Expressed Circular RNAs and Their Regulation Networks During the Developmental Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2018, 51(23): 4575-4590.