Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (9): 1807-1819.doi: 10.3864/j.issn.0578-1752.2024.09.014

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Cloning and Identification of Differentially Expressed lncRNAs in Follicles of Meishan Pigs and Duroc Pigs with Their Correlation Analysis with miRNAs

ZHANG HuaPeng1(), ZHANG QingZe1, HE Fan1, QI MengFan1, FU BinBin1, LI QingChun1, LI MengXun1, MA LiPeng1, LIU Yi1, HUANG Tao1,2()   

  1. 1 College of Animal Science and Technology, Shihezi University, Shihezi 832000, Xinjiang
    2 Xinjiang Pig Seed Industry Engineering Technology Research Center, Changji 831100, Xinjiang
  • Received:2023-11-06 Accepted:2024-01-11 Online:2024-05-01 Published:2024-05-09
  • Contact: HUANG Tao

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Abstract:

【Objective】The objective of this study was to clone and identify the differentially expressed lncRNA-ALDBSSCT0000005583 in M2 follicles on the fourth day of follicular stage in Meishan pigs and Duroc pigs, and to analyze the correlation between the expression of miRNAs in porcine granulosa cells, so as to provide a theoretical basis for exploring the role of lncRNAs in the development of follicles in sows by regulating miRNAs. 【Method】Based on the differentially expressed lncRNA- ALDBSSCT0000005583 screened in Meishan and Duroc M2 follicles in our early research, the full-length sequence of ALDBSSCT0000005583 was verified by RT-qPCR and cloned by RACE; the coding ability of this lncRNA was predicted by the coding potential assessment tool of CAPT and CPC, which was further identified by the primary expression test; the coding ability of this lncRNA was identified by the primary expression test; the subcellular coding ability of NA-ALDBSSCT0000005583 was identified by the nucleoplasmic separation experiment and tested to identify its coding ability; the subcellular localization of lncRNA-ALDBSSCT0000005583 by nucleoplasmic isolation assay and its expression level in various tissues were detected by RT-qPCR; miRBase website was used to locate the miRNA database of pigs, and the combination of RNAhybrid and miRanda online software was used to predicte the relationship with the lncRNA-ALDBSSCT0000005583. The inter-species conserved miRNAs that interacted with lncRNA-ALDBSSCT0000005583 were predicted by TargetScan and miRanda, the target genes that interacted with lncRNA-ALDBSSCT0000005583 were predicted by TargetScan and miRanda, and their target genes were subjected to GO enrichment and KEGG signaling pathway analyses; the effects of target genes on miRNA expression were verified by overexpression as well as interference with lncRNA. 【Result】The expression level of lncRNA-ALDBSSCT0000005583 in M2 follicles of Duroc pigs was significantly higher than that in Meishan pigs, and the size of lncRNA 5′RACE and 3′RACE fragments was 569 bp and 546 bp, respectively, and the sequencing analysis showed that the size of lncRNA-ALDBSSCT0000005583 was 588 bp. Bioinformatics predicted that the encoding potential was low, and the results of prokaryotic expression assay further proved that it did not code for proteins. Tissue expression profiling showed that lncRNA-ALDBSSCT0000005583 was expressed in the adrenal gland, spleen, liver and ovaries, and low in the hypothalamus and heart, while the subcellular localization results showed that the lncRNA was mainly present in the cytoplasm. After bioinformatics analysis, a total of 9 conserved miRNAs were screened for potential interaction with lncRNA-ALDBSSCT0000005583, including two miRNAs related to ovarian development: miR-193a-5p and miR-361-3p. KEGG and GO enrichment analysis showed that the target genes of miR-193a-5p and miR-361-3p were related to phylogenetic processes and biological processes such as cell-to-cell signaling. It was also significantly involved in oxytocin, Ras, NF-κB gonadotropin- releasing hormone secretion and other pathways. Subsequently, lncRNA-ALDBSSCT0000005583 was overexpressed in granulosa cells, and the expressions of miR-193a-5p and miR-361-3p were significantly down-regulated by RT-qPCR (P<0.05), but there was no significant effect after interference with lncRNA-ALDBSSCT0000005583. 【Conclusion】 lncRNA-ALDBSSCT0000005583 was a lncRNA that did not have the ability to code for proteins. There was a significant difference in the expression level between the medium follicles of Meishan and Duroc pigs, and the expression level was higher in the adrenal glands, spleen, liver and ovaries, which is mainly found in the cytoplasm of granulosa cells, and might be involved in the development of porcine ovarian granulosa cells by interacting with miR-193a-5p and miR-361-3p.

Key words: lncRNA-ALDBSSCT0000005583, pig, follicle, granulosa cells, miR-193a-5p, miR-361-3p

Table 1

Primer sequences for RT-qPCR and vector construction"

基因名称 Gene name 引物序列Primer sequence（5′-3′） 用途 Usage
lncRNA-ALDBSSCT0000005583 DL-F:ACGTGTACAGGGCCTGACTCG RT-qPCR
DL-R:TTCTCGCATCCACGTACCTG
pcDNA3.1-lncRNA-5583 F:GG G AATTCGTAGTGACGCAGGCGCGAGACTG 载体构建
Vector construction
R:GGG CTCGAGCCAAATTTGAAACTGTTTTATTAAA
GAPDH F:AACATCATCCCTGCTTCTACCG RT-qPCR
R:GGTCAGATCCACAACCG
U6 F: CGCTTCGGCAGCACATATACTA RT-qPCR
R: ATGGAACGCTTCACGAATTTGC
miR-193a-5p F: AACAAGTGGGTCTTTGCGGGC RT-qPCR
miR-361-3p F:AACAAGCCCCCAGGTGTGATTCTG RT-qPCR
miRNAs通用引物
Universal primers for miRNAs		 R:AGTGCAGGGTCCGAGGTATT RT-qPCR
5′ RACE特异性引物
5′ RACE-specific primers		 GSP:GATTACGCCAAGCTTCCCACTTGTCATTCCGATGTCAGAGGGG RACE克隆
Rapid-amplification of cDNA ends clone
3′ RACE特异性引物
3′ RACE-specific primers		 GSP:GATTACGCCAAGCTTGCGGCTATCCAAGACCATTGAGGGTCC RACE克隆
Rapid-amplification of cDNA ends clone
通用引物（UPM）
Universal primers		 TAATACGACTCACTATAGGGCAAGCAGTGGTATCAACGCAGAGT RACE克隆
Rapid-amplification of cDNA ends clone
siRNA-lncRNA sense（5′-3′） CAGAUCUCCUGUAAGAUGUTT lncRNA干扰序列
lncRNA interference sequence
siRNA-lncRNA antisense（5′-3′） ACAUCUUACAGGAGAUCUGTT

Fig. 1

Expression of lncRNA-ALDBSSCT0000005583 in M2 follicles in Meishan pigs and Duroc pigs A: Next-generation sequencing results ALDBSSCT0000005583 expression level in M2 follicles; B: RT-qPCR to verify the expression level of ALDBSSCT0000005583"

Fig. 2

Splicing sequence characteristics of lncRNA-ALDBSSCT0000005583 A: 3' RACE representative images and Sanger DNA sequencing; B: 5' RACE representative images and Sanger DNA sequencing; C:lncRNA- ALDBSSCT0000005583 full-length RNA sequence"

Table 2

The CPAT website predicted the results of the coding potential"

基因名称
Gene name		 编码/非编码
Encoding/Non-coding		 编码潜能
Coding potential
lncRNA-ALDBSSCT0000005583 非编码Non-coding 0.0122981
HG19 编码 Encoding 0.9998311
HOTAIR 非编码Non-coding 0.1257913

Table 3

The CPC website predicted the results of the coding potential"

基因名称
Gene name		 编码/非编码
Encoding/Non-coding		 编码潜能
Coding potential
lncRNA-ALDBSSCT0000005583 非编码Non-coding 0.01716
HG19 编码Encoding 0.99987
HOTAIR 非编码Non-coding 0.18488

Fig. 3

Construction of prokaryotic expression vector and analysis of SDS-PAGE electrophoresis A: lncRNA-full-length amplification and ligation to the pET-28a(+) vector Sanger DNA sequencing ALDBSSCT0000005583; B: pET-28a-YY1 double digestion results and Sanger DNA sequencing; C: SDS-PAGE electrophoresis analysis"

Fig. 4

Identification of granulosa cells"

Fig. 5

lncRNA-ALDBSSCT0000005583 subcellular localization"

Fig. 6

Expression of lncRNA-ALDBSSCT0000005583 in different tissues of Duroc pigs"

Fig. 7

RNAhybrid and miRanda predict miRNA targeting lncRNA-ALDBSSCT0000005583"

Fig. 8

lncRNA-miRNA-mRNA network construction"

Table 4

GO-enrichment entries for miRNAs target genes that interacted with lncRNA-ALDBSSCT0000005583"

GO条目 GO term 基因数目 Gene count 富集倍数 Fold enrichment P值 P value
系统进程System process 13 1.90 0.018140
细胞酰胺代谢过程Cellular amide metabolic process 11 1.91 0.027469
有机氮化合物分解代谢过程Organonitrogen compound catabolic process 11 1.86 0.033325
细胞-细胞信号转导Cell-cell signaling 11 1.74 0.048981
神经系统过程Nervous system process 8 2.15 0.032080
循环系统过程Circulatory system process 7 3.62 0.003088
细胞因子产生Cytokine production 7 2.17 0.041634
硫化合物代谢过程Sulfur compound metabolic process 6 4.46 0.002150
血液循环Blood circulation 6 3.25 0.010149
系统过程调节Regulation of system process 6 2.84 0.018724

Table 5

Signaling pathways of miRNAs target genes interacting with lncRNA-ALDBSSCT0000005583"

信号通路条目 Pathway term 基因数目 Gene count 富集倍数 Fold enrichment P值 P value
多巴胺能突触Dopaminergic synapse 6 3.77 0.00510
Ras信号通路Ras signaling pathway 8 2.76 0.00841
钙信号通路Calcium signaling pathway 8 2.68 0.00993
酪氨酸代谢Tyrosine metabolism 3 6.63 0.01022
嘌呤代谢Purine metabolism 5 3.17 0.02076
肥厚型心肌病Hypertrophic cardiomyopathy 4 3.63 0.02423
催产素信号通路Oxytocin signaling pathway 5 2.76 0.03482
心肌细胞中的肾上腺素能信号转导Adrenergic signaling in cardiomyocytes 5 2.74 0.03569
NF-κB信号通路NF-kappa B signaling pathway 4 3.06 0.04188
促性腺激素释放激素分泌GnRH secretion 3 3.83 0.04330

Fig. 9

Efficiency of RT-qPCR in detecting overexpressed/interfering lncRNA-ALDBSSCT0000005583 and its effect on miRNAs A. Overexpression lncRNA-ALDBSSCT0000005583 efficiency detection; B. siRNA- ALDBSSCT0000005583 efficiency assay; C. Effect of overexpression of lncRNA-ALDBSSCT0000005583 on miR-193a-5p; D. Effect of overexpression of lncRNA-ALDBSSCT0000005583 on miR-193a-5p; E. Effect of interfering lncRNA-ALDBSSCT0000005583 on miR-361-3p; F. Effect of interfering lncRNA-ALDBSSCT0000005583 on miR-1361-3p"

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