高通量环状RNA测序揭示hsa_circ_0001900在肾母细胞瘤中特异性高表达且与不良预后相关

doi:10.12122/j.issn.1673-4254.2025.11.19

南方医科大学学报 ›› 2025, Vol. 45 ›› Issue (11): 2466-2474.doi: 10.12122/j.issn.1673-4254.2025.11.19

高通量环状RNA测序揭示hsa_circ_0001900在肾母细胞瘤中特异性高表达且与不良预后相关

高志强(), 林洁, 洪鹏, 胡再宏, 崔孔孔, 王语, 董军君, 石秦林, 田小毛(), 魏光辉

重庆医科大学附属儿童医院泌尿外科，国家儿童健康与疾病临床医学研究中心//儿童发育疾病研究教育部重点实验室//结构性出生缺陷与器官修复重建重庆市重点实验室，重庆 400014

收稿日期:2024-05-19 出版日期:2025-11-20 发布日期:2025-11-28
通讯作者: 田小毛 E-mail:1815234622@qq.com;xiao-mao@ hospital.cqmu.edu.cn
作者简介:高志强，硕士，E-mail：1815234622@qq.com
基金资助:
国家自然科学基金青年项目(82403383);中国博士后科学基金(2024M753886);重庆市自然科学基金面上项目(CSTB2025NSCQ-GPX1154);重庆市博士后研究项目特别资助(2412013582995479)

High-throughput circular RNA sequencing reveals tumor-specific high expression of hsa_circ_0001900 in Wilms tumor in association with poor prognosis

Zhiqiang GAO(), Jie LIN, Peng HONG, Zaihong HU, Kongkong CUI, Yu WANG, Junjun DONG, Qinlin SHI, Xiaomao TIAN(), Guanghui WEI

Department of Urological Surgery, Children's Hospital of Chongqing Medical University, National Clinical Research Center for Child Health and Disorders, Ministry of Education Key Laboratory of Child Development and Disorders, Chongqing Key Laboratory of Structural Birth Defect and Organ Reconstruction, Chongqing 400014, China

Received:2024-05-19 Online:2025-11-20 Published:2025-11-28
Contact: Xiaomao TIAN E-mail:1815234622@qq.com;xiao-mao@ hospital.cqmu.edu.cn
Supported by:
Youth Program of National Natural Science Foundation of China(82403383)

摘要/Abstract

摘要：

目的探究环状RNA表达谱及其在肾母细胞瘤（WT）预后和进展中的潜在作用。方法搜集4对配对WT组织送环状RNA测序，筛选差异表达环状RNA。使用qPCR对表达水平最高的前6个候选环状RNA进行临床样本表达验证。选择有代表性的环状RNA在较大临床队列中分析其与临床病理特征和预后的相关性。最后，使用Sanger测序和RNase R酶消化实验验证该分子的成环位点和结构稳定性。结果基于高通量环状RNA测序在WT中鉴定到23，978个环状RNA分子，其中10，884个环状RNA已获得注释。根据筛选参数（|log2FC|>2和P值<0.05），去除表达丰度较低的样本，鉴定出614个差异表达的环状RNA分子，其中包括269个上调和345个下调。基于临床样本表达验证hsa_circ_0001900表达丰度最高与临床来源的肿瘤组织中和测序结果表达趋势一致，诊断ROC曲线显示该分子具有良好的鉴别诊断能力（曲线下面积为0.72）。临床相关性分析提示其表达水平与WT体积呈正相关（R=0.35，P=0.040），同时高表达组患儿的无复发生存率（RFS）具有明显降低的趋势（4年无复发生存率分别为81.25% vs 85.11%，P=0.496）。最后，本研究设计针对“反向剪接”位点的发散引物，该分子的成环剪接位点序列得到Sanger测序的验证，Rnase R酶消化实验进一步证实该分子的稳定共价结构。结论本研究首次展示WT中环状RNA的全面表达谱，其中hsa_circ_0001900的表达水平与WT肿瘤大小和患儿预后有关，可能是WT进展的关键驱动基因。

关键词: 肾母细胞瘤, Wilms Tumor, 环状RNA, hsa_circ_0001900

Abstract:

Objective To explore the expression profile of circular RNAs (circRNAs) and their potential roles in prognosis and progression of Wilms' tumor (WT). Methods Four pairs of WT and adjacent tissues were collected for high-throughput circRNA sequencing to identify the differentially expressed circular RNAs. RT-qPCR was used to verify the expression levels of the top 6 candidate circRNAs in the clinical samples. hsa_circ_0001900 was selected for analysis of its correlation with clinicopathological features and prognosis in 34 patients with WT. Sanger sequencing and RNase R digestion experiments were used to verify the cycling site and structural stability of hsa_circ_0001900 molecule. Results A total of 23 978 circular RNA molecules were identified in WT tissues by high-throughput circular RNA sequencing, and among them 614 were differentially expressed in WT. hsa_circ_0001900 showed the highest expression level among the differentially expressed circRNAs, which was consistent with the findings in clinical tumor samples and the sequencing results. Correlation analysis showed that hsa_circ_0001900 expression level was positively correlated with WT volume, and the children with high hsa_circ_0001900 expression had a lowered recurrence-free survival rate. The results of Sanger sequencing verified the circular splice site sequence of the molecule, and Rnase R digestion assay confirmed its stable covalent structure. Conclusion This study presents a comprehensive expression profile of circular RNAs in WT, and the expression level of hsa_circ_0001900 is related to the size of WT and the patients' prognosis, suggesting its possible role as a key driving gene in WT progression.

Key words: nephroblastoma, Wilms tumor, circular RNA, hsa_circ_0001900

高志强, 林洁, 洪鹏, 胡再宏, 崔孔孔, 王语, 董军君, 石秦林, 田小毛, 魏光辉. 高通量环状RNA测序揭示hsa_circ_0001900在肾母细胞瘤中特异性高表达且与不良预后相关[J]. 南方医科大学学报, 2025, 45(11): 2466-2474.

Zhiqiang GAO, Jie LIN, Peng HONG, Zaihong HU, Kongkong CUI, Yu WANG, Junjun DONG, Qinlin SHI, Xiaomao TIAN, Guanghui WEI. High-throughput circular RNA sequencing reveals tumor-specific high expression of hsa_circ_0001900 in Wilms tumor in association with poor prognosis[J]. Journal of Southern Medical University, 2025, 45(11): 2466-2474.

图/表 9

表1 测序结果质控表

Tab.1 Quality control for sequencing results

Samples	Output of data (Gb)	Q30 (%)
Tumor tissue-1	15.060	88.84
Tumor tissue-2	13.910	88.83
Tumor tissue-3	14.581	89.52
Tumor tissue-4	13.873	89.72
Adjacent control-1	13.325	90.70
Adjacent control-2	14.272	90.45
Adjacent control-3	15.289	90.44
Adjacent control-4	11.826	90.67

表2 基因q-PCR引物表

Tab.2 Primer sequences for q-PCR

Genes	Pre-primer (5'→3')	Post-primer (3'→5')
hsa_circ_0001900	CGTTCAGTGCCTCGAAAGAAC	CTGGTCCCCTTTCAGGATGAG
hsa_circ_0004425	AAGTGTGGACCCTGCAAATA	CCATTTGATCCACAGACAGGA
hsa_circ_0005230	CTCTTTGTTTTGCACACTAGGGA	ACCAGGTGAGCAGTCAAGAA
hsa_circ_0075828	GGAAGTGGCTAATGGATCTG	ATGGAGAACAGCCATCCATG
hsa_circ_0008122	TGTCTCAAAGCCAGACCTGAT	ATTCTGTTGTTCGGTGTCCAG
hsa_circ_0006151	GGCACCAGCATAGCCAGTAGT	GATGACCAGGCGCTTTTCACA
GAPDH	CCTTCCTGGGCATGGAGTC	TGATCTTCATTGTGCTGGGTG

图1 环状RNA的鉴定和注释

Fig.1 Identification and annotation of circRNAs A: Schematic diagram of Wilms tumor (WT) circular RNA sequencing analysis. B: Circos showing the full view of the circRNAs, with the outer circles representing chromosomes, the inner circles representing samples, and the red part of each sample representing "spliced" readings of the circRNAs. C: Venn diagram of circRNA sequencing data annotated with circBase database.

图2 环状RNA的分类和差异表达模式

Fig.2 Classification and differential expression patterns of circRNAs. A: Circular RNA classification. B: Principal component analysis (PCA). C: Volcano plot of the differentially expressed circRNAs. Red dots indicate upregulation and blue dots indicate downregulation. The horizontal dashed line represents the truncated P value of 0.05, and the vertical dashed line represents the 2-fold logFC value.

图3 临床样本验证提示hsa_circ_0001900在WT中呈现出肿瘤特异性表达模式

Fig.3 Validation of tumor-specific expression pattern of hsa_circ_0001900 in clinical samples of WT A: Ranking map of circRNA expression abundance. B: Expression validation of the top 6 circRNAs in clinical samples. C: ROC diagnostic curve of hsa_circ_0001900. *P<0.05, **P<0.01 vs Tumor group.

表3 临床样本表达验证的环状RNA分子的基本特征

Tab.3 Characteristics of circRNA molecules for expression validation in clinical samples

circRNA	Chromosomal loci	Direction of ring formation	Genome length	Splice sequence length	Gene ID	Gene of parent	Trend of expression
hsa_circ_0008122	chr19:23134080-23136043	+	1964	223	ENSG00000183850	ZNF730	up
hsa_circ_0001900	chr9:135881633-135883078	-	1446	425	ENSG00000130559	CAMSAP1	up
hsa_circ_0006151	chr10:68468123-68470163	-	2041	367	ENSG00000138346	DNA2	up
hsa_circ_0004425	chr9:100498765-100516771	+	18007	364	ENSG00000241697	TMEFF1	up
hsa_circ_0075828	Chr6:22020339-22020542	+	204	204	ENSG00000272168	CASC15	up
hsa_circ_0005230	Chr1:172140480-172144437	-	3958	3958	ENSG00000230630	DNM3OS	up

图4 临床相关性分析提示WT中hsa_circ_0001900的高表达与较大的肿瘤体积和较差的预后有关

Fig.4 Correlation analysis of hsa_circ_0001900 expression level in WT with tumor volume and prognosis. A: Expression levels of hsa_circ_0001900 in different cancers. B: Verification of differential expression of hsa_circ_0001900 in a patient cohort. C: The expression level of hsa_circ_0001900 is positively correlated with tumor volume. D: Children with high expression of hsa_circ_0001900 had shorter survival time. *P<0.05, **P<0.01 vs Tumor group.

图5 环状RNA分子hsa_circ_0001900环状结构的注释和验证

Fig.5 Annotation and verification of circular structure of hsa_circ_0001900. A: Sanger sequencing based on PCR products that verifies the reverse splicing sequence of hsa_circ_0001900. B: Agarose gel electrophoresis verifies the RNase R enzyme tolerance of hsa_circ_0001900 from a qualitative perspective. C: qPCR verifies the structural stability of hsa_circ_0001900 from a quantitative perspective. ****P<0.0001.

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高通量环状RNA测序揭示hsa_circ_0001900在肾母细胞瘤中特异性高表达且与不良预后相关

High-throughput circular RNA sequencing reveals tumor-specific high expression of hsa_circ_0001900 in Wilms tumor in association with poor prognosis

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