L-苹果酸对猪卵巢颗粒细胞增殖及转录谱的影响

doi:10.11843/j.issn.0366-6964.2025.11.017

畜牧兽医学报 ›› 2025, Vol. 56 ›› Issue (11): 5563-5574.doi: 10.11843/j.issn.0366-6964.2025.11.017

L-苹果酸对猪卵巢颗粒细胞增殖及转录谱的影响

赵笑怡¹^,²(), 朱龙龙³, 刘辉², 张董燕², 蔡龙², 王雅蕾², 王晶², 赵俊星¹^,*(), 陈美霞²^,*()

1. 山西农业大学动物科学学院, 太谷 030801
2. 北京市农林科学院畜牧兽医研究所, 北京 100097
3. 河南科技大学动物科技学院, 洛阳 471023

收稿日期:2025-04-18 出版日期:2025-11-23 发布日期:2025-11-27
通讯作者: 赵俊星,陈美霞 E-mail:zxy_9z@163.com;junxzh@163.com;meixia10nian@163.com
作者简介:赵笑怡(1999-)，女，山西垣曲人，硕士，主要从事动物遗传育种与繁殖研究，E-mail：zxy_9z@163.com
基金资助:
国家重点研发计划(2022YFD1300405-9)；北京市农林科学院青年科研基金(QNJJ202237)；北京市农林科学院改革与发展项目(XMS202415)；国家自然科学基金(32202705)；北京市科协”青年人才托举工程”

Effects of L-Malic Acid on the Proliferation and Transcriptional Profile of Porcine Ovarian Granulosa Cells

ZHAO Xiaoyi¹^,²(), ZHU Longlong³, LIU Hui², ZHANG Dongyan², CAI Long², WANG Yalei², WANG Jing², ZHAO Junxing¹^,*(), CHEN Meixia²^,*()

1. College of Animal Science, Shanxi Agricultural University, Taigu 030801, China
2. Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
3. College of Animal Science and Technology, Henan University of Science and Technology, Luoyang 471023, China

Received:2025-04-18 Online:2025-11-23 Published:2025-11-27
Contact: ZHAO Junxing, CHEN Meixia E-mail:zxy_9z@163.com;junxzh@163.com;meixia10nian@163.com

摘要/Abstract

摘要：

旨在探讨L-苹果酸(L-malic acid，L-MA)对猪卵巢颗粒细胞(porcine ovary granulosa cells，PGCs)增殖的影响，并基于转录组学揭示其可能的作用机制。本研究以原代分离培养的猪卵巢颗粒细胞为研究对象，设置对照组和L-MA处理组(10、25、50、100、200 μmol·L^-1), 利用CCK-8法、实时荧光定量PCR、EdU染色法(5-ethynyl-2'-deoxyuridine)等技术检测细胞活力和细胞增殖的变化；利用转录组测序分析L-MA对PGCs基因转录谱的影响。结果发现，与对照组相比，25、50、100和200 μmol·L^-1的L-MA均显著提高了PGCs细胞活力(P < 0.05)，其中L-MA终浓度为50 μmol·L^-1时，PGCs细胞活力最高。50 μmol·L^-1 L-MA处理后，PGCs的增殖细胞核抗原(proliferating cell nuclear antigen，PCNA)基因mRNA表达量显著增加(P < 0.01)；EdU阳性细胞比例显著增加。转录组分析显示，基于|FC|≥1.5且P < 0.05的筛选标准，L-MA处理后PGCs中169个基因显著上调，118个基因显著下调。GO功能富集显示，差异表达基因主要富集在编码细胞周期复合物以及核酸酶等细胞组分，以及遗传物质复制、表观遗传修饰、物质转运和代谢、细胞增殖和分化等分子功能和生物学过程；KEGG和GSEA富集显示，差异表达基因主要参与细胞免疫、遗传物质复制、物质代谢和生殖功能相关的信号通路。此外，通过对差异表达基因转录因子功能和靶基因预测，发现转录因子ELF3是最有可能受L-MA调控的转录因子，其与PCNA启动子区域存在可能的结合序列。综上所述，L-MA可以显著促进猪卵巢颗粒细胞增殖，这可能与L-MA调控细胞中编码细胞周期复合物以及核酸酶等组分的基因表达，增强与遗传物质复制、表观遗传修饰和物质转运等相关的分子功能和生物学过程，以及提升细胞健康水平等有关。本研究为应用L-苹果酸相关产品调控卵巢颗粒细胞增殖及卵巢功能提供了重要的科学依据。

关键词: L-苹果酸, 猪卵巢颗粒细胞, 细胞增殖, 转录组分析

Abstract:

The present study was designed to examine the effects of L-malic acid (L-MA) on the cell proliferation of porcine ovarian granulosa cells (PGCs) and to uncover the potential mechanism based on transcriptomic analysis. In this study, primary PGCs were isolated, cultured and randomly assigned to either a control group or L-MA treatment groups (10, 25, 50, 100, and 200 μmol·L^-1). CCK-8 assay, EdU incorporation assay (5-ethynyl-2'-deoxyuridine) and qPCR analysis were used to assess the cell viability and cell proliferation. Furthermore, RNA sequencing (RNA-seq) was employed to delineate L-MA-induced the transcriptional landscape alterations in PGCs. Compared with the control group, 25, 50, 100 and 200 μmol·L^-1 L-MA significantly increased cell viability of PGCs (P < 0.05). PGCs exhibited the highest cell viability at an L-MA final concentration of 50 μmol·L^-1. Treatment with 50 μmol·L^-1 L-MA markedly upregulated the mRNA expression of proliferating cell nuclear antigen (PCNA) (P < 0.01), a key proliferation marker, and enhanced the proportion of EdU-positive cells in PGCs. Transcriptomic analysis revealed that under the threshold of |FC|≥1.5 and P < 0.05, 169 significantly upregulated and 118 downregulated genes were identified in PGCs with L-MA exposure. GO enrichment analysis demonstrated that differentially expressed genes (DEGs) were predominantly enriched in cellular components related to cell cycle complexes and nucleases, with molecular functions and biological processes related to genetic material replication, epigenetic modification, substance transport and metabolism, as well as cell proliferation and differentiation. KEGG and GSEA analyses further indicated that DEGs were primarily involved in signaling pathways associated with cellular immunity, genetic material replication, substance metabolism, and reproductive functions. Notably, predictions of transcription factor (TF) and binding sequences between TF and TF's target genes suggested that ELF3 was identified as the most likely candidate transcriptional factor mediated by L-MA, with potential binding sites within the PCNA promoter region. In summary, the findings demonstrate that L-MA significantly enhances the proliferation of porcine ovarian granulosa cells. This proliferative effect may be attributed to L-MA-mediated regulation of gene expression involving cell cycle complexes and nucleases, enhancement of molecular functions and biological processes related to genetic material replication, epigenetic modification, and substance transport, as well as improvement of cell health. This study provides important scientific evidence for the potential application of L-malic acid-based products in modulating granulosa cell proliferation and ovarian function.

Key words: L-malic acid, porcine ovarian granulosa cells, cell proliferation, transcriptome analysis

中图分类号:

S828.3

赵笑怡, 朱龙龙, 刘辉, 张董燕, 蔡龙, 王雅蕾, 王晶, 赵俊星, 陈美霞. L-苹果酸对猪卵巢颗粒细胞增殖及转录谱的影响[J]. 畜牧兽医学报, 2025, 56(11): 5563-5574.

ZHAO Xiaoyi, ZHU Longlong, LIU Hui, ZHANG Dongyan, CAI Long, WANG Yalei, WANG Jing, ZHAO Junxing, CHEN Meixia. Effects of L-Malic Acid on the Proliferation and Transcriptional Profile of Porcine Ovarian Granulosa Cells[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(11): 5563-5574.

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基因 Gene	对照组 Control	处理组 Treatment	倍变化 FC	log₂FC	P值 P-value	校正P值 P-adjust	上调/下调 Regulation
ONECUT2	0.18	0.37	2.08	1.06	0.01	1.00	up
ELF3	0.65	1.30	2.00	1.00	＜0.01	0.01	up
SIM2	0.02	0.15	9.47	3.24	0.01	1.00	up
STAT4	0.16	0.04	0.27	-1.91	0.03	1.00	down
FOXA1	0.06	0.14	2.26	1.18	0.03	1.00	up
HEYL	0.09	0.19	2.26	1.17	0.05	1.00	up
POU2F2	0.10	0.24	3.08	1.62	0.01	1.00	up
ZBED1	1.92	3.93	2.06	1.05	＜0.01	＜0.01	up

转录因子 TF	检索基因 Query	起始位置 Start	终止位置 Stop	正链/负链 Strand	结合位点预测分数 Score	P值 P-value	校正P值 Q value	结合位点匹配序列 Mached sequence
ELF3	PCNA	1 049	1 060	-	13.020 4	2.25E-05	0.089 6	GAGGCGGAAGCC
ELF3	PCNA	660	673	+	11.485 7	4.88E-05	0.108 0	TCAAACTTCCTGTG
ELF3	PCNA	1 771	1 784	-	11.278 6	5.54E-05	0.108 0	CAACACTTCCTCAG

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L-苹果酸对猪卵巢颗粒细胞增殖及转录谱的影响

Effects of L-Malic Acid on the Proliferation and Transcriptional Profile of Porcine Ovarian Granulosa Cells

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