棉酚对睾丸生精功能和支持细胞凋亡的影响

doi:10.11843/j.issn.0366-6964.2025.11.018

畜牧兽医学报 ›› 2025, Vol. 56 ›› Issue (11): 5575-5587.doi: 10.11843/j.issn.0366-6964.2025.11.018

棉酚对睾丸生精功能和支持细胞凋亡的影响

陈茜¹^,²^,³(), 童江¹^,²^,³, 潘宇恒¹^,²^,³, 马剑峰¹^,²^,³, 师愉倩¹^,²^,³, 陈思宇¹^,²^,³, 李佳鑫¹^,²^,³, 周婷⁴, 刘辰东⁴, 朱砺¹^,²^,³, 沈林園¹^,²^,³^,*(), 甘麦邻¹^,²^,³^,*()

1. 四川农业大学动物科技学院猪禽种业全国重点实验室, 成都 611130
2. 四川农业大学动物科技学院农业农村部畜禽生物组学重点实验室, 成都 611130
3. 四川农业大学动物科技学院畜禽遗传资源发掘与创新利用四川省重点实验室, 成都 611130
4. 四川省丽天牧业有限公司营养部, 达州 635000

收稿日期:2025-04-09 出版日期:2025-11-23 发布日期:2025-11-27
通讯作者: 沈林園,甘麦邻 E-mail:chenqian1@stu.sicau.edu.cn;shenlinyuan@sicau.edu.cn;ganmailin@sicau.edu.cn
作者简介:陈茜(2003-)，女，四川江油人，本科，主要从事动物遗传育种与繁殖研究，E-mail: chenqian1@stu.sicau.edu.cn
基金资助:
中国博士后科学基金(BX20230250；2023M732509)；四川省科技计划(24NSFSC1176；2021YFYZ0030；2021YFYZ0007；SCCXTD-2025-8)；国家生猪产业技术体系(CARS-35)；四川农业大学国家大学生创新训练计划项目(202410626025)

The Impact of Gossypol on Spermatogenic Capacity of the Testis and Apoptosis of Sertoli Cells

CHEN Qian¹^,²^,³(), TONG Jiang¹^,²^,³, PAN Yuheng¹^,²^,³, MA Jianfeng¹^,²^,³, SHI Yuqian¹^,²^,³, CHEN Siyu¹^,²^,³, LI Jiaxin¹^,²^,³, ZHOU Ting⁴, LIU Chendong⁴, ZHU Li¹^,²^,³, SHEN Linyuan¹^,²^,³^,*(), GAN Mailin¹^,²^,³^,*()

1. National Key Laboratory of Pig and Poultry Seed Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
2. Key Laboratory of Livestock and Poultry Biomics of Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
3. Sichuan Provincial Key Laboratory of Exploration and Innovative Utilization of Livestock and Poultry Genetic Resources, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
4. Sichuan Litian Animal Husbandry Co., Ltd. Nutrition Department, Dazhou 635000, China

Received:2025-04-09 Online:2025-11-23 Published:2025-11-27
Contact: SHEN Linyuan, GAN Mailin E-mail:chenqian1@stu.sicau.edu.cn;shenlinyuan@sicau.edu.cn;ganmailin@sicau.edu.cn

摘要/Abstract

摘要：

旨在探究棉酚(gossypol)引起小鼠睾丸组织损伤和TM4细胞(小鼠睾丸支持细胞)凋亡的生殖毒性机理。本研究建立棉酚灌胃雄性ICR小鼠(improved castle road)模型(0、30 (mg·kg)·d^-1，连续30 d)和棉酚染毒TM4细胞模型(0、15、20、25 μmol·L^-1)，随后采用精子自动分析系统检测小鼠精子质量；HE染色法观察小鼠睾丸组织病理学变化；实时荧光定量PCR技术检测小鼠睾丸组织中凋亡、自噬、铁死亡、紧密连接和精子发生相关基因的表达量以及TM4细胞中凋亡相关基因的表达量，Western blot技术检测小鼠睾丸组织中凋亡相关蛋白表达情况。结果发现，棉酚可显著降低小鼠体重增长速率、精子活力和精子密度(P < 0.01)，并引发睾丸组织病理学改变(曲细精管皱缩，部分支持细胞被破坏，精子数量减少等)。睾丸组织中铁死亡、自噬和凋亡这3种死亡方式相关基因的表达趋势均有变化，且凋亡相关基因的表达趋势变化最明显，凋亡抑制基因Bcl-2显著下调(P < 0.05)，凋亡促进基因Bax、Tnf-α以及Bax/Bcl-2比值上调(P < 0.01，P < 0.05，P < 0.01)；睾丸组织中凋亡蛋白Bax、Tnf-α及Bax/Bcl-2比值显著升高(P < 0.05)；此外，睾丸组织中紧密连接和精子发生相关基因显著下调。在TM4细胞体外试验中，使用不同浓度棉酚染毒均能显著影响TM4细胞内凋亡相关基因的表达，凋亡促进基因Bax、Tnf-α及Bax/Bcl-2的表达量极显著上调(P < 0.01)，这与睾丸组织的定量结果一致。综上，棉酚染毒所导致的小鼠睾丸生精能力减弱与TM4细胞发生凋亡密切相关，这种凋亡与Bax、Tnf-α、Bax/Bcl-2表达升高有关。

关键词: 棉酚, TM4细胞, RT-qPCR, 凋亡, Bax, Tnf-α, Bax/Bcl-2

Abstract:

The aim of this study was to explore the reproductive toxicity mechanism of gossypol-induced testicular tissue injury and TM4 cells(mouse testicular sertoli cells) apoptosis in mice. A gossypol intragastric administration model in male ICR(improved castle road) mice (0, 30 (mg·kg) ·d^-1) for 30 consecutive days) and a gossypol exposure model in TM4 cells (0, 15, 20, 25 μmol·L^-1) were established. Subsequently, the sperm quality of mice was assessed by an automatic sperm analysis system; the histopathological alterations of testicular tissue were observed via HE staining; and the expression levels of apoptosis, autophagy, ferroptosis, tight junction, and spermatogenesis-related genes in testicular tissue, as well as apoptosis-related genes in TM4 cells, were detected using real-time fluorescence quantitative PCR, and the expression of apoptosis-related proteins in testicular tissue was detected by Western blot. The findings revealed that gossypol significantly decreased the weight gain rate, sperm motility, and sperm density of mice (P < 0.01), and elicited histopathological changes in testicular tissue (such as atrophy of seminiferous tubules, destruction of some sertoli cells, and reduction in sperm count). The expression trends of genes related to the three death modes of ferroptosis, autophagy, and apoptosis in testicular tissue all changed, and the expression trend of apoptosis-related genes changed most significantly. The expression of the apoptosis inhibitory gene Bcl-2 was significantly downregulated (P < 0.05), while the expressions of the apoptosis promoting genes Bax, Tnf-α, and the Bax/Bcl-2 ratio were upregulated (P < 0.01, P < 0.05, P < 0.01). The expressions of apoptosis proteins Bax, Tnf-α, and the Bax/Bcl-2 ratio in testicular tissue were significantly increased (P < 0.05). Additionally, the expressions of tight junction and spermatogenesis-related genes in testicular tissue were significantly downregulated. In the in vitro experiment with TM4 cells, exposure to different concentrations of gossypol significantly influenced the expression of apoptosis-related genes within TM4 cells, and the expressions of apoptosis promoting genes Bax, Tnf-α, and the Bax/Bcl-2 ratio were Extremely significantly upregulated (P < 0.01), which was consistent with the quantitative results of testicular tissue. In summary, the weakened spermatogenic ability of the testis in gossypol-exposed mice is closely related to the apoptosis of TM4 cells, and this apoptosis is associated with the increased expressions of Bax, Tnf-α, and Bax/Bcl-2.

Key words: gossypol, TM4 cells, RT-qPCR, apoptosis, Bax, Tnf-α, Bax/Bcl-2

中图分类号:

S814.1

陈茜, 童江, 潘宇恒, 马剑峰, 师愉倩, 陈思宇, 李佳鑫, 周婷, 刘辰东, 朱砺, 沈林園, 甘麦邻. 棉酚对睾丸生精功能和支持细胞凋亡的影响[J]. 畜牧兽医学报, 2025, 56(11): 5575-5587.

CHEN Qian, TONG Jiang, PAN Yuheng, MA Jianfeng, SHI Yuqian, CHEN Siyu, LI Jiaxin, ZHOU Ting, LIU Chendong, ZHU Li, SHEN Linyuan, GAN Mailin. The Impact of Gossypol on Spermatogenic Capacity of the Testis and Apoptosis of Sertoli Cells[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(11): 5575-5587.

图/表 6

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基因 Gene	功能 Function	引物序列(5′→3′) Primers sequence	产物长度/bp Products length
Bcl-2	凋亡相关基因	F：GGAACAGGACGCTCAGACTT	119
		R：GCAGGATAGCAGCACAGGAT
Bax		F：TGAAGACAGGGGCCTTTTTG	140
		R：AATTCGCCGGAGACACTCG
P53		F：TCACAGCGTCTGTTGACATTT	210
		R：ACCAAGCTCATTACCCTGACA
Tnf-α		F：GACGTGGAACTGGCAGAAGAG	160
		R：TTGGTGGTTTGTGAGTGTGAG
Ki67		F：ACCGTGGAGTAGTTTATCTGGG	126
		R：TGTTTCCAGTCCGCTTACTTCT
P62	自噬相关基因	F：TCCAGCTTGAACCCTATTGAGA	166
		R：GTCCTGCATCACTGAGCATCT
Vps15		F：CTGGCGACAGGAGACTGAC	188
		R：GGGGAAACCAAGTCCCAGAA
Atg5		F：TGTGCTTCGAGATGTGTGGTT	120
		R：GTCAAATAGCTGACTCTTGGCAA
Ulk1		F：AAGTTCGAGTTCTCTCGCAAG	190
		R：CGATGTTTTCGTGCTTTAGTTCC
Lc3		F：GGCTACGGCTACTATCGCAC	100
		R：AGGAGGGCATGACAAAGGAGA
Acsl4	铁死亡相关基因	F：CTCACCATTATATTGCTGCCTGT	163
		R：TCTCTTTGCCATAGCGTTTTTCT
Ho-1		F：AAGCCGAGAATGCTGAGTTCA	198
		R：GCCGTGTAGATATGGTACAAGGA
Ptgs2		F：TGAGCAACTATTCCAAACCAGC	74
		R：GCACGTAGTCTTCGATCACTATC
Gpx4		F：GCCTGGATAAGTACAGGGGTT	99
		R：CATGCAGATCGACTAGCTGAG
Fth1		F：AGACCGTGATGACTGGGAGA	138
		R：TCAATGAAGTCACATAAGTGGGGA
Zo1	紧密连接相关基因	F：CGCGGAGAGAGACAAGATGT	55
		R：CATTGCTGTGCTCTTAGCGG
Cdh1		F：AACCCAAGCACGTATCAGGG	94
		R：GAGTGTTGGGGGCATCATCA
Occludlin		F：CCCTCTTTCCTTAGGCGACA	95
		R：CCCAAGATAAGCGAACCTGC
Claudin5		F：GTTAAGGCACGGGTAGCACT	137
		R：TACTTCTGTGACACCGGCAC
Sycp3	精子发生相关基因	F：ATGATGGAAACTCAGCAGCA	135
		R：GCATGCCTCTTAGCTAATGTTTT
Sycp1		F：AGGTTCTGAGGGGAAGCTCA	98
		R：CCTCCTGGGCCGTTGTC
Ddx4		F：GCAGCAAGTGATTCAGGCAA	146
		R：TCACTGCTTTCACCTCCTTCA
β-actin	内参基因	F：TGGAATCCTGTGGCATCCATGAAAC	110
		R：TGGAATCCTGTGGCATCCATGAAAC

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棉酚对睾丸生精功能和支持细胞凋亡的影响

The Impact of Gossypol on Spermatogenic Capacity of the Testis and Apoptosis of Sertoli Cells

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