急性热应激通过降低牛磺酸水平影响猪睾丸支持细胞的功能

doi:10.11843/j.issn.0366-6964.2025.04.026

Abstract

Abstract:

To investigate the metabolic response to acute heat stress of porcine sertoli cells, porcine sertoli cells were collected under 3 conditions: before acute heat stress (control group), immediately after acute heat stress (43℃, 0.5 h; HS0.5 group), and after a 36 hour recovery post-acute heat stress (HS0.5-R36 group), with 3 biological replicates per group. Metabolic profiling was detected using liquid chromatography-tandem mass spectrometry (LC-MS/MS). Differential metabolites were validated via ELISA. The effects of key differential metabolite on cell viability, proliferation, and apoptosis were assessed using CCK-8, EdU, and Annexin V FITC/PI kits. Level of reactive oxygen species (ROS), mitochondrion distribution, and mitochondrion membrane potential were evaluated using ROS, RH123 and Mito Tracker staining. The results showed that 33, 57 and 115 significant differential secondary metabolites (P < 0.05; VIP>1.00) were identified respectively in HS0.5 vs. Control, HS0.5-R36 vs. HS0.5 and HS0.5-R36 vs. Control comparisons. The pathway analysis showed that significant differential metabolites were mainly enriched in taurine and hypotaurine metabolism and other pathways. ELISA verified that acute heat stress significantly decreased levels of taurine and gamma-aminobutyric acid, which were consistent to metabolomic results. Taurine level was significantly decreased around 5.7 μmol·L^-1 in HS0.5-R36 group as compared to control group. Treatment of porcine sertoli cells using taurine of 5.7 μmol·L^-1 for 48 h significantly increased cell viability, promoted proliferation, suppressed apoptosis and enhanced mitochondrial function (P < 0.05). These results suggest that acute heat stress could significantly alter metabolism, and the differential metabolite taurine partially mediate the damage exerted by acute heat stress on porcine sertoli cells. These results provide new insights for rescuing damage caused by acute heat stress on porcine sertoli cells.

Key words: porcine, sertoli cell, acute heat stress, metabolomics, taurine

CLC Number:

S828.3

WANG Xinxin, LIU Xiaoying, WANG Yi, WANG Fang, ZHAO Han, DU Zhiqiang, YANG Caixia. Acute Heat Stress Affects the Functions of Porcine Sertoli Cells via Decreasing Taurine Level[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(4): 1779-1790.

Figures/Tables 6

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Fig. 6

References 41

1	PARRISH J J , WILLENBURG K L , GIBBS K M , et al. Scrotal insulation and sperm production in the boar[J]. Mol Reprod Dev, 2017, 84 (9): 969- 978. doi: 10.1002/mrd.22841
2	LI C , WANG Y , LI L , et al. Betaine protects against heat exposure-induced oxidative stress and apoptosis in bovine mammary epithelial cells via regulation of ROS production[J]. Cell Stress Chaperones, 2019, 24 (2): 453- 460. doi: 10.1007/s12192-019-00982-4
3	CHEN K L , WANG H L , JIANG L Z , et al. Heat stress induces apoptosis through disruption of dynamic mitochondrial networks in dairy cow mammary epithelial cells[J]. In Vitro Cell Dev Biol Anim, 2020, 56 (4): 322- 331. doi: 10.1007/s11626-020-00446-5
4	DURAIRAJANAYAGAM D , AGARWAL A , ONG C . Causes, effects and molecular mechanisms of testicular heat stress[J]. Reprod Biomed Online, 2015, 30 (1): 14- 27. doi: 10.1016/j.rbmo.2014.09.018
5	KIM B , PARK K , RHEE K . Heat stress response of male germ cells[J]. Cell Mol Life Sci, 2013, 70 (15): 2623- 2636. doi: 10.1007/s00018-012-1165-4
6	RIZZOTO G , BOE-HANSEN G , KLEIN C , et al. Acute mild heat stress alters gene expression in testes and reduces sperm quality in mice[J]. Theriogenology, 2020, 158, 375- 381. doi: 10.1016/j.theriogenology.2020.10.002
7	WANG S H , CHENG C Y , TANG P C , et al. Acute heat stress induces differential gene expressions in the testes of a broiler-type strain of Taiwan country chickens[J]. PLoS One, 2015, 10 (5): e0125816. doi: 10.1371/journal.pone.0125816
8	CHEN S R , LIU Y X . Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli cell signaling[J]. Reproduction, 2015, 149 (4): R159- R167. doi: 10.1530/REP-14-0481
9	NI F D , HAO S L , YANG W X . Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis[J]. Cell Death Dis, 2019, 10 (8): 541. doi: 10.1038/s41419-019-1782-z
10	YANG C X , CHEN L , YANG Y W , et al. Acute heat stress reduces viability but increases lactate secretion of porcine immature Sertoli cells through transcriptome reprogramming[J]. Theriogenology, 2021, 173, 183- 192. doi: 10.1016/j.theriogenology.2021.06.024
11	WEST P R , WEIR A M , SMITH A M , et al. Predicting human developmental toxicity of pharmaceuticals using human embryonic stem cells and metabolomics[J]. Toxicol Appl Pharmacol, 2010, 247 (1): 18- 27. doi: 10.1016/j.taap.2010.05.007
12	REVEGLIA P , RAIMONDO M L , MASI M , et al. Untargeted and targeted LC-MS/MS based metabolomics study on in vitro culture of Phaeoacremonium species[J]. J Fungi (Basel), 2022, 8 (1): 55. doi: 10.3390/jof8010055
13	AN X , LI Q , CHEN N , et al. Effects of Pgam1-mediated glycolysis pathway in Sertoli cells on Spermatogonial stem cells based on transcriptomics and energy metabolomics[J]. Front Vet Sci, 2022, 9, 992877. doi: 10.3389/fvets.2022.992877
14	YANG Y W , CHEN L , MOU Q , et al. Ascorbic acid promotes the reproductive function of porcine immature Sertoli cells through transcriptome reprogramming[J]. Theriogenology, 2020, 158, 309- 320. doi: 10.1016/j.theriogenology.2020.09.022
15	ALDAHHAN R A , STANTON P G . Heat stress response of somatic cells in the testis[J]. Mol Cell Endocrinol, 2021, 527, 111216. doi: 10.1016/j.mce.2021.111216
16	BELHADJ SLIMEN I , NAJAR T , GHRAM A , et al. Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review[J]. J Anim Physiol Anim Nutr (Berl), 2016, 100 (3): 401- 412. doi: 10.1111/jpn.12379
17	MALMGREN L , LARSSON K . Semen quality and fertility after heat stress in boars[J]. Acta Vet Scand, 1984, 25 (3): 425- 435. doi: 10.1186/BF03547257
18	ZHOU W J , YANG H L , MEI J , et al. Fructose-1, 6-bisphosphate prevents pregnancy loss by inducing decidual COX-2 macrophage differentiation[J]. Sci Adv, 2022, 8 (8): eabj2488. doi: 10.1126/sciadv.abj2488
19	ZHAO X , JIANG L , FANG X , et al. Host-microbiota interaction-mediated resistance to inflammatory bowel disease in pigs[J]. Microbiome, 2022, 10 (1): 115. doi: 10.1186/s40168-022-01303-1
20	ZHANG B , CHEN T , CAO M , et al. Gut microbiota dysbiosis induced by decreasing endogenous melatonin mediates the pathogenesis of Alzheimer's disease and obesity[J]. Front Immunol, 2022, 13, 900132. doi: 10.3389/fimmu.2022.900132
21	DENG C C , ZHANG J P , HUO Y N , et al. Melatonin alleviates the heat stress-induced impairment of Sertoli cells by reprogramming glucose metabolism[J]. J Pineal Res, 2022, 73 (3): e12819. doi: 10.1111/jpi.12819
22	ROSSI G S , ELBASSIOUNY A , JAMISON J , et al. Heat exposure limits pentose phosphate pathway activity in bumblebees[J]. Conserv Physiol, 2024, 12 (1): coae031. doi: 10.1093/conphys/coae031
23	LIU F , ZHANG T , HE Y , et al. Integration of transcriptome and proteome analyses reveals the regulation mechanisms of Larimichthys polyactis liver exposed to heat stress[J]. Fish Shellfish Immunol, 2023, 135, 108704. doi: 10.1016/j.fsi.2023.108704
24	GONZULEZ R R , LEYVA C L , PEREGRINO U A B , et al. The combination of hypoxia and high temperature affects heat shock, anaerobic metabolism, and pentose phosphate pathway key components responses in the white shrimp (Litopenaeus vannamei)[J]. Cell Stress Chaperones, 2023, 28 (5): 493- 509. doi: 10.1007/s12192-022-01265-1
25	LI Y , MA T , LV X , et al. Fluoride stimulates the MAPK pathway to regulate endoplasmic reticulum stress and heat shock proteins to induce duodenal toxicity in chickens[J]. Poult Sci, 2024, 103 (12): 104408. doi: 10.1016/j.psj.2024.104408
26	DUTTA G , ALEX R , SINGH A , et al. Functional transcriptome analysis revealed upregulation of MAPK-SMAD signaling pathways in chronic heat stress in crossbred cattle[J]. Int J Biometeorol, 2024, 68 (7): 1371- 1385. doi: 10.1007/s00484-024-02672-y
27	HUANG J , CHAI X , WU Y , et al. β-Hydroxybutyric acid attenuates heat stress-induced neuroinflammation via inhibiting TLR4/p38 MAPK and NF-κB pathways in the hippocampus[J]. FASEB J, 2022, 36 (4): e22264.
28	LIU L , GONG X , ZHANG X , et al. Resveratrol alleviates heat-stress-induced impairment of the jejunal mucosa through TLR4/MAPK signaling pathway in black-boned chicken[J]. Poult Sci, 2024, 103 (1): 103242. doi: 10.1016/j.psj.2023.103242
29	ZHANG M , DUNSHEA F R , WARNER R D , et al. Impacts of heat stress on meat quality and strategies for amelioration: a review[J]. Int J Biometeorol, 2020, 64 (9): 1613- 1628. doi: 10.1007/s00484-020-01929-6
30	ZHAO H , KE H , ZHANG L , et al. Integrated analysis about the effects of heat stress on physiological responses and energy metabolism in Gymnocypris chilianensis[J]. Sci Total Environ, 2022, 806 (Pt 3): 151252.
31	NADERI M , SEYEDABADI M , AMIRI FT , et al. Taurine protects against perfluorooctanoic acid-induced hepatotoxicity via inhibition of oxidative stress, inflammatory, and apoptotic pathways[J]. Toxicol Res (Camb), 2023, 12 (1): 124- 132. doi: 10.1093/toxres/tfad005
32	吕秋凤, 董公麟, 曹双, 等. 牛磺酸抗应激作用的研究进展[J]. 中国畜牧杂志, 2014, 50 (21): 78- 81.
	LV Q F , DONG G L , CAO S , et al. Research progress on taurine anti-stress[J]. Chinese Journal of Animal Science, 2014, 50 (21): 78- 81.
33	QARADAKHI T , GADANEC L K , MCSWEENEY K R , et al. The Anti-inflammatory effect of taurine on cardiovascular disease[J]. Nutrients, 2020, 12 (9): 2847. doi: 10.3390/nu12092847
34	SANTULLI G , KANSAKAR U , VARZIDEH F , et al. Functional role of taurine in aging and cardiovascular health: an updated overview[J]. Nutrients, 2023, 15 (19): 4236. doi: 10.3390/nu15194236
35	HIGUCHI M , CELINO F T , SHIMIZU-YAMAGUCHI S , et al. Taurine plays an important role in the protection of spermatogonia from oxidative stress[J]. Amino Acids, 2012, 43 (6): 2359- 2369. doi: 10.1007/s00726-012-1316-9
36	SINGH P , GOLLAPALLI K , MANGIOLA S , et al. Taurine deficiency as a driver of aging[J]. Science, 2023, 380 (6649): eabn9257. doi: 10.1126/science.abn9257
37	CHAWLA D . Taurine and neonatal nutrition[J]. Indian J Pediatr, 2018, 85 (10): 829. doi: 10.1007/s12098-018-2781-2
38	CAO T , ZHANG W , WANG Q , et al. Cancer SLC6A6-mediated taurine uptake transactivates immune checkpoint genes and induces exhaustion in CD8⁺ T cells[J]. Cell, 2024, 187 (9): 2288- 2304. doi: 10.1016/j.cell.2024.03.011
39	张金秋, 马子力, 韩立秋, 等. 牛磺酸对不同饲养方式蛋鸡肾脏功能、抗氧化能力和细胞因子水平的影响[J]. 天津农学院学报, 2014, 21 (1): 9- 14.
	ZHANG J Q , MA Z L , HAN L Q , et al. Influence of dietary taurine on renal functions, anti-oxidation activity and cytokines level in laying hens with different rearing patterns[J]. Journal of Tianjin Agricultural University, 2014, 21 (1): 9- 14.
40	温静, 余哲琪, 田佳迎, 等. γ-氨基丁酸对热应激雏鸡胰腺组织结构、抗氧化能力、消化酶活性及细胞凋亡的影响[J]. 动物营养学报, 2021, 33 (5): 2927- 2938.
	WEN J , YU Z Q , TIAN J Y , et al. Effects of γ-Aminobutyric acid on pancreatic tissue structure, antioxidant capacity, digestive enzyme activity and cell apoptosis of heat-stressed chicks[J]. Chinese Journal of Animal Nutrition, 2021, 33 (5): 2927- 2938.
41	TANG J , CHEN Z . The protective effect of γ-aminobutyric acid on the development of immune function in chickens under heat stress[J]. J Anim Physiol Anim Nutr (Berl), 2016, 100 (4): 768- 777. doi: 10.1111/jpn.12385

[1]	MENG Xiangxu, LI Jia, REN Deming, CHEN Kuirong, HE Yiyun, WANG Lixian, SHENG Xihui, WANG Ligang. Study on Serum Metabolomics of High and Low Resilience Group of Min Pigs with Porcine Reproductive and Respiratory Syndrome [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(4): 1689-1699.
[2]	HOU Wanchen, XU Tong. Cannabidiol Antagonizes BPA-induced Apoptosis and Autophagy in Porcine Intestinal Epithelial Cells through the BRD4/AMPK/mTOR Signaling Pathway [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(4): 1919-1933.
[3]	LIU Aijun, ZHANG Chuanliang, HUANG Xiaobing, ZHOU Caiqin. Research Progress on the Life Cycle of Porcine Reproductive and Respiratory Syndrome Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(3): 1027-1041.
[4]	WU Peiling, LI Yixuan, WANG Haojie, LI Yafei, LIU Shaomeng, LIU Qingyun, WANG Xiangru. Research Progress of Porcine Epidemic Diarrhea Vaccine for Pigs [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(3): 1042-1058.
[5]	WANG Hong, ZHAO Weimin, CHENG Jinhua, LI Huixia, FANG Xiaomin. Identification and Transcriptional Regulation Analysis of the Core Promoter of Porcine CYP3A29 Gene [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(3): 1147-1158.
[6]	YU Xinya, HE Haijian, WANG Lei, NI Yuchen, DU Jing, ZHOU Yingshan, DONG Wanyu, WANG Xiaodu. Effect of lncRNA 18850 on Porcine Epidemic Diarrhea Virus Replication [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(3): 1366-1375.
[7]	FAN Jie, TAI Yirun, ZHU Yanli, CHEN Zhixiong, HU Qiaoyun, CHEN Zhi, LIU Tiantian, LI Xin, FAN Zhongxin, GE Meng. Investigation of Porcine Circovirus 2 Infection Status and Analysis of Genetic Evolution in Hunan Province in Recent Years [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(3): 1376-1385.
[8]	ZHANG Dongxuan, WANG Zhihao, QIAO Yan, ZHAO Xiaoxiao, FAN Songjie, ZHANG Chao. Prokaryotic Expression of S1 Protein in Porcine Epidemic Diarrhea Virus and Screening of Its Aptamers [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(2): 839-850.
[9]	SHAO Yongheng, NI Minting, GAO Mengling, TANG Jiao, ZHANG Gengxin, LIN Shengyu, LIU Guangliang, CHEN Jianing, WANG Wenhui. Prokaryotic Expression of VP1 Protein to Porcine Teschovirus Type 5 and the Establishment of an Indirect ELISA Detection Method [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(2): 883-889.
[10]	SUN Yawen, CHEN Siying, LI Kang, LENG Xuan, WANG Dong, PANG Yunwei. Strategies for Alleviating Cryoinjury of Porcine Vitrified-Oocytes [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(1): 36-44.
[11]	CAI Yunfeng, LI Hong, HUANG Xiaoming, HE Qing, DING Zhenyu, YU Wanting, LUO Shile, CHEN Fangzhi, WANG Naidong, YANG Yi, ZHAN Yang. Study on the Presentation Strategy and Immunogenicity of Porcine Parvovirus Epitope Inserted by 3-fold Axes Region on the Surface of Porcine Circovirus Type 2 Virus-like Particles [J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(1): 307-318.
[12]	Nanzhu CHEN, Junliang LI, Dawei YU, Xinyi ZHOU, Jing WANG, Huiying ZOU, Weihua DU. Analysis of Imprinted Expression and DNA Methylation Status of the Porcine MKRN3 Gene [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(9): 3853-3863.
[13]	Liguo GAO, Hanqin SHEN, Yiquan CHEN, Sheng CHEN, Wencheng LIN, Feng CHEN. Prokaryotic Expression of Recombinant VP6* Protein of Porcine Rotavirus and Establishment of Indirect ELISA Detection Method [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(9): 4021-4028.
[14]	Ning PENG, Yaxu LIANG, Fei LONG, Dongming YU, Xiang ZHONG. Inhibitory Effect of Resveratrol on Rotavirus-infected Porcine Intestinal Epithelial Cells IPEC-J2 [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(9): 4213-4225.
[15]	Zhentao XIA, Nan WANG, Wanjie WANG, Qilü ZHOU, Lei HUANG, Yulian MU. Characteristics Analysis of TGEV Infection Mediated by IPEC-J2 with Knockout of pAPN Gene [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(8): 3395-3407.

Acute Heat Stress Affects the Functions of Porcine Sertoli Cells via Decreasing Taurine Level

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 6

References 41

Related Articles 15

Recommended Articles

Metrics

Comments