Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (6): 1241-1252.doi: 10.3864/j.issn.0578-1752.2022.06.015

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles     Next Articles

Effects of FB1 on Apoptosis and Autophagy of Porcine Oocytes in vitro Maturation

LI WenHui(),HE YiJing,JIANG Yao,ZHAO HongYu,PENG Lei,LI Jia,RUI Rong,JU ShiQiang()   

  1. College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095
  • Received:2021-01-29 Accepted:2021-06-17 Online:2022-03-16 Published:2022-03-25
  • Contact: ShiQiang JU E-mail:1065167020@qq.com;jusq@njau.edu.cn

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Abstract:

【Objective】The purpose of this study was to investigate the effects of fumonisin B1 (FB1) on porcine oocyte in vitro maturation and its potential mechanism, so as to provide the theoretical reference for effective prevention and treatment of reproductive toxicity injury caused by FB1 in the clinic.【Method】Porcine cumulus oocyte complexes (COCs) were collected and randomly divided into groups, and treated with different concentrations of FB1 (0, 10, 20 and 30 μg·mL-1) for 44 h during in vitro maturation, respectively. Then, the first polar body (PB1) extrusion and embryo development after activation of oocytes were analyzed, and the effects of FB1 on meiotic progression and cytoskeleton structure of oocytes were further detected by immunofluorescence staining and combined with confocal microscopy. In order to further explore the mechanism of FB1 on toxic injury of porcine oocytes, the JC-1, Annexin V-FITC and LC3A/B fluorescence staining were used to detect mitochondrial function, early apoptosis and autophagy levels in oocytes, respectively. On this basis, the expression of apoptosis/autophagy related to proteins were further analyzed by Western blotting.【Result】FB1 treatment had significant inhibitory effects on oocyte maturation, while PB1 extrusion rate decreased in a concentration-dependent manner. When the concentration of FB1 reached more than 20 μg·mL -1, the PB1 extrusion was significantly decreased (P<0.01), and the cleavage rate and blastocyst rate of the embryos after oocytes parthenogenetic activation were significantly decreased (P<0.01), damaging the development potential of oocytes to a certain extent. And the cell cycle analysis showed that FB1 treatment also disordered the meiotic cycle progression, resulting in a significant increase in the proportion of oocytes that arrested at germinal vesicle breakdown (GVBD) (P<0.01), and a significant decrease in the proportion of oocytes that successfully developed to the Metaphase II (MII) (P<0.01), with an increase in spindle abnormal rate (P<0.01) and a decrease in actin distribution at the plasma membrane (P<0.05). Further studies showed that, compared with control group, the mitochondrial membrane potential was significantly decreased (P<0.05), impairing mitochondrial function. At the same time, the rate of early apoptosis was obviously increased (P<0.01), and the level of autophagy was also significantly increased (P<0.01) in FB1-treated oocytes. Western blotting analysis showed that the expressions of pro-apoptotic protein BAX and autophagy protein LC3A/B II in FB1-treated oocytes were significantly up-regulated (P<0.05), and the expression of anti-apoptotic protein BCL2 was significantly down-regulated (P<0.05), indicating the occurrence of early apoptosis and autophagy.【Conclusion】FB1 had obvious toxic effects on porcine oocyte maturation in vitro and embryo development after activation, resulting in meiotic cycle arrest, spindle structure disorder, actin distribution reduction and mitochondrial injury, and its toxic mechanism might be related to the induction of apoptosis and autophagy in oocytes.

Key words: porcine oocytes, fumonisin B1, cytoskeleton, apoptosis, autophagy

Fig. 1

Effects of the different concentrations of FB1 on the first polar body extrusion rate of porcine oocytes A: The porcine oocyte morphologies after 44 h of culture in vitro (The black arrows point to the first polar body); B: The effects of different concentration of FB1 on PB1 extrusion rate"

Fig. 2

Effects of FB1 on embryo cleavage rate and blastocyst rate after oocytes activation A: Morphologies of 2-cell/4-cell embryo and blastocyst (The black arrows point to the cleaved embryos); B: Cleavage rate; C; Blastocyst rate"

Fig. 3

Representative images of dynamic distribution of chromosome and α-tubulin in porcine oocytes during meiotic progression Blue: chromosome; green: tubulin"

Fig. 4

Effects of FB1 on the cell cycle progression (44 h) of porcine oocytes during meiotic maturation GV: germinal vesicle; GVBD: germinal vesicle breakdown; MI: first metaphase of meiosis; ATI: first anaphase-telophase of meiosis; MII: second metaphase of meiosis"

Fig. 5

Effect of FB1 on spindle structure in porcine oocytes A: Representative images of spindle structure and chromosomes alignment (Blue: chromosome; green: tubulin); B: Percentage of spindle defects"

Fig. 6

Effects of FB1 on the expression and distribution of actin in porcine oocytes A: Representative images of actin distribution (Red: actin); B: Relative average fluorescence intensities of actin on the plasma membrane"

Fig. 7

Effect of FB1 on mitochondrial membrane potential of porcine oocytes A: Representative images of JC-1 staining (Green: JC-1 monomer; red: JC-1 aggregates; yellow: merge); B: Relative average fluorescence intensities of JC-1 red/green signals"

Fig. 8

Effects of FB1 on early apoptosis rate and expression of apoptosis-related proteins in porcine oocytes A: Representative images of Annexin V-FITC staining and the early apoptosis rate (Green: fluorescence signal of Annexin V); B: The protein expression of BAX and BCL2"

Fig. 9

Effect of FB1 on the expression of autophagy marker LC3A/B protein in porcine oocytes A: Representative images of LC3A/B staining and relative average fluorescence intensity of LC3A/B (Red: LC3 fluorescence signal); B: The protein expression of LC3A/B"

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