DOI QR코드

DOI QR Code

Effects of lipopolysaccharides on the maturation of pig oocytes

  • Yi, Young-Joo (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Adikari, Adikari Arachchige Dilki Indrachapa (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Moon, Seung-Tae (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Lee, Sang-Myeong (Laboratory of Veterinary Virology, College of Veterinary Medicine, Chungbuk National University) ;
  • Heo, Jung-Min (Department of Animal Science and Biotechnology, Chungnam National University)
  • 투고 : 2021.01.19
  • 심사 : 2021.02.09
  • 발행 : 2021.03.01

초록

Bacterial infections in the female reproductive tract negatively affect ovarian function, follicular development, and embryo development, leading to the eventual failure of fertilization. Moreover, bacterial lipopolysaccharides (LPS) can interfere with the immune system and reproductive system of the host animal. Therefore, this study examined the effect of LPS on the in vitro maturation (IVM) of pig oocytes. Oocytes were matured in TCM199 medium in the presence of varying concentrations of LPS (0 - 50 ㎍·mL-1). The maturation rate, cortical granules (CGs) migration, and chromosome alignment were subsequently evaluated during the meiotic development of the oocytes. We observed a dose-dependent and significant decrease in the metaphase II (MII) rate with increasing concentrations of LPS (97.6% control [0 ㎍·mL-1 LPS] vs. 10.4-74.9% LPS [1 - 50 ㎍·mL-1], p < 0.05). In addition, compared to the control oocytes without LPS, higher levels of abnormal CGs distribution (18.1 - 50.0% LPS vs. 0% control), chromosome/spindle alignment (20.3 - 56.7% LPS vs. 0% control), and intracellular ROS generation were observed in oocytes matured with LPS (p < 0.05). Nitrite levels were also increased in the maturation medium derived from the oocytes matured with LPS (p < 0.05). These results indicate that LPS induces oxidative stress during IVM and affects oocyte maturation, including CGs migration and chromosome alignment of pig oocytes.

키워드

과제정보

We thank Hee-Jeong Lee for experimental assistance. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2013R1A6A3A04063769).

참고문헌

  1. Abeydeera LR, Wang WH, Prather RS, Day BN. 1998. Maturation in vitro of pig oocytes in protein-free culture media: Fertilization and subsequent embryo development in vitro. Biology of Reproduction 58:1316-1320. https://doi.org/10.1095/biolreprod58.5.1316
  2. Angrisano T, Pero R, Peluso S, Keller S, Sacchetti S, Bruni CB, Chiariotti L, Lembo F. 2010. LPS-induced IL-8 activation in human intestinal epithelial cells is accompanied by specific histone H3 acetylation and methylation changes. BMC microbiology 10:1-8. https://doi.org/10.1186/1471-2180-10-1
  3. Borges ED, Berteli TS, Reis TF, Silva AS, Vireque AA. 2020. Microbial contamination in assisted reproductive technology: Source, prevalence, and cost. Journal of Assisted Reproduction and Genetics 37:53-61. https://doi.org/10.1007/s10815-019-01640-5
  4. Bromfield JJ, Sheldon IM. 2011. Lipopolysaccharide initiates inflammation in bovine granulosa cells via the TLR4 pathway and perturbs oocyte meiotic progression in vitro. Endocrinology 152:5029-5040. https://doi.org/10.1210/en.2011-1124
  5. Coleman JW. 2001. Nitric oxide in immunity and inflammation. International Immunopharmacology 1:1397-1406. https://doi.org/10.1016/S1567-5769(01)00086-8
  6. Gao LL, Zhou CX, Zhang XL, Liu P, Jin Z, Zhu GY, Ma Y, Li J, Yang ZX, Zhang D. 2017. ZP3 is required for germinal vesicle breakdown in mouse oocyte meiosis. Scientific Reports 7:1-10. https://doi.org/10.1038/s41598-016-0028-x
  7. Gilbert RO. 2011. The effects of endometritis on the establishment of pregnancy in cattle. Reproduction, Fertility and Development 24:252-257. https://doi.org/10.1071/RD11915
  8. Herath S, Williams EJ, Lilly ST, Gilbert RO, Dobson H, Bryant CE, Sheldon IM. 2007. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134:683-693. https://doi.org/10.1530/REP-07-0229
  9. Hertl JA, Grohn YT, Leach JDG, Bar D, Bennett GJ, Gonzalez RN, Schukken YH. 2010. Effects of clinical mastitis caused by gram-positive and gram-negative bacteria and other organisms on the probability of conception in New York State Holstein dairy cows. Journal of Dairy Science 93:1551-1560. https://doi.org/10.3168/jds.2009-2599
  10. Hirao Y. 2011. Conditions affecting growth and developmental competence of mammalian oocytes in vitro. Animal Science Journal 82:187-197. https://doi.org/10.1111/j.1740-0929.2010.00870.x
  11. Karsch FJ, Battaglia DF, Breen KM, Debus N, Harris TG. 2002. Mechanisms for ovarian cycle disruption by immune/inflammatory stress. Stress 5:101-112. https://doi.org/10.1080/10253890290027868
  12. Li H, Guo S, Cai L, Ma W, Shi Z. 2017. Lipopolysaccharide and heat stress impair the estradiol biosynthesis in granulosa cells via increase of HSP70 and inhibition of smad3 phosphorylation and nuclear translocation. Cellular Signalling 30:130-141. https://doi.org/10.1016/j.cellsig.2016.12.004
  13. Magata F, Shimizu T. 2017. Effect of lipopolysaccharide on developmental competence of oocytes. Reproductive Toxicology 71:1-7. https://doi.org/10.1016/j.reprotox.2017.04.001
  14. Nakamura Y, Yamagata Y, Sugino N, Takayama H, Kato H. 2002. Nitric oxide inhibits oocyte meiotic maturation. Biology of Reproduction 67:1588-1592. https://doi.org/10.1095/biolreprod.102.005264
  15. Park BH, Kim UH, Jang SS, Yang SH, Lee EM, Kang DH, Kwon EG, Chung KY. 2016. Biological effects of dietary probiotics on blood characteristics in Hanwoo heifers subjected to lipopolysaccharide (LPS) challenge. Korean Journal of Agricultural Science 43:818-827. [in Korean] https://doi.org/10.7744/kjoas.20160086
  16. Pelzer ES, Allan JA, Cunningham K, Mengersen K, Allan JM, Launchbury T, Knox CL. 2011. Microbial colonization of follicular fluid: Alterations in cytokine expression and adverse assisted reproduction technology outcomes. Human Reproduction 26:1799-1812. https://doi.org/10.1093/humrep/der108
  17. Qin T, Yin Y, Yu Q, Yang Q. 2015. Bursopentin (BP5) protects dendritic cells from lipopolysaccharide-induced oxidative stress for immunosuppression. PLoS One 10:e0117477. https://doi.org/10.1371/journal.pone.0117477
  18. Raza H, John A, Shafarin J. 2016. Potentiation of LPS-induced apoptotic cell death in human hepatoma HepG2 cells by aspirin via ROS and mitochondrial dysfunction: Protection by N-acetyl cysteine. PloS One 11:e0159750. https://doi.org/10.1371/journal.pone.0159750
  19. Richards JS, Sharma SC, Falender AE, Lo YH. 2002. Expression of FKHR, FKHRL1, and AFX genes in the rodent ovary: Evidence for regulation by IGF-I, estrogen, and the gonadotropins. Molecular Endocrinology 16:580-599. https://doi.org/10.1210/mend.16.3.0806
  20. Rincon JA, Gindri PC, Mion B, Ferronato GA, Barbosa AA, Maffi AS, Pradiee J, Mondadori RG, Correa MN, Pegoraro LMC, Schneider A. 2019. Early embryonic development of bovine oocytes challenged with LPS in vitro or in vivo. Reproduction 158:453-463. https://doi.org/10.1530/rep-19-0316
  21. Romar R, Canovas S, Matas C, Gadea J, Coy P. 2019. Pig in vitro fertilization: Where are we and where do we go? Theriogenology 137:113-121. https://doi.org/10.1016/j.theriogenology.2019.05.045
  22. Sagar S, Kumar P, Behera RR, Pal A. 2014. Effects of CEES and LPS synergistically stimulate oxidative stress inactivates OGG1 signaling in macrophage cells. Journal of Hazardous Materials 278:236-249. https://doi.org/10.1016/j.jhazmat.2014.05.096
  23. Sharma A. 2013. Transgenerational epigenetic inheritance: focus on soma to germline information transfer. Progress in Biophysics and Molecular Biology 113:439-446. https://doi.org/10.1016/j.pbiomolbio.2012.12.003
  24. Sheldon IM, Rycroft AN, Dogan B, Craven M, Bromfield JJ, Chandler A, Simpson KW. 2010. Specific strains of Escherichia coli are pathogenic for the endometrium of cattle and cause pelvic inflammatory disease in cattle and mice. PLoS One 5:e9192. https://doi.org/10.1371/journal.pone.0009192
  25. Siristatidis C, Vogiatzi P, Varounis C, Askoxylaki M, Chrelias C, Papantoniou N. 2016. The effect of reactive oxygen species on embryo quality in IVF. In Vivo 30:149-153.
  26. Sun X, Xiu F, Pan B, Li Y, Haskins JT, Shen W, Li J. 2018. Antimicrobial peptide expression in swine granulosa cells in response to lipopolysaccharide. Theriogenology 119:80-90. https://doi.org/10.1016/j.theriogenology.2018.06.011
  27. Tornell J, Billig H, Hillensjo T. 1990. Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 3', 5'-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta Physiologica Scandinavica 139:511-517. https://doi.org/10.1111/j.1748-1716.1990.tb08953.x
  28. Tunctan B, Korkmaz B, Yildirim H, Tamer L, Atik U, Buharalioglu CK. 2005. Increased production of nitric oxide contributes to renal oxidative stress in endotoxemic rat. American Journal of Infectious Diseases 1:111-115. https://doi.org/10.3844/ajidsp.2005.111.115
  29. Williams EJ, Sibley K, Miller AN, Lane EA, Fishwick J, Nash DM, Herath S, England GCW, Dobson H, Sheldon IM. 2008. The effect of Escherichia coli lipopolysaccharide and tumour necrosis factor alpha on ovarian function. American Journal of Reproductive Immunology 60:462-473. https://doi.org/10.1111/j.1600-0897.2008.00645.x
  30. Zhao SJ, Pang YW, Zhao XM, Du WH, Hao HS, Zhu HB. 2017. Effects of lipopolysaccharide on maturation of bovine oocyte in vitro and its possible mechanisms. Oncotarget 8:4656-4667. https://doi.org/10.18632/oncotarget.13965
  31. Zorov DB, Juhaszova M, Sollott SJ. 2014. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiological Reviews 94:909-950. https://doi.org/10.1152/physrev.00026.2013