Animal Bioscience

  • 제37권9호
  • /
  • Pages.1558-1567
  • /
  • 2024
  • /
  • 2765-0189(pISSN)
  • /
  • 2765-0235(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
권호 표지
DOI QR코드

DOI QR Code

Effect of cholesterol-loaded cyclodextrin treatment on boar sperm cryopreservation

  • Silong Zhang (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Hanbing Zhang (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Kexiong Liu (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Xiaoling Xu (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Yusheng Qin (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Linli Xiao (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Chunmei Zhou (Beijing Feifan Biotechnology Co., Ltd.) ;
  • Jianliang Wu (Beijing Zhongyu Pig Breeding Co., Ltd.) ;
  • Yan Liu (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Jiahua Bai (Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences)
  • 투고 : 2024.01.18
  • 심사 : 2024.05.02
  • 발행 : 2024.09.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective: This study investigated the efficacy of different concentrations of cholesterolloaded cyclodextrin (CLC) on cryopreservation in boar sperm quality. Methods: In this study, we treated boar sperm with different concentrations of CLC before freezing and analyzed the sperm cholesterol concentration, plasma membrane, acrosome integrity rate and total motility rate before and after freeze-thawing. We also investigated the levels of reactive oxygen species (ROS), malondialdehyde (MDA), adenosine triphosphate (ATP), and structural- and oxidative-damage related proteins in all groups after thawing. Results: The results revealed that the cholesterol concentration of the CLC-treated groups was higher than that of the control group, both before freezing and after thawing (p<0.05). The plasma membrane integrity rate, acrosome integrity rate, and total motility rate of sperm were also enhanced after thawing in the CLC-treated group (all p<0.05). Moreover, ROS and MDA production and ATP loss were reduced in CLC-treated sperm during freezing and thawing (p<0.05). Finally, CLC pretreatment partially prevented the consumption of various proteins involved in metabolism including capping actin protein of muscle Z-line subunit beta (CAPZB), heat shock protein 90 alpha family class A member 1 (HSP90AA1) and phosphoglycerate mutase 2 (PGAM2) (p<0.05). Conclusion: The CLC treatment increased cholesterol concentration and decreased structural injury and oxidative damage during boar sperm freezing and thawing, improving the efficacy of sperm cryopreservation in boar.

키워드

과제정보

This research was funded by grants from the National Key Research and Development Program, China (grant number 2022YFD1300302); the Scientific & Technological Innovation Ability Construction Project of the Beijing Academy of Agriculture and Forestry Sciences (grant number KJCX20210428) and the National Center of Technology Innovation for Pigs (grant number NCTIP-XD/B03).

참고문헌

  1. Yeste M. Recent advances in boar sperm cryopreservation: state of the art and current perspectives. Reprod Domest Anim 2015;50(Suppl 2):71-9. https://doi.org/10.1111/rda.12569 
  2. Hernandez M, Roca J, Calvete JJ, et al. Cryosurvival and in vitro fertilizing capacity postthaw is improved when boar spermatozoa are frozen in the presence of seminal plasma from good freezer boars. J Androl 2007;28:689-97. https://doi.org/10.2164/jandrol.107.002725 
  3. Zhu Z, Li R, Fan X, et al. Resveratrol improves boar sperm quality via 5'AMP-activated protein kinase activation during cryopreservation. Oxid Med Cell Longev 2019;2019:5921503. https://doi.org/10.1155/2019/5921503 
  4. Roca J, Rodriguez MJ, Gil MA, et al. Survival and in vitro fertility of boar spermatozoa frozen in the presence of superoxide dismutase and/or catalase. J Androl 2005;26:15-24. 
  5. Gadea J, Garcia-Vazquez F, Matas C, Gardon JC, Canovas S, Gumbao D. Cooling and freezing of boar spermatozoa: supplementation of the freezing media with reduced glutathione preserves sperm function. J Androl 2005;26:396-404. https://doi.org/10.2164/jandrol.04155 
  6. Basioura A, Tsakmakidis IA, Martinez EA, et al. Effect of astaxanthin in extenders on sperm quality and functional variables of frozen-thawed boar semen. Anim Reprod Sci 2020;218:106478. https://doi.org/10.1016/j.anireprosci.2020.106478 
  7. Aksoy M, Akman O, Lehimcioglu NC, Erdem H. Cholesterolloaded cyclodextrin enhances osmotic tolerance and inhibits the acrosome reaction in rabbit spermatozoa. Anim Reprod Sci 2010; 120:166-72. https://doi.org/10.1016/j.anireprosci.2010.02.014 
  8. Lone SA. Possible mechanisms of cholesterol-loaded cyclodextrin action on sperm during cryopreservation. Anim Reprod Sci 2018;192:1-5. https://doi.org/10.1016/j.anireprosci.2018.03.009 
  9. Moce E, Blanch E, Tomas C, Graham JK. Use of cholesterol in sperm cryopreservation: present moment and perspectives to future. Reprod Domest Anim 2010;45(Suppl 2):57-66. https://doi.org/10.1111/j.1439-0531.2010.01635.x 
  10. Parks JE, Lynch DV. Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology 1992;29:255-66. https://doi.org/10.1016/0011-2240(92)90024-v 
  11. Gharib R, Greige-Gerges H, Fourmentin S, Charcosset C, Auezova L. Liposomes incorporating cyclodextrin-drug inclusion complexes: current state of knowledge. Carbohydr Polym 2015;129: 175-86. https://doi.org/10.1016/j.carbpol.2015. 04.048 
  12. Takeo T, Hoshii T, Kondo Y, et al. Methyl-beta-cyclodextrin improves fertilizing ability of C57BL/6 mouse sperm after freezing and thawing by facilitating cholesterol efflux from the cells. Biol Reprod 2008;78:546-51. https://doi.org/10.1095/biolreprod.107.065359 
  13. Yoshimoto H, Takeo T, Irie T, Nakagata N. Fertility of coldstored mouse sperm is recovered by promoting acrosome reaction and hyperactivation after cholesterol efflux by methylbeta-cyclodextrin. Biol Reprod 2017;96:446-55. https://doi.org/10.1095/biolreprod.116.142901 
  14. Yadav HP, Kumar A, Shah N, et al. Effect of cholesterol loaded cyclodextrin supplementation on tyrosine phosphorylation and apoptosis like changes in frozen thawed Hariana bull spermatozoa. Theriogenology 2017;96:164-71. https://doi.org/10.1016/j.theriogenology.2017.04.016 
  15. Tomas C, Gomez-Fernandez J, Gomez-Izquierdo E, Moce E, de Mercado E. Addition of cholesterol-loaded cyclodextrins to the thawing extender: effects on boar sperm quality. Reprod Domest Anim 2014;49:427-32. https://doi.org/10.1111/rda.12291 
  16. Tomas C, Blanch E, Hernandez M, et al. Treating boar sperm with cholesterol-loaded cyclodextrins widens the sperm osmotic tolerance limits and enhances the in vitro sperm fertilising ability. Anim Reprod Sci 2011;129:209-20. https://doi.org/10.1016/j.anireprosci.2011.12.003 
  17. Tomas C, Blanch E, Fazeli A, Moce E. Effect of a pre-freezing treatment with cholesterol-loaded cyclodextrins on boar sperm longevity, capacitation dynamics, ability to adhere to porcine oviductal epithelial cells in vitro and DNA fragmentation dynamics. Reprod Fertil Dev 2013;25:935-46. https://doi.org/10.1071/rd12079 
  18. Tomas C, Blanch E, Cebrian B, Moce E. In vivo fertilising ability of frozen-thawed boar sperm treated with cholesterolloaded cyclodextrins prior to cryopreservation. Anim Reprod Sci 2013;140:77-82. https://doi.org/10.1016/j.anireprosci.2013.05.007 
  19. Lee YS, Lee S, Lee SH, Yang BK, Park CK. Effect of cholesterolloaded- cyclodextrin on sperm viability and acrosome reaction in boar semen cryopreservation. Anim Reprod Sci 2015;159:124-30. https://doi.org/10.1016/j.anireprosci.2015.06.006 
  20. Blanch E, Tomas C, Hernandez M, et al. Egg yolk and glycerol requirements for freezing boar spermatozoa treated with methyl β-cyclodextrin or cholesterol-loaded cyclodextrin. J Reprod Dev 2014;60:143-9. https://doi.org/10.1262/jrd.2013-073 
  21. Batissaco L, Arruda RP, Alves MBR, et al. Cholesterol-loaded cyclodextrin is efficient in preserving sperm quality of cryopreserved ram semen with low freezability. Reprod Biol 2020;20:14-24. https://doi.org/10.1016/j.repbio.2020.01.002 
  22. Schafer J, Waberski D, Jung M, Schulze M. Impact of holding and equilibration time on post-thaw quality of shipped boar semen. Anim Reprod Sci 2017;187:109-15. https://doi.org/10.1016/j.anireprosci.2017.10.014 
  23. Ringwelski JM, Beever JE, Knox RV. Effect of interval between inseminations when using frozen-thawed boar sperm on fertility and fetal paternity in mature gilts. Anim Reprod Sci 2013;137:197-204. https://doi.org/10.1016/j.anireprosci.2013.01.007 
  24. Knox RV, Ringwelski JM, McNamara KA, Aardsma M, Bojko M. The effect of extender, method of thawing, and duration of storage on in vitro fertility measures of frozenthawed boar sperm. Theriogenology 2015;84:407-12. https://doi.org/10.1016/j.theriogenology.2015.03.029 
  25. Fraser L, Zasiadczyk L, Strzezek J, Strzezek R, Karpiesiuk K. Freezability and fertility of frozen-thawed boar semen supplemented with ostrich egg yolk lipoproteins. Pol J Vet Sci 2018;21:255-63. https://doi.org/10.24425/119046 
  26. Pintus E, Kadlec M, Jovicic M, Sedmikova M, Ros-Santaella JL. Aminoguanidine protects boar spermatozoa against the deleterious effects of oxidative stress. Pharmaceutics 2018;10:212. https://doi.org/10.3390/pharmaceutics10040212 
  27. Navratil AM, Bliss SP, Berghorn KA, et al. Constitutive localization of the gonadotropin-releasing hormone (GnRH) receptor to low density membrane microdomains is necessary for GnRH signaling to ERK. J Biol Chem 2003;278:31593-602. https://doi.org/10.1074/jbc.M304273200 
  28. Min L, He S, Chen Q, Peng F, Peng H, Xie M. Comparative proteomic analysis of cellular response of human airway epithelial cells (A549) to benzo(a)pyrene. Toxicol Mech Methods 2011;21:374-82. https://doi.org/10.3109/153765162010.551555 
  29. Li R, Wu X, Zhu Z, et al. Polyamines protect boar sperm from oxidative stress in vitro. J Anim Sci 2022;100:skac069. https://doi.org/10.1093/jas/skac069 
  30. Moce E, Purdy PH, Graham JK. Treating ram sperm with cholesterol-loaded cyclodextrins improves cryosurvival. Anim Reprod Sci 2010;118:236-47. https://doi.org/10.1016/j.anireprosci.2009.06.013 
  31. Murphy C, English AM, Holden SA, Fair S. Cholesterolloaded- cyclodextrins improve the post-thaw quality of stallion sperm. Anim Reprod Sci 2014;145:123-9. https://doi.org/10.1016/j.anireprosci.2014.01.013 
  32. Naseer Z, Ahmad E, Aksoy M, et al. Protective effect of cholesterol-loaded cyclodextrin pretreatment against hydrogen peroxide induced oxidative damage in ram sperm. Cryobiology 2015;71:18-23. https://doi.org/10.1016/j.cryobiol.2015.06.007 
  33. Purdy PH, Graham JK. Effect of cholesterol-loaded cyclodextrin on the cryosurvival of bull sperm. Cryobiology 2004;48:36-45. https://doi.org/10.1016/j.cryobiol.2003.12.001 
  34. Moore AI, Squires EL, Graham JK. Adding cholesterol to the stallion sperm plasma membrane improves cryosurvival. Cryobiology 2005;51:241-9. https://doi.org/10.1016/j.cryobiol.2005.07.004 
  35. Blanch E, Tomas C, Graham JK, Moce E. Response of boar sperm to the treatment with cholesterol-loaded cyclodextrins added prior to cryopreservation. Reprod Domest Anim 2012;47:959-64. https://doi.org/10.1111/j.1439-0531.2012.01999.x 
  36. Salmon VM, Leclerc P, Bailey JL. Novel technical strategies to optimize cryopreservation of goat semen using cholesterolloaded cyclodextrin. Cryobiology 2017;74:19-24. https://doi.org/10.1016/j.cryobiol.2016.12.010 
  37. Khosravizadeh Z, Khodamoradi K, Rashidi Z, et al. Sperm cryopreservation and DNA methylation: possible implications for ART success and the health of offspring. J Assist Reprod Genet 2022;39:1815-24. https://doi.org/10.1007/s10815-022-02545-6 
  38. Kumar P, Mehta JS, Ravi SK, et al. Cholesterol loaded cyclodextrin supplementation enhances the cholesterol-to-phospholipid ratio and diminishes oxidative stress in jack spermatozoa during cryopreservation. J Equine Vet Sci 2020;94:103237. https://doi.org/10.1016/j.jevs.2020.103237 
  39. Mateo-Otero Y, Madrid-Gambin F, Llavanera M, et al. Sperm physiology and in vitro fertilising ability rely on basal metabolic activity: insights from the pig model. Commun Biol 2023;6:344. https://doi.org/10.1038/s42003-023-04715-3 
  40. Rodriguez-Gil JE, Bonet S. Current knowledge on boar sperm metabolism: comparison with other mammalian species. Theriogenology 2016;85:4-11. https://doi.org/10.1016/j.theriogenology.2015.05.005 
  41. Guo H, Gong Y, He B, Zhao R. Relationships between mitochondrial DNA content, mitochondrial activity, and boar sperm motility. Theriogenology 2017;87:276-83. https://doi.org/10.1016/j.theriogenology.2016.09.005 
  42. Kim S, Hooper S, Agca C, Agca Y. Post-thaw ATP supplementation enhances cryoprotective effect of iodixanol in rat spermatozoa. Reprod Biol Endocrinol 2016;14:5. https://doi.org/10.1186/s12958-016-0141-5 
  43. Zhu Z, Kawai T, Umehara T, Hoque SAM, Zeng W, Shimada M. Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free Radic Biol Med 2019;141:159-71. https://doi.org/10.1016/j.freeradbiomed.2019.06.018 
  44. Mostek A, Janta A, Majewska A, Ciereszko A. Bull sperm capacitation is accompanied by redox modifications of proteins. Int J Mol Sci 2021;22:7903. https://doi.org/10.3390/ijms22157903 
  45. Xiong Z, Zhang H, Huang B, et al. Expression pattern of prohibitin, capping actin protein of muscle Z-line beta subunit and tektin-2 gene in Murrah buffalo sperm and its relationship with sperm motility. Asian-Australas J Anim Sci 2018;31:1729-37. https://doi.org/10.5713/ajas.18.0025 
  46. Qiu X, Wang HY, Yang ZY, et al. Uncovering the prominent role of satellite cells in paravertebral muscle development and aging by single-nucleus RNA sequencing. Genes Dis 2023;10:2597-613. https://doi.org/10.1016/j.gendis.2023.01.005 
  47. Wojtusik J, Wang Y, Pukazhenthi BS. Pretreatment with cholesterol-loaded cyclodextrins prevents loss of motility associated proteins during cryopreservation of addra gazelle (Nanger dama ruficollis) spermatozoa. Cryobiology 2018;81:74-80. https://doi.org/10.1016/j.cryobiol.2018.02.007 
  48. Zhang XG, Hu S, Han C, Zhu QC, Yan GJ, Hu JH. Association of heat shock protein 90 with motility of post-thawed sperm in bulls. Cryobiology 2015;70:164-9. https://doi.org/10.1016/j.cryobiol.2014.12.010 
  49. Cao WL, Wang YX, Xiang ZQ, Li Z. Cryopreservationinduced decrease in heat-shock protein 90 in human spermatozoa and its mechanism. Asian J Androl 2003;5:43-6.