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Effect of acteoside on the re-localization and abnormal morphology of mitochondria in porcine oocytes during in vitro maturation

Abstract

Purpose

The aim of this study is to investigate the effect of acteoside, an antioxidant, on in vitro maturation (IVM) of oocytes to improve early parthenogenetic embryonic developmental competence.

Methods

Porcine immature oocytes (total 770) were cultured in IVM medium with acteoside at various concentrations, 0 (control), 10, 30, and 50 μM. Each group was assessed for maturation and subsequent development rates, reactive oxygen species (ROS) level (15 oocytes per group and four independent experiments performed), ultrastructure observation (15 oocytes per group), mitochondrial activity (30 oocytes per groups and three independent experiments performed), and expression patterns of apoptosis-related genes (100 expended parthenogenetic embryos per group and three independent experiment performed). Main outcome measures were the rates of IVM, blastocyst formation, ROS, mitochondria, and expression of apoptosis-related genes in oocytes treated with acteoside.

Result(s)

Addition of acteoside during IVM did not change the maturation efficiency of oocytes but improved the rate of blastocyst formation with significantly decreased ROS level. Moreover, in acteoside-treated oocytes, cytoplasmic maturation was improved with morphologically uniform distribution of mitochondria and lipid droplets in cytoplasm. Acteoside supplementation also increased the mRNA expression levels of antiapoptotic genes and reduced those of pro-apoptotic genes.

Conclusion(s)

Acteoside supplementation in IVM medium improves the oocyte quality and subsequent development of pre-implantation embryos that would eventually contribute to produce embryos with high embryonic development competence.

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References

  1. 1.

    Wei D, Zhang C, Xie J, Song X, Yin B, Liu Q, et al. Supplementation with low concentrations of melatonin improves nuclear maturation of human oocytes in vitro. J Assist Reprod Genet. 2013;30(7):933–8. doi:10.1007/s10815-013-0021-2.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Machtinger R, Combelles CM, Missmer SA, Correia KF, Williams P, Hauser R, et al. Bisphenol-A and human oocyte maturation in vitro. Hum Reprod. 2013;28(10):2735–45. doi:10.1093/humrep/det312.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Gomez E, Tarin JJ, Pellicer A. Oocyte maturation in humans: the role of gonadotropins and growth factors. Fertil Steril. 1993;60(1):40–6.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Alak BM, Coskun S, Friedman CI, Kennard EA, Kim MH, Seifer DB. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril. 1998;70(6):1126–30.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Krisher RL. The effect of oocyte quality on development. J Anim Sci. 2004;82(E-Suppl):E14–23.

    PubMed  Google Scholar 

  6. 6.

    Jimenez-Macedo AR, Izquierdo D, Urdaneta A, Anguita B, Paramio MT. Effect of roscovitine on nuclear maturation, MPF and MAP kinase activity and embryo development of prepubertal goat oocytes. Theriogenology. 2006;65(9):1769–82. doi:10.1016/j.theriogenology.2005.10.012.

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Cheng WM, Sun XL, An L, Zhu SE, Li XH, Li Y, et al. Effect of different parthenogenetic activation methods on the developmental competence of in vitro matured porcine oocytes. Anim Biotechnol. 2007;18(2):131–41. doi:10.1080/10495390601096148.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Chappaz E, Albornoz MS, Campos D, Che L, Palin MF, Murphy BD, et al. Adiponectin enhances in vitro development of swine embryos. Domest Anim Endocrinol. 2008;35(2):198–207. doi:10.1016/j.domaniend.2008.05.007.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Kim HS, Jeong YI, Lee JY, Jeong YW, Hossein MS, Hyun HS, et al. Effects of recombinant relaxin on in vitro maturation of porcine oocytes. J Vet Med Sci. 2010;72(3):333–7.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Yuan Y, Krisher RL. Effect of ammonium during in vitro maturation on oocyte nuclear maturation and subsequent embryonic development in pigs. Anim Reprod Sci. 2010;117(3–4):302–7. doi:10.1016/j.anireprosci.2009.05.012.

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Kim JS, Song BS, Lee SR, Yoon SB, Huh JW, Kim SU, et al. Supplementation with estradiol-17beta improves porcine oocyte maturation and subsequent embryo development. Fertil Steril. 2011;95(8):2582–4. doi:10.1016/j.fertnstert.2011.03.013.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Tareq KM, Akter QS, Khandoker MA, Tsujii H. Selenium and vitamin E improve the in vitro maturation, fertilization and culture to blastocyst of porcine oocytes. J Reprod Dev. 2012;58(6):621–8.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Jeong YW, Hossein MS, Bhandari DP, Kim YW, Kim JH, Park SW, et al. Effects of insulin-transferrin-selenium in defined and porcine follicular fluid supplemented IVM media on porcine IVF and SCNT embryo production. Anim Reprod Sci. 2008;106(1–2):13–24. doi:10.1016/j.anireprosci.2007.03.021.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Devasagayam TP, Tilak JC, Boloor KK, Sane KS, Ghaskadbi SS, Lele RD. Free radicals and antioxidants in human health: current status and future prospects. J Assoc Phys India. 2004;52:794–804.

    CAS  Google Scholar 

  15. 15.

    Ribarov SR, Benov LC. Relationship between the hemolytic action of heavy metals and lipid peroxidation. Biochim Biophys Acta. 1981;640(3):721–6.

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Evans MD, Dizdaroglu M, Cooke MS. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res. 2004;567(1):1–61. doi:10.1016/j.mrrev.2003.11.001.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Guerin P, El Mouatassim S, Menezo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 2001;7(2):175–89.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Nasr-Esfahani MH, Aitken JR, Johnson MH. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development. 1990;109(2):501–7.

    CAS  PubMed  Google Scholar 

  19. 19.

    Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10:49. doi:10.1186/1477-7827-10-49.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Watanabe H, Okawara S, Bhuiyan M, Fukui Y. Effect of lycopene on cytoplasmic maturation of porcine oocytes in vitro. Reprod Domest Anim = Zuchthygiene. 2010;45(5):838–45. doi:10.1111/j.1439-0531.2009.01365.x.

    CAS  PubMed  Google Scholar 

  21. 21.

    Kang JT, Koo OJ, Kwon DK, Park HJ, Jang G, Kang SK, et al. Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J Pineal Res. 2009;46(1):22–8. doi:10.1111/j.1600-079X.2008.00602.x.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Tao Y, Chen H, Tian NN, Huo DT, Li G, Zhang YH, et al. Effects of L-ascorbic acid, alpha-tocopherol and co-culture on in vitro developmental potential of porcine cumulus cells free oocytes. Reprod Domest Anim = Zuchthygiene. 2010;45(1):19–25. doi:10.1111/j.1439-0531.2008.01129.x.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Lee K, Wang C, Chaille JM, Machaty Z. Effect of resveratrol on the development of porcine embryos produced in vitro. J Reprod Dev. 2010;56(3):330–5.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Murai M, Tamayama Y, Nishibe S. Phenylethanoids in the herb of Plantago lanceolata and inhibitory effect on arachidonic acid-induced mouse ear edema. Planta Med. 1995;61(5):479–80. doi:10.1055/s-2006-958143.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Xiong Q, Kadota S, Tani T, Namba T. Antioxidative effects of phenylethanoids from Cistanche deserticola. Biol Pharm Bull. 1996;19(12):1580–5.

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Kyriakopoulou I, Magiatis P, Skaltsounis AL, Aligiannis N, Harvala C. Samioside, a new phenylethanoid glycoside with free-radical scavenging and antimicrobial activities from Phlomis samia. J Nat Prod. 2001;64(8):1095–7.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Saimaru H, Orihara Y. Biosynthesis of acteoside in cultured cells of Olea europaea. J Nat Med. 2010;64(2):139–45. doi:10.1007/s11418-009-0383-z.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Afanas’ev IB. Superoxide and nitric oxide in pathological conditions associated with iron overload: the effects of antioxidants and chelators. Curr Med Chem. 2005;12(23):2731–9.

    Article  PubMed  Google Scholar 

  29. 29.

    Brevini TA, Vassena R, Francisci C, Gandolfi F. Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol Reprod. 2005;72(5):1218–23. doi:10.1095/biolreprod.104.038141.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Liu L, Hammar K, Smith PJ, Inoue S, Keefe DL. Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium. 2001;30(6):423–33. doi:10.1054/ceca.2001.0251.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Brookes PS, Levonen AL, Shiva S, Sarti P, Darley-Usmar VM. Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med. 2002;33(6):755–64.

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Hao ZD, Liu S, Wu Y, Wan PC, Cui MS, Chen H, et al. Abnormal changes in mitochondria, lipid droplets, ATP and glutathione content, and Ca(2+) release after electro-activation contribute to poor developmental competence of porcine oocyte during in vitro ageing. Reprod Fertil Dev. 2009;21(2):323–32.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Torner H, Brussow KP, Alm H, Ratky J, Pohland R, Tuchscherer A, et al. Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology. 2004;61(9):1675–89. doi:10.1016/j.theriogenology.2003.09.013.

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007;77:21–49. doi:10.1016/S0070-2153(06)77002-8.

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Jansen RP, Burton GJ. Mitochondrial dysfunction in reproduction. Mitochondrion. 2004;4(5–6):577–600. doi:10.1016/j.mito.2004.07.038.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Sun QY, Wu GM, Lai L, Park KW, Cabot R, Cheong HT, et al. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction. 2001;122(1):155–63.

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction. 2004;128(3):269–80. doi:10.1530/rep.1.00240.

    Article  PubMed  Google Scholar 

  38. 38.

    Katayama M, Zhong Z, Lai L, Sutovsky P, Prather RS, Schatten H. Mitochondrial distribution and microtubule organization in fertilized and cloned porcine embryos: implications for developmental potential. Dev Biol. 2006;299(1):206–20. doi:10.1016/j.ydbio.2006.07.022.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Dell’Aquila ME, Ambruosi B, De Santis T, Cho YS. Mitochondrial distribution and activity in human mature oocytes: gonadotropin-releasing hormone agonist versus antagonist for pituitary down-regulation. Fertil Steril. 2009;91(1):249–55. doi:10.1016/j.fertnstert.2007.10.042.

    Article  PubMed  Google Scholar 

  40. 40.

    Liu S, Li Y, Gao X, Yan JH, Chen ZJ. Changes in the distribution of mitochondria before and after in vitro maturation of human oocytes and the effect of in vitro maturation on mitochondria distribution. Fertil Steril. 2010;93(5):1550–5. doi:10.1016/j.fertnstert.2009.03.050.

    Article  PubMed  Google Scholar 

  41. 41.

    Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod. 2010;83(6):909–18. doi:10.1095/biolreprod.110.084145.

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Lee KW, Kim HJ, Lee YS, Park HJ, Choi JW, Ha J, et al. Acteoside inhibits human promyelocytic HL-60 leukemia cell proliferation via inducing cell cycle arrest at G0/G1 phase and differentiation into monocyte. Carcinogenesis. 2007;28(9):1928–36. doi:10.1093/carcin/bgm126.

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Coticchio G, Dal-Canto M, Guglielmo MC, Mignini-Renzini M, Fadini R. Human oocyte maturation in vitro. Int J Dev Biol. 2012;56(10–12):909–18. doi:10.1387/ijdb.120135gv.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Kim DH, Ko DS, Lee HC, Lee HJ, Park WI, Kim SS, et al. Comparison of maturation, fertilization, development, and gene expression of mouse oocytes grown in vitro and in vivo. J Assist Reprod Genet. 2004;21(7):233–40.

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Dennery PA. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today. 2007;81(3):155–62. doi:10.1002/bdrc.20098.

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Noda Y, Matsumoto H, Umaoka Y, Tatsumi K, Kishi J, Mori T. Involvement of superoxide radicals in the mouse two-cell block. Mol Reprod Dev. 1991;28(4):356–60. doi:10.1002/mrd.1080280408.

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Kang JT, Kwon DK, Park SJ, Kim SJ, Moon JH, Koo OJ, et al. Quercetin improves the in vitro development of porcine oocytes by decreasing reactive oxygen species levels. J Vet Sci. 2013;14(1):15–20.

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Kwak SS, Cheong SA, Jeon Y, Lee E, Choi KC, Jeung EB, et al. The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology. 2012;78(1):86–101. doi:10.1016/j.theriogenology.2012.01.024.

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553–72. doi:10.1093/humupd/dmp016.

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Romek M, Gajda B, Rolka M, Smorag Z. Mitochondrial activity and morphology in developing porcine oocytes and pre-implantation non-cultured and cultured embryos. Reprod Domest Anim = Zuchthygiene. 2011;46(3):471–80. doi:10.1111/j.1439-0531.2010.01691.x.

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, et al. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol Reprod. 2001;64(3):904–9.

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Zhang W, Liu Y, An Z, Huang D, Qi Y, Zhang Y. Mediating effect of ROS on mtDNA damage and low ATP content induced by arsenic trioxide in mouse oocytes. Toxicol in Vitro. 2011;25(4):979–84. doi:10.1016/j.tiv.2011.03.009.

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Menezo Y, Dale B, Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote. 2010;18(4):357–65. doi:10.1017/S0967199410000286.

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495–516. doi:10.1080/01926230701320337.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 1993;74(4):597–608.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Jurisicova A, Latham KE, Casper RF, Casper RF, Varmuza SL. Expression and regulation of genes associated with cell death during murine preimplantation embryo development. Mol Reprod Dev. 1998;51(3):243–53. doi:10.1002/(SICI)1098-2795(199811)51:3<243::AID-MRD3>3.0.CO;2-P.

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Metcalfe AD, Hunter HR, Bloor DJ, Lieberman BA, Picton HM, Leese HJ, et al. Expression of 11 members of the BCL-2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation. Mol Reprod Dev. 2004;68(1):35–50. doi:10.1002/mrd.20055.

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant from the Next-Generation BioGreen 21 program (Grant No. PJ011359) funded by the Rural Development Administration, Republic of Korea. We are thankful to Dr. John Hammond in USDA-ARS for his scientific comments and writing support on the manuscript.

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Correspondence to Min Kyu Kim.

Additional information

Capsule Acteoside supplementation in IVM medium improves the oocyte quality and subsequent development of pre-implantation embryos that would eventually contribute to produce embryos with high embryonic development competence.

Keun Jung Kim and Ju Lan Chun contributed equally to this work.

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Supplement Figure 1
figure4

Active mitochondrial distribution in porcine oocytes matured in vitro with a 0 μM (control) or b 10 μM acteoside. Oocytes were stained with MitoTracker Red FM. Bar = 20 μm (30 oocytes per groups were used, and three independent experiments were performed) (GIF 115 kb)

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Kim, K.J., Chun, J.L., Lee, KB. et al. Effect of acteoside on the re-localization and abnormal morphology of mitochondria in porcine oocytes during in vitro maturation. J Assist Reprod Genet 33, 939–948 (2016). https://doi.org/10.1007/s10815-016-0729-x

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Keywords

  • Acteoside
  • IVM
  • ROS
  • Mitochondria
  • Apoptosis-related genes