Journal of Animal Science and Technology

Korean Society of Animal Sciences and Technology (한국축산학회)
권호 표지
DOI QR코드

DOI QR Code

Rapamycin treatment during prolonged in vitro maturation enhances the developmental competence of immature porcine oocytes

  • Seung-Eun Lee (Stem Cell Research Center, Jeju National University) ;
  • Han-Bi Lee (Stem Cell Research Center, Jeju National University) ;
  • Jae-Wook Yoon (Stem Cell Research Center, Jeju National University) ;
  • Hyo-Jin Park (Stem Cell Research Center, Jeju National University) ;
  • So-Hee Kim (Stem Cell Research Center, Jeju National University) ;
  • Dong-Hun Han (Stem Cell Research Center, Jeju National University) ;
  • Eun-Seo Lim (Stem Cell Research Center, Jeju National University) ;
  • Eun-Young Kim (Stem Cell Research Center, Jeju National University) ;
  • Se-Pill Park (Stem Cell Research Center, Jeju National University)
  • Received : 2023.07.25
  • Accepted : 2023.09.23
  • Published : 2024.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Porcine oocytes undergo in vitro maturation (IVM) for 42-44 h. During this period, most oocytes proceed to metaphase and then to pro-metaphase if the nucleus has sufficiently matured. Forty-four hours is sufficient for oocyte nuclear maturation but not for full maturation of the oocyte cytoplasm. This study investigated the influences of extension of the IVM duration with rapamycin treatment on molecular maturation factors. The phospho-p44/42 mitogen-activated protein kinase (MAPK) level was enhanced in comparison with the total p44/42 MAPK level after 52 h of IVM. Oocytes were treated with and without 10 µM rapamycin (10 R and 0 R, respectively) and examined after 52 h of IVM, whereas control oocytes were examined after 44 h of IVM. Phospho-p44/42 MAPK activity was upregulated the 10 R and 0 R oocytes than in control oocytes. The expression levels of maternal genes were highest in 10 R oocytes and were higher in 0 R oocytes than in control oocytes. Reactive oxygen species (ROS) activity was dramatically increased in 0 R oocytes but was similar in 10 R and control oocytes. The 10 R group exhibited an increased embryo development rate, a higher total cell number per blastocyst, and decreased DNA fragmentation. The mRNA level of development-related (POU5F1 and NANOG) mRNA, oocyte-apoptotic (BCL2L1) genes were highest in 10 R blastocysts. These results suggest that prolonged IVM duration with rapamycin treatment represses ROS production and increases expression of molecular maturation factors. Therefore, this is a good strategy to enhance the developmental capacity in porcine oocytes.

Keywords

Acknowledgement

This work was supported by a grant (RS-2023-00254212) from Technology Commercialization Support Program, Ministry of Agriculture, Food and Rural Affairs, Korea.

References

  1. Hatirnaz S, Ata B, Hatirnaz ES, Dahan MH, Tannus S, Tan J, et al. Oocyte in vitro maturation: a sytematic review. Turk J Obstet Gynecol. 2018;15:112-25. https://doi.org/10.4274/tjod.23911
  2. Lee JB, Lee MG, Lin T, Shin HY, Lee JE, Kang JW, et al. Effect of oocyte chromatin status in porcine follicles on the embryo development in vitro. Asian-Australas J Anim Sci. 2019;32:956-65. https://doi.org/10.5713/ajas.18.0739
  3. Motlik J, Crozet N, Fulka J. Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J Reprod Fertil. 1984;72:323-8. https://doi.org/10.1530/jrf.0.0720323
  4. Pawlak P, Warzych E, Cieslak A, Malyszka N, Maciejewska E, Madeja ZE, et al. The consequences of porcine IVM medium supplementation with follicular fluid become reflected in embryo quality, yield and gene expression patterns. Sci Rep. 2018;8:15306. https://doi.org/10.1038/s41598-018-33550-4
  5. Wang QL, Zhao MH, Jin YX, Kim NH, Cui XS. Gonadotropins improve porcine oocyte maturation and embryo development through regulation of maternal gene expression. J Embryo Transf. 2013;28:361-71. https://doi.org/10.12750/JET.2013.28.4.361
  6. Ye J, Coleman J, Hunter MG, Craigon J, Campbell KHS, Luck MR. Physiological temperature variants and culture media modify meiotic progression and developmental potential of pig oocytes in vitro. Reproduction. 2007;133:877-86. https://doi.org/10.1530/REP-06-0318
  7. Abeydeera LR, Wang WH, Prather RS, Day BN. Effect of incubation temperature on in vitro maturation of porcine oocytes: nuclear maturation, fertilisation and developmental competence. Zygote. 2001;9:331-7. https://doi.org/10.1017/S0967199401001381
  8. Nie J, Yan K, Sui L, Zhang H, Zhang H, Yang X, et al. Mogroside V improves porcine oocyte in vitro maturation and subsequent embryonic development. Theriogenology. 2020;141:35-40. https://doi.org/10.1016/j.theriogenology.2019.09.010
  9. Almubarak AM, Kim E, Yu IJ, Jeon Y. Supplementation with Niacin during in vitro maturation improves the quality of porcine embryos. Theriogenology. 2021;169:36-46. https://doi.org/10.1016/j.theriogenology.2021.04.005
  10. Alvarez GM, Dalvit GC, Achi MV, Miguez MS, Cetica PD. Immature oocyte quality and maturational competence of porcine cumulus-oocyte complexes subpopulations. Biocell. 2009;33:167-77. https://doi.org/10.32604/biocell.2009.33.167
  11. Chen Q, Gao L, Li J, Yuan Y, Wang R, Tian Y, et al. α-Ketoglutarate improves meiotic maturation of porcine oocytes and promotes the development of pa embryos, potentially by reducing oxidative stress through the Nrf2 pathway. Oxid Med Cell Longev. 2022;2022:7113793. https://doi.org/10.1155/2022/7113793
  12. Suzuki H, Jeong BS, Yang X. Dynamic changes of cumulus-oocyte cell communication during in vitro maturation of porcine oocytes. Biol Reprod. 2000;63:723-9. https://doi.org/10.1095/biolreprod63.3.723
  13. Wongsrikeao P, Kaneshige Y, Ooki R, Taniguchi M, Agung B, Nii M, et al. Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim. 2005;40:166-70. https://doi.org/10.1111/j.1439-0531.2005.00576.x
  14. Baruffi R, Avelino KB, Petersen CG, Mauri AL, Garcia JM, Franco JG Jr. Nuclear and cytoplasmic maturation of human oocytes cultured in vitro. Fertil Steril. 2004;82:S265-6. https://doi.org/10.1016/j.fertnstert.2004.07.709
  15. Lin T, Lee JE, Kang JW, Oqani RK, Cho ES, Kim SB, et al. Melatonin supplementation during prolonged in vitro maturation improves the quality and development of poor-quality porcine oocytes via anti-oxidative and anti-apoptotic effects. Mol Reprod Dev. 2018;85:665-81. https://doi.org/10.1002/mrd.23052
  16. Van NTT, My LBA, Van Thuan N, Bui HT. Improve the developmental competence of porcine oocytes from small antral follicles by pre-maturation culture method. Theriogenology. 2020;149:139-48. https://doi.org/10.1016/j.theriogenology.2020.02.038
  17. Funahashi H, Cantley TC, Day BN. Preincubation of cumulus-oocyte complexes before exposure to gonadotropins improves the developmental competence of porcine embryos matured and fertilized in vitro. Theriogenology. 1997;47:679-86. https://doi.org/10.1016/S0093-691X(97)00026-5
  18. Chian RC, Nakahara H, Niwa K, Funahashi H. Fertilization and early cleavage in vitro of ageing bovine oocytes after maturation in culture. Theriogenology. 1992;37:665-72. https://doi.org/10.1016/0093-691X(92)90146-I
  19. Kikuchi K, Izaike Y, Noguchi J, Furukawa T, Daen FP, Naito K, et al. Decrease of histone H1 kinase activity in relation to parthenogenetic activation of pig follicular oocytes matured and aged in vitro. J Reprod Fertil. 1995;105:325-30. https://doi.org/10.1530/jrf.0.1050325
  20. Nagai T. Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. Gamete Res. 1987;16:243-9. https://doi.org/10.1002/mrd.1120160306
  21. Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15:573-85. https://doi.org/10.1093/humupd/dmp014
  22. Dumont FJ, Melino MR, Staruch MJ, Koprak SL, Fischer PA, Sigal NH. The immunosuppressive macrolides FK-506 and rapamycin act as reciprocal antagonists in murine T cells. J Immunol. 1990;144:1418-24. https://doi.org/10.4049/jimmunol.144.4.1418
  23. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell. 2007;12:9-22. https://doi.org/10.1016/j.ccr.2007.05.008
  24. Lee SE, Sun SC, Choi HY, Uhm SJ, Kim NH. mTOR is required for asymmetric division through small GTPases in mouse oocytes. Mol Reprod Dev. 2012;79:356-66. https://doi.org/10.1002/mrd.22035
  25. Song BS, Kim JS, Kim YH, Sim BW, Yoon SB, Cha JJ, et al. Induction of autophagy during in vitro maturation improves the nuclear and cytoplasmic maturation of porcine oocytes. Reprod Fertil Dev. 2014;26:974-81. https://doi.org/10.1071/RD13106
  26. Lee SE, Kim EY, Choi HY, Moon JJ, Park MJ, Lee JB, et al. Rapamycin rescues the poor developmental capacity of aged porcine oocytes. Asian-Australas J Anim Sci. 2014;27:635-47. https://doi.org/10.5713/ajas.2013.13816
  27. Kim DS, Kim SH, Yoon JT. Regulatory effect of apoptosis on morphological changes in cell mass of porcine blastocyst through supplementation of rapamycin during in vitro culture. J Adv Vet Anim Res. 2020;7:614-20. https://doi.org/10.5455/javar.2020.g459
  28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods. 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  29. Jia BY, Xiang DC, Shao QY, Zhang B, Liu SN, Hong QH, et al. Inhibitory effects of astaxanthin on postovulatory porcine oocyte aging in vitro. Sci Rep. 2020;10:20217. https://doi.org/10.1038/s41598-020-77359-6
  30. Jiao Y, Wang Y, Jiang T, Wen K, Cong P, Chen Y, et al. Quercetin protects porcine oocytes from in vitro aging by reducing oxidative stress and maintaining the mitochondrial functions. Front Cell Dev Biol. 2022;10:915898. https://doi.org/10.3389/fcell.2022.915898
  31. Pyeon DB, Lee SE, Yoon JW, Park HJ, Park CO, Kim SH, et al. The antioxidant dieckol reduces damage of oxidative stress-exposed porcine oocytes and enhances subsequent parthenotes embryo development. Mol Reprod Dev. 2021;88:349-61. https://doi.org/10.1002/mrd.23466
  32. Fan HY, Sun QY. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod. 2004;70:535-47. https://doi.org/10.1095/biolreprod.103.022830
  33. Liang CG, Su YQ, Fan HY, Schatten H, Sun QY. Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol Endocrinol. 2007;21:2037-55. https://doi.org/10.1210/me.2006-0408
  34. Wehrend A, Meinecke B. Kinetics of meiotic progression, M-phase promoting factor (MPF) and mitogen-activated protein kinase (MAP kinase) activities during in vitro maturation of porcine and bovine oocytes: species specific differences in the length of the meiotic stages. Anim Reprod Sci. 2001;66:175-84. https://doi.org/10.1016/S0378-4320(01)00094-X
  35. Kim HJ, Choi SH, Han MH, Son DS, Ryu IS, Kim IC, et al. Effects of maturation duration and activation treatments on activation and development of porcine follicular oocytes. J Embryo Transf. 2005;20:25-33.
  36. Hua Z, Zheng XM, Wei QX, Xu HQ, Wang YG, Liu XM, et al. Effect of cumulus-oocyte complexes (COCs) culture duration on in vitro maturation and parthenogenetic development of pig oocyte. Afr J Biotechnol. 2011;10:867-73.
  37. Ma W, Zhang D, Hou Y, Li YH, Sun QY, Sun XF, et al. Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol Reprod. 2005;72:373-83. https://doi.org/10.1095/biolreprod.104.030999
  38. Steuerwald NM, Steuerwald MD, Mailhes JB. Post-ovulatory aging of mouse oocytes leads to decreased MAD2 transcripts and increased frequencies of premature centromere separation and anaphase. Mol Hum Reprod. 2005;11:623-30. https://doi.org/10.1093/molehr/gah231
  39. Lin FH, Zhang WL, Li H, Tian XD, Zhang J, Li X, et al. Role of autophagy in modulating post-maturation aging of mouse oocytes. Cell Death Dis. 2018;9:308. https://doi.org/10.1038/s41419-018-0368-5
  40. Agarwal A, Gupta S, Sharma R. Oxidative stress and its implications in female infertility - a clinician's perspective. Reprod Biomed Online. 2005;11:641-50. https://doi.org/10.1016/S1472-6483(10)61174-1
  41. Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG, et al. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radic Res. 2009;43:287-94. https://doi.org/10.1080/10715760802695985
  42. Choi WJ, Banerjee J, Falcone T, Bena J, Agarwal A, Sharma RK. Oxidative stress and tumor necrosis factor-α-induced alterations in metaphase II mouse oocyte spindle structure. Fertil Steril. 2007;88:1220-31. https://doi.org/10.1016/j.fertnstert.2007.02.067
  43. Downs SM, Mastropolo AM. The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol. 1994;162:154-68. https://doi.org/10.1006/dbio.1994.1075
  44. Zhang X, Wu XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 2006;16:841-50. https://doi.org/10.1038/sj.cr.7310095
  45. Fatehi AN, Roelen BAJ, Colenbrander B, Schoevers EJ, Gadella BM, Bevers MM, et al. Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote. 2005;13:177-85. https://doi.org/10.1017/S0967199405003126
  46. Zhang X, Li XH, Ma X, Wang ZH, Lu S, Guo YL. Redox-induced apoptosis of human oocytes in resting follicles in vitro. J Soc Gynecol Investig. 2006;13:451-8. https://doi.org/10.1016/j.jsgi.2006.05.005
  47. Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod. 2000;63:805-10. https://doi.org/10.1095/biolreprod63.3.805
  48. Tatemoto H, Ootaki K, Shigeta K, Muto N. Enhancement of developmental competence after in vitro fertilization of porcine oocytes by treatment with ascorbic acid 2-O-α-glucoside during in vitro maturation. Biol Reprod. 2001;65:1800-6. https://doi.org/10.1095/biolreprod65.6.1800
  49. Tatemoto H, Muto N, Sunagawa I, Shinjo A, Nakada T. Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol Reprod. 2004;71:1150-7. https://doi.org/10.1095/biolreprod.104.029264
  50. Kikuchi K, Onishi A, Kashiwazaki N, Iwamoto M, Noguchi J, Kaneko H, et al. Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol Reprod. 2002;66:1033-41. https://doi.org/10.1095/biolreprod66.4.1033
  51. Pomar FJR, Teerds KJ, Kidson A, Colenbrander B, Tharasanit T, Aguilar B, et al. Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology. 2005;63:2254-68. https://doi.org/10.1016/j.theriogenology.2004.10.015
  52. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 2001;409:363-6. https://doi.org/10.1038/35053110
  53. Scholer HR, Dressler GR, Balling R, Rohdewohld H, Gruss P. Oct-4: a germline-specific transcription factor mapping to the mouse t-complex. EMBO J. 1990;9:2185-95. https://doi.org/10.1002/j.1460-2075.1990.tb07388.x
  54. Rosner MH, Vigano MA, Ozato K, Timmons PM, Poirie F, Rigby PWJ, et al. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature. 1990;345:686-92. https://doi.org/10.1038/345686a0
  55. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell. 1998;95:379-91. https://doi.org/10.1016/S0092-8674(00)81769-9
  56. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113:643-55. https://doi.org/10.1016/S0092-8674(03)00392-1
  57. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113:631-42. https://doi.org/10.1016/S0092-8674(03)00393-3
  58. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell. 2005;123:917-29. https://doi.org/10.1016/j.cell.2005.08.040
  59. Wei Y, Zhang L, Wang C, Li Z, Luo M, Xie G, et al. Anti-apoptotic protein BCL-XL as a therapeutic vulnerability in gastric cancer. Animal Model Exp Med. 2023;6:245-54. https://doi.org/10.1002/ame2.12330
  60. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 1997;275:1129-32. https://doi.org/10.1126/science.275.5303.1129
  61. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ. 2006;13:1423-33. https://doi.org/10.1038/sj.cdd.4401950