본문 바로가기
KERD
논문

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

1

조회

0

다운로드

0

인용

0

참고문헌

키워드

주제분류축산학

초록

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.

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.

참고문헌 (61)

  1. Hatırnaz Ş, "Oocyte in vitro maturation : a sytematic review", Turk J Obstet Gynecol, 15, pp.112~125 (2018)[DOI]
  2. Lee JB, "Effect of oocyte chromatin status in porcine follicles on the embryo development in vitro", Asian-Australas J Anim Sci, 32, pp.956~965 (2019)[DOI]
  3. Motlik J, "Meiotic competence in vitro of pig oocytes isolated from early antral follicles", J Reprod Fertil, 72, pp.323~328 (1984)[DOI]
  4. Pawlak P, "The consequences of porcine IVM medium supplementation with follicular fluid become reflected in embryo quality, yield and gene expression patterns", Sci Rep, 8, pp.15306~ (2018)[DOI]
  5. Wang QL, "Gonadotropins improve porcine oocyte maturation and embryo development through regulation of maternal gene expression", J Embryo Transf, 28, pp.361~371 (2013)[DOI]
  6. Ye J, "Physiological temperature variants and culture media modify meiotic progression and developmental potential of pig oocytes in vitro", Reproduction, 133, pp.877~886 (2007)[DOI]
  7. Abeydeera LR, "Effect of incubation temperature on in vitro maturation of porcine oocytes : nuclear maturation, fertilisation and developmental competence", Zygote, 9, pp.331~337 (2001)[DOI]
  8. Nie J, "Mogroside V improves porcine oocyte in vitro maturation and subsequent embryonic development", Theriogenology, 141, pp.35~40 (2020)[DOI]
  9. Almubarak AM, "Supplementation with Niacin during in vitro maturation improves the quality of porcine embryos", Theriogenology, 169, pp.36~46 (2021)[DOI]
  10. Alvarez GM, "Immature oocyte quality and maturational competence of porcine cumulus-oocyte complexes subpopulations", Biocell, 33, pp.167~177 (2009)[DOI]
  11. Chen Q, "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, pp.7113793~ (2022)[DOI]
  12. Suzuki H, "Dynamic changes of cumulus-oocyte cell communication during in vitro maturation of porcine oocytes", Biol Reprod, 63, pp.723~729 (2000)[DOI]
  13. Wongsrikeao P, "Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes", Reprod Domest Anim, 40, pp.166~170 (2005)[DOI]
  14. Baruffi R, "Nuclear and cytoplasmic maturation of human oocytes cultured in vitro", Fertil Steril, 82, pp.S265~S266 (2004)[DOI]
  15. Lin T, "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, 85, pp.665~681 (2018)[DOI]
  16. Van NTT, "Improve the developmental competence of porcine oocytes from small antral follicles by pre-maturation culture method", Theriogenology, 149, pp.139~148 (2020)[DOI]
  17. Funahashi H, "Preincubation of cumulus-oocyte complexes before exposure to gonadotropins improves the developmental competence of porcine embryos matured and fertilized in vitro", Theriogenology, 47, pp.679~686 (1997)[DOI]
  18. Chian RC, "Fertilization and early cleavage in vitro of ageing bovine oocytes after maturation in culture", Theriogenology, 37, pp.665~672 (1992)[DOI]
  19. Kikuchi K, "Decrease of histone H1kinase activity in relation to parthenogenetic activation of pig follicular oocytes matured and aged in vitro", J Reprod Fertil, 105, pp.325~330 (1995)[DOI]
  20. Nagai T, "Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol", Gamete Res, 16, pp.243~249 (1987)[DOI]
  21. Miao YL, "Oocyte aging : cellular and molecular changes, developmental potential and reversal possibility", Hum Reprod Update, 15, pp.573~585 (2009)[DOI]
  22. Dumont FJ, "The immunosuppressive macrolides FK-506 and rapamycin act as reciprocal antagonists in murine T cells", J Immunol, 144, pp.1418~1424 (1990)[DOI]
  23. Guertin DA, "Defining the role of mTOR in cancer", Cancer Cell, 12, pp.9~22 (2007)[DOI]
  24. Lee SE, "mTOR is required for asymmetric division through small GTPases in mouse oocytes", Mol Reprod Dev, 79, pp.356~366 (2012)[DOI]
  25. Song BS, "Induction of autophagy during in vitro maturation improves the nuclear and cytoplasmic maturation of porcine oocytes", Reprod Fertil Dev, 26, pp.974~981 (2014)[DOI]
  26. Lee SE, "Rapamycin rescues the poor developmental capacity of aged porcine oocytes", Asian-Australas J Anim Sci, 27, pp.635~647 (2014)[DOI]
  27. Kim DS, "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, 7, pp.614~620 (2020)[DOI]
  28. Livak KJ, "Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method", Methods, 25, pp.402~408 (2001)[DOI]
  29. Jia BY, "Inhibitory effects of astaxanthin on postovulatory porcine oocyte aging in vitro", Sci Rep, 10, pp.20217~ (2020)[DOI]
  30. Jiao Y, "Quercetin protects porcine oocytes from in vitro aging by reducing oxidative stress and maintaining the mitochondrial functions", Front Cell Dev Biol, 10, pp.915898~ (2022)[DOI]
  31. Pyeon DB, "The antioxidant dieckol reduces damage of oxidative stress-exposed porcine oocytes and enhances subsequent parthenotes embryo development", Mol Reprod Dev, 88, pp.349~361 (2021)[DOI]
  32. Fan HY, "Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals", Biol Reprod, 70, pp.535~547 (2004)[DOI]
  33. Liang CG, "Mechanisms regulating oocyte meiotic resumption : roles of mitogen-activated protein kinase", Mol Endocrinol, 21, pp.2037~2055 (2007)[DOI]
  34. Wehrend A, "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, 66, pp.175~184 (2001)[DOI]
  35. Kim HJ, "Effects of maturation duration and activation treatments on activation and development of porcine follicular oocytes", J Embryo Transf, 20, pp.25~33 (2005)
  36. Hua Z, "Effect of cumulus-oocyte complexes(COCs)culture duration on in vitro maturation and parthenogenetic development of pig oocyte", Afr J Biotechnol, 10, pp.867~873 (2011)
  37. Ma W, "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, 72, pp.373~383 (2005)[DOI]
  38. Steuerwald NM, "Post-ovulatory aging of mouse oocytes leads to decreased MAD2 transcripts and increased frequencies of premature centromere separation and anaphase", Mol Hum Reprod, 11, pp.623~630 (2005)[DOI]
  39. Lin FH, "Role of autophagy in modulating post-maturation aging of mouse oocytes", Cell Death Dis, 9, pp.308~ (2018)[DOI]
  40. Agarwal A, "Oxidative stress and its implications in female infertility –a clinician’s perspective", Reprod Biomed Online, 11, pp.641~650 (2005)[DOI]
  41. Tripathi A, "Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis", Free Radic Res, 43, pp.287~294 (2009)[DOI]
  42. Choi WJ, "Oxidative stress and tumor necrosis factor–α–induced alterations in metaphase II mouse oocyte spindle structure", Fertil Steril, 88, pp.1220~1231 (2007)[DOI]
  43. Downs SM, "The participation of energy substrates in the control of meiotic maturation in murine oocytes", Dev Biol, 162, pp.154~168 (1994)[DOI]
  44. Zhang X, "Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles", Cell Res, 16, pp.841~850 (2006)[DOI]
  45. Fatehi AN, "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, 13, pp.177~185 (2005)[DOI]
  46. Zhang X, "Redox-induced apoptosis of human oocytes in resting follicles in vitro", J Soc Gynecol Investig, 13, pp.451~458 (2006)[DOI]
  47. Tatemoto H, "Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation : role of cumulus cells", Biol Reprod, 63, pp.805~810 (2000)[DOI]
  48. Tatemoto H, "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, 65, pp.1800~1806 (2001)[DOI]
  49. Tatemoto H, "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, 71, pp.1150~1157 (2004)[DOI]
  50. Kikuchi K, "Successful piglet production after transfer of blastocysts produced by a modified in vitro system", Biol Reprod, 66, pp.1033~1041 (2002)[DOI]
  51. Pomar FJR, "Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species : a comparative study", Theriogenology, 63, pp.2254~2268 (2005)[DOI]
  52. Bernstein E, "Role for a bidentate ribonuclease in the initiation step of RNA interference", Nature, 409, pp.363~366 (2001)[DOI]
  53. Schöler HR, "Oct‐4: a germline‐specific transcription factor mapping to the mouse t‐complex", EMBO J, 9, pp.2185~2195 (1990)[DOI]
  54. Rosner MH, "A POUdomain transcription factor in early stem cells and germ cells of the mammalian embryo", Nature, 345, pp.686~692 (1990)[DOI]
  55. Nichols J, "Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4", Cell, 95, pp.379~391 (1998)[DOI]
  56. Chambers I, "Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells", Cell, 113, pp.643~655 (2003)[DOI]
  57. Mitsui K, "The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells", Cell, 113, pp.631~642 (2003)[DOI]
  58. Niwa H, "Interaction between Oct3", 4 and Cdx2 determines trophectoderm differentiation, 2005, pp.123, 917~929
  59. Wei Y, "Anti-apoptotic protein BCL-XL as a therapeutic vulnerability in gastric cancer", Animal Model Exp Med, 6, pp.245~254 (2023)[DOI]
  60. Yang J, "Prevention of apoptosis by Bcl-2:release of cytochrome c from mitochondria blocked", Science, 275, pp.1129~1132 (1997)[DOI]
  61. Garrido C, "Mechanisms of cytochrome c release from mitochondria", Cell Death Differ, 13, pp.1423~1433 (2006)[DOI]

관련 논문AI추천

Rapamycin Rescues the Poor Developmental Capacity of Aged Porcine Oocytes김은영, 박민지, 박세필, 이승은, 이준범, 정창진, 최현용, Jeremiah Jiman Moon아세아·태평양축산학회 · Animal Bioscience2014 · 제27권 제5호Rapamycin Influences the Efficiency of In vitro Fertilization and Development in the Mouse: A Role for Autophagic Activation신혜진, Geun-Kyung Lee, Hyunjung Jade Lim아세아·태평양축산학회 · Animal Bioscience2016 · 제29권 제8호Improving the meiotic competence of small antral follicle-derived porcine oocytes by using dibutyryl-cAMP and melatoninJitjumnong ๋Jakree, Tang Pin-Chi아세아·태평양축산학회 · Animal Bioscience2024 · 제37권 제6호The use of pituitary adenylate cyclase-activating polypeptide in the pre-maturation system improves in vitro developmental competence from small follicles of porcine oocytes김규준, 박규미, 소경하, 현상환, Minghui Jin, Yongquan Han아세아·태평양축산학회 · Animal Bioscience2019 · 제32권 제12호Effect of oocyte chromatin status in porcine follicles on the embryo development in vitro강정원, 신현영, 이민구, 이재은, 이주빈, 진동일, Tao Lin아세아·태평양축산학회 · Animal Bioscience2019 · 제32권 제7호Protodioscin protects porcine oocytes against H2O2-induced oxidative stress during in vitro maturation김소희, 박세필, 윤재욱, Kim Eun-Young, Lee Do-Geon, Lee Seung-Eun, Oh Seung-Hwan, Park Hyo-Jin, Pyeon Da-Bin아세아·태평양축산학회 · Animal Bioscience2023 · 제36권 제5호

이 간행물의 다른 논문 (15건)