한국동물생명공학회지 (Journal of Animal Reproduction and Biotechnology)

  • 제36권4호
  • /
  • Pages.183-188
  • /
  • 2021
  • /
  • 2671-4639(pISSN)
  • /
  • 2671-4663(eISSN)
한국동물생명공학회 (The Korean Society of Animal Reproduction and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

The role of sonic hedgehog signaling pathway in in vitro oocyte maturation

  • Lee, Sanghoon (Laboratory of Theriogenology, College of Veterinary Medicine, Chungnam National University) ;
  • Cho, Jongki (Laboratory of Theriogenology, College of Veterinary Medicine, Chungnam National University)
  • 투고 : 2021.11.18
  • 심사 : 2021.11.25
  • 발행 : 2021.12.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

In vitro maturation (IVM) of oocytes is the procedure where the immature oocytes are cultivated in a laboratory until they are mature. Since IVM oocytes generally have low developmental competence as compared to those matured in vivo, development of an optimal IVM culture system by fine-tuning culture conditions is crucial to maintain high quality. In-depth knowledge and a deep understanding of the in vivo physiology of oocyte maturation are pre-requisites to accomplish this. Within ovarian follicles, various signaling pathways that drive oocyte development and maturation regulate interaction between oocytes and surrounding somatic cells. This review discusses the sonic hedgehog (SHH) signaling pathway, which has been demonstrated to be intimately involved in folliculogenesis and oocyte maturation. Advances in elucidating the role of the SHH signaling pathway in oocyte maturation will aid attempts to improve the current inferior in vitro oocyte maturation system.

키워드

참고문헌

  1. Abd El-Aziz AH, Mahrous UE, Kamel SZ, Sabek AA. 2016. Factors influencing in vitro production of bovine embryos: a review. Asian J. Anim. Vet. Adv. 11:737-756. https://doi.org/10.3923/ajava.2016.737.756
  2. Appeltant R, Somfai T, Maes D, VAN Soom A, Kikuchi K. 2016. Porcine oocyte maturation in vitro: role of cAMP and oocyte-secreted factors - a practical approach. J. Reprod. Dev. 62:439-449. https://doi.org/10.1262/jrd.2016-016
  3. Boyer A, Lapointe E, Zheng X, Cowan RG, Li H, Quirk SM, DeMayo FJ, Richards JS, Boerboom D. 2010. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J. 24:3010-3025. https://doi.org/10.1096/fj.09-145789
  4. Choudhry Z, Rikani AA, Choudhry AM, Tariq S, Zakaria F, Asghar MW, Sarfraz MK, Haider K, Shafiq AA, Mobassarah NJ. 2014. Sonic hedgehog signalling pathway: a complex network. Ann. Neurosci. 21:28-31. https://doi.org/10.5214/ans.0972.7531.210109
  5. Das D and Arur S. 2017. Conserved insulin signaling in the regulation of oocyte growth, development, and maturation. Mol. Reprod. Dev. 84:444-459. https://doi.org/10.1002/mrd.22806
  6. Enomoto-Iwamoto M, Nakamura T, Aikawa T, Higuchi Y, Yuasa T, Yamaguchi A, Nohno T, Noji S, Matsuya T, Kurisu K, Koyama E, Pacifici M, Iwamoto M. 2000. Hedgehog proteins stimulate chondrogenic cell differentiation and cartilag formation. J. Bone Miner. Res. 15:1659-1668. https://doi.org/10.1359/jbmr.2000.15.9.1659
  7. Ferreira EM, Vireque AA, Adona PR, Meirelles FV, Ferriani RA, Navarro PA. 2009. Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71:836-848. https://doi.org/10.1016/j.theriogenology.2008.10.023
  8. Gougeon A. 1996. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 17:121-155. https://doi.org/10.1210/edrv-17-2-121
  9. Grondahl C. 2008. Oocyte maturation. Basic and clinical aspects of in vitro maturation (IVM) with special emphasis of the role of FF-MAS. Dan. Med. Bull. 55:1-16.
  10. Handrigan GR and Richman JM. 2010. Autocrine and paracrine Shh signaling are necessary for tooth morphogenesis, but not tooth replacement in snakes and lizards (Squamata). Dev. Biol. 337:171-186. https://doi.org/10.1016/j.ydbio.2009.10.020
  11. Hatirnaz S, Ata B, Hatirnaz ES, Dahan MH, Tannus S, Tan J, Tan SL. 2018. Oocyte in vitro maturation: a sytematic review. Turk. J. Obstet. Gynecol. 15:112-125. https://doi.org/10.4274/tjod.23911
  12. Hooper JE and Scott MP. 2005. Communicating with Hedgehogs. Nat. Rev. Mol. Cell Biol. 6:306-317. https://doi.org/10.1038/nrm1622
  13. Ingham PW and McMahon AP. 2001. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15:3059-3087. https://doi.org/10.1101/gad.938601
  14. Jeon YE, Hwangbo Y, Kim SY, Park CK. 2020. Alpha-linolenic acid enhances maturation and developmental competence via regulation of glutathione, cAMP and fatty acid accumulation during in vitro maturation of porcine oocytes. J. Anim. Reprod. Biotechnol. 35:357-365. https://doi.org/10.12750/JARB.35.4.357
  15. Jin JX, Lee S, Khoirinaya C, Oh A, Kim GA, Lee BC. 2016. Supplementation with spermine during in vitro maturation of porcine oocytes improves early embryonic development after parthenogenetic activation and somatic cell nuclear transfer. J. Anim. Sci. 94:963-970. https://doi.org/10.2527/jas.2015-9761
  16. Jing J, Jiang X, Chen J, Yao X, Zhao M, Li P, Pan Y, Ren Y, Liu W, Lyu L. 2017. Notch signaling pathway promotes the development of ovine ovarian follicular granulosa cells. Anim. Reprod. Sci. 181:69-78. https://doi.org/10.1016/j.anireprosci.2017.03.017
  17. Kidder GM and Vanderhyden BC. 2010. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 88:399-413. https://doi.org/10.1139/Y10-009
  18. Krisher RL. 2004. The effect of oocyte quality on development. J. Anim. Sci. 82 E-Suppl:E14-E23.
  19. Lee S, Jin JX, Khoirinaya C, Kim GA, Lee BC. 2016. Lanosterol influences cytoplasmic maturation of pig oocytes in vitro and improves preimplantation development of cloned embryos. Theriogenology 85:575-584. https://doi.org/10.1016/j.theriogenology.2015.09.041
  20. Lee S, Jin JX, Taweechaipaisankul A, Kim GA, Ahn C, Lee BC. 2017. Melatonin influences the sonic hedgehog signaling pathway in porcine cumulus oocyte complexes. J. Pineal Res. 63:e12424. https://doi.org/10.1111/jpi.12424
  21. Lee S, Jin JX, Taweechaipaisankul A, Kim GA, Ahn C, Lee BC. 2018. Sonic hedgehog signaling mediates resveratrol to improve maturation of pig oocytes in vitro and subsequent preimplantation embryo development. J. Cell. Physiol. 233:5023-5033. https://doi.org/10.1002/jcp.26367
  22. Lee S, Kang HG, Jeong PS, Nanjidsuren T, Song BS, Jin YB, Lee SR, Kim SU, Sim BW. 2020. Effect of oocyte quality assessed by brilliant cresyl blue (BCB) staining on cumulus cell expansion and sonic hedgehog signaling in porcine during in vitro maturation. Int. J. Mol. Sci. 21:4423. https://doi.org/10.3390/ijms21124423
  23. Lee S, Park EJ, Moon JH, Kim SJ, Song K, Lee BC. 2015. Sequential treatment with resveratrol-trolox improves development of porcine embryos derived from parthenogenetic activation and somatic cell nuclear transfer. Theriogenology 84:145-154. https://doi.org/10.1016/j.theriogenology.2015.02.021
  24. Li L, Shi X, Shi Y, Wang Z. 2021. The signaling pathways involved in ovarian follicle development. Front. Physiol. 12:730196. https://doi.org/10.3389/fphys.2021.730196
  25. Lonergan P and Fair T. 2016. Maturation of oocytes in vitro. Annu. Rev. Anim. Biosci. 4:255-268. https://doi.org/10.1146/annurev-animal-022114-110822
  26. Luciano AM and Sirard MA. 2018. Successful in vitro maturation of oocytes: a matter of follicular differentiation. Biol. Reprod. 98:162-169. https://doi.org/10.1093/biolre/iox149
  27. Marchal R, Caillaud M, Martoriati A, Gerard N, Mermillod P, Goudet G. 2003. Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan synthases, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biol. Reprod. 69:1013-1022. https://doi.org/10.1095/biolreprod.103.015602
  28. Marin Bivens CL, Grondahl C, Murray A, Blume T, Su YQ, Eppig JJ. 2004. Meiosis-activating sterol promotes the metaphase I to metaphase II transition and preimplantation developmental competence of mouse oocytes maturing in vitro. Biol. Reprod. 70:1458-1464. https://doi.org/10.1095/biolreprod.103.026351
  29. McMahon AP, Ingham PW, Tabin CJ. 2003. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53:1-114. https://doi.org/10.1016/S0070-2153(03)53002-2
  30. Moawad AR, Ghoneim IM, Darwish GM, Badr MR, El-Badry DA, EL-Wishy ABA. 2020. Factors affecting in vitro embryo production: insights into dromedary camel. J. Anim. Reprod. Biotechnol. 35:119-141. https://doi.org/10.12750/JARB.35.2.119
  31. Nguyen NT, Lin DP, Yen SY, Tseng JK, Chuang JF, Chen BY, Lin TA, Chang HH, Ju JC. 2009. Sonic hedgehog promotes porcine oocyte maturation and early embryo development. Reprod. Fertil. Dev. 21:805-815. https://doi.org/10.1071/RD08277
  32. Nilsson E and Skinner MK. 2001. Cellular interactions that control primordial follicle development and folliculogenesis. J. Soc. Gynecol. Investig. 8(1 Suppl Proceedings):S17-S20. https://doi.org/10.1177/1071557601008001S06
  33. Nusslein-Volhard C and Wieschaus E. 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287:795-801. https://doi.org/10.1038/287795a0
  34. Osawa H, Ohnishi H, Takano K, Noguti T, Mashima H, Hoshino H, Kita H, Sato K, Matsui H, Sugano K. 2006. Sonic hedgehog stimulates the proliferation of rat gastric mucosal cells through ERK activation by elevating intracellular calcium concentration. Biochem. Biophys. Res. Commun. 344:680-687. https://doi.org/10.1016/j.bbrc.2006.03.188
  35. Palma GA, Arganaraz ME, Barrera AD, Rodler D, Mutto AA, Sinowatz F. 2012. Biology and biotechnology of follicle development. ScientificWorldJournal 2012:938138.
  36. Paulini F, Silva RC, Rolo JL, Lucci CM. 2014. Ultrastructural changes in oocytes during folliculogenesis in domestic mammals. J. Ovarian Res. 7:102. https://doi.org/10.1186/s13048-014-0102-6
  37. Russell MC, Cowan RG, Harman RM, Walker AL, Quirk SM. 2007. The hedgehog signaling pathway in the mouse ovary. Biol. Reprod. 77:226-236. https://doi.org/10.1095/biolreprod.106.053629
  38. Saadeldin IM and Cho J. 2021. Current approaches for assisted oocyte maturation in camels. J. Anim. Reprod. Biotechnol. 36:162-167. https://doi.org/10.12750/JARB.36.3.162
  39. Saldana JI, Solanki A, Lau CI, Sahni H, Ross S, Furmanski AL, Ono M, Hollander G, Crompton T. 2016. Sonic Hedgehog regulates thymic epithelial cell differentiation. J. Autoimmun. 68:86-97. https://doi.org/10.1016/j.jaut.2015.12.004
  40. Spicer LJ, Sudo S, Aad PY, Wang LS, Chun SY, Ben-Shlomo I, Klein C, Hsueh AJ. 2009. The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells. Reproduction 138:329-339. https://doi.org/10.1530/REP-08-0317
  41. Sugimura S, Yamanouchi T, Palmerini MG, Hashiyada Y, Imai K, Gilchrist RB. 2018. Effect of pre-in vitro maturation with cAMP modulators on the acquisition of oocyte developmental competence in cattle. J. Reprod. Dev. 64:233-241. https://doi.org/10.1262/jrd.2018-009
  42. Wang DC, Huang JC, Lo NW, Chen LR, Mermillod P, Ma WL, Chiang HI, Ju JC. 2017. Sonic Hedgehog promotes in vitro oocyte maturation and term development of embryos in Taiwan native goats. Theriogenology 103:52-58. https://doi.org/10.1016/j.theriogenology.2017.07.029
  43. Wang HX, Li TY, Kidder GM. 2010. WNT2 regulates DNA synthesis in mouse granulosa cells through beta-catenin. Biol. Reprod. 82:865-875. https://doi.org/10.1095/biolreprod.109.080903
  44. Wijgerde M, Ooms M, Hoogerbrugge JW, Grootegoed JA. 2005. Hedgehog signaling in mouse ovary: Indian hedgehog and desert hedgehog from granulosa cells induce target gene expression in developing theca cells. Endocrinology 146:3558-3566. https://doi.org/10.1210/en.2005-0311