Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

The use of pituitary adenylate cyclase-activating polypeptide in the pre-maturation system improves in vitro developmental competence from small follicles of porcine oocytes

  • Park, Kyu-Mi (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University) ;
  • Kim, Kyu-Jun (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University) ;
  • Jin, Minghui (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University) ;
  • Han, Yongquan (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University) ;
  • So, Kyoung-Ha (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University) ;
  • Hyun, Sang-Hwan (Institute for Stem Cell and Regenerative Medicine (ISCRM), Chungbuk National University)
  • Received : 2019.02.26
  • Accepted : 2019.06.26
  • Published : 2019.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: We investigated how pituitary adenylate cyclase-activating polypeptide (PACAP) affects embryonic development during pre-in vitro maturation (pre-IVM) using porcine oocytes isolated from small follicles. Methods: We divided the follicles into the experimental groups by size (SF, small follicles; MF, medium follicles) and treated with and without PACAP and cultured for 18 hours (PreSF[-]PACAP; without PACAP, Pre-SF[+]PACAP; with PACAP) before undergoing IVM. The gene expression related to extracellular matrix formation (amphiregulin, epiregulin, and hyaluronan synthase 2 [HAS2]) and apoptosis (Bcl-2-associated X [BAX], B-cell lymphoma 2, and cysteine-aspartic acid protease 3) was investigated after maturation. The impact on developmental competence was assessed by the cleavage and blastocyst rate and total cell number of blastocysts in embryos generated from parthenogenesis (PA) and in vitro fertilization (IVF). Results: Cleavage rates in the Pre-SF(+)PACAP after PA were significantly higher than SF and Pre-SF(-)PACAP (p<0.05). The cleavage rates between MF and Pre- SF(+)PACAP groups yielded no notable differences after IVF. Pre-SF(+)PACAP displayed the higher rate of blastocyst formation and greater total cell number than SF and Pre-SF(-)PACAP (p<0.05). Cumulus cells showed significant upregulation of HAS2 mRNA in the Pre-SF(+)PACAP compared to the SF (p<0.05). In comparison to other groups, the Pre-SF(+)PACAP group displayed a downregulation in mRNA expression of BAX in matured oocytes (p<0.05). Conclusion: The PACAP treatment during pre-IVM improved the developmental potential of porcine oocytes derived from SF by regulating cumulus expansion and apoptosis of oocytes.

Keywords

References

  1. Bode G, Clausing P, Gervais F, et al. The utility of the minipig as an animal model in regulatory toxicology. J Pharmacol Toxicol Methods 2010;62:196-220. https://doi.org/10.1016/j.vascn.2010.05.009
  2. Moor R, Trounson A. Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. J Reprod Fertil 1977;49:101-9. https://doi.org/10.1530/jrf.0.0490101
  3. Combelles CM, Cekleniak NA, Racowsky C, Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 2002;17:1006-16. https://doi.org/10.1093/humrep/17.4.1006
  4. Nevoral J, Orsak M, Klein P, et al. Cumulus cell expansion, its role in oocyte biology and perspectives of measurement: A review. Scientia Agriculturae Bohemica 2014;45:212-25. https://doi.org/10.1515/sab-2015-0002
  5. Su Y-Q, Sugiura K, Eppig JJ. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 2009;27:32-42. https://doi.org/10.1055/s-0028-1108008
  6. Tesfaye D, Ghanem N, Carter F, et al. Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro. Reprod Fertil Dev 2009;21:451-61. https://doi.org/10.1071/RD08190
  7. Kim E, Jeon Y, Kim DY, Lee E, Hyun S-H. Antioxidative effect of carboxyethylgermanium sesquioxide (Ge-132) on IVM of porcine oocytes and subsequent embryonic development after parthenogenetic activation and IVF. Theriogenology 2015;84:226-36. https://doi.org/10.1016/j.theriogenology.2015.03.006
  8. Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod 2010;25:2999-3011. https://doi.org/10.1093/humrep/deq246
  9. Richani D, Wang X, Zeng HT, Smitz J, Thompson JG, Gilchrist RB. Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence. Mol Reprod Dev 2014;81:422-35. https://doi.org/10.1002/mrd.22307
  10. Guimaraes AL, Pereira SA, Leme LO, Dode MA. Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology 2015;83:52-7. https://doi.org/10.1016/j.theriogenology.2014.07.042
  11. Cao H, Bian Y, Zhang F, et al. Functional role of Forskolin and PD166285 in the development of denuded mouse oocytes. Asian-Australas J Anim Sci 2018;31:344-53. https://doi.org/10.5713/ajas.17.0441
  12. Wu D, Cheung QC, Wen L, Li J. A growth-maturation system that enhances the meiotic and developmental competence of porcine oocytes isolated from small follicles. Biol Reprod 2006;75:547-54. https://doi.org/10.1095/biolreprod.106.051300
  13. Gilchrist RB, Zeng HT, Wang X, Richani D, Smitz J, Thompson JG. Reevaluation and evolution of the simulated physiological oocyte maturation system. Theriogenology 2015;84:656-7. https://doi.org/10.1016/j.theriogenology.2015.03.032
  14. Park B, Lee H, Lee Y, et al. Cilostamide and forskolin treatment during pre-IVM improves preimplantation development of cloned embryos by influencing meiotic progression and gap junction communication in pigs. Theriogenology 2016;86:757-65. https://doi.org/10.1016/j.theriogenology.2016.02.029
  15. Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JQ, Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum Reprod 2016;31:810-21. https://doi.org/10.1093/humrep/dew020
  16. Park K-M, So K-H, Hyun S-H. Pituitary adenylate cyclaseactivating polypeptide (PACAP) treatment during pre-maturation increases the maturation of porcine oocytes derived from small follicles. J Anim Reprod Biotechnol 2018;33:1-11. https://doi.org/10.12750/JET.2018.31.1.1
  17. Liu R-H, Li Y-H, Jiao L-H, Wang X-N, Wang H, Wang W-H. Extracellular and intracellular factors affecting nuclear and cytoplasmic maturation of porcine oocytes collected from different sizes of follicles. Zygote 2002;10:253-60. https://doi.org/10.1017/S0967199402002332
  18. Lee H, Elahi F, Lee J, Lee ST, Hyun S-H, Lee E. Supplement of cilostamide in growth medium improves oocyte maturation and developmental competence of embryos derived from small antral follicles in pigs. Theriogenology 2017;91:1-8. https://doi.org/10.1016/j.theriogenology.2016.12.015
  19. Pisegna JR, Wank SA. Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type I receptor. Proc Natl Acad Sci USA 1993;90:6345-9. https://doi.org/10.1073/pnas.90.13.6345
  20. Vaudry D, Falluel-Morel A, Bourgault S, et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 2009;61:283-357. https://doi.org/10.1124/pr.109.001370
  21. Barberi M, Di Paolo V, Latini S, Guglielmo MC, Cecconi S, Canipari R. Expression and functional activity of PACAP and its receptors on cumulus cells: effects on oocyte maturation. Mol Cell Endocrinol 2013;375:79-88. https://doi.org/10.1016/j.mce.2013.05.006
  22. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 2006;20:1352-65. https://doi.org/10.1210/me.2005-0504
  23. McKenzie LJ, Pangas SA, Carson SA, et al. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod 2004;19:2869-74. https://doi.org/10.1093/humrep/deh535
  24. Maeda-Sano K, Gotoh M, Morohoshi T, Someya T, Murofushi H, Murakami-Murofushi K. Cyclic phosphatidic acid and lysophosphatidic acid induce hyaluronic acid synthesis via CREB transcription factor regulation in human skin fibroblasts. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids 2014;1841:1256-63. https://doi.org/10.1016/j.bbalip.2014.05.004
  25. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol 2008;28:7001-11. https:// doi.org/10.1128/MCB.00732-08
  26. Khan DR, Guillemette C, Sirard M-A, Richard FJ. Transcriptomic analysis of cyclic AMP response in bovine cumulus cells. Physiol Genomics 2015;47:432-42. https://doi.org/10.1152/physiolgenomics.00043.2015
  27. Sugimura S, Yamanouchi T, Palmerini MG, Hashiyada Y, Imai K, Gilchrist RB. Effect of pre-in vitro maturation with cAMP modulators on the acquisition of oocyte developmental competence in cattle. J Reprod Dev 2018;64:233-41. https://doi.org/10.1262/jrd.2018-009
  28. Marchal R, Vigneron C, Perreau C, Bali-Papp A, Mermillod P. Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology 2002;57:1523-32. https://doi.org/10.1016/S0093-691X(02)00655-6
  29. Bernal SM, Heinzmann J, Herrmann D, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 2015;23:367-77. https://doi.org/10.1017/S0967199413000658
  30. Buell M, Chitwood JL, Ross PJ. cAMP modulation during sheep in vitro oocyte maturation delays progression of meiosis without affecting oocyte parthenogenetic developmental competence. Anim Reprod Sci 2015;154:16-24. https://doi.org/10.1016/j.anireprosci.2014.12.012
  31. Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JG, Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum Reprod 2016;31:810-21. https://doi.org/10.1093/humrep/dew020
  32. Host E, Mikkelsen AL, Lindenberg S, Smidt-Jensen S. Apoptosis in human cumulus cells in relation to maturation stage and cleavage of the corresponding oocyte. Acta Obstet Gynecol Scand 2000;79:936-40. https://doi.org/10.1034/j.1600-0412.2000.079011936.x
  33. Dejda A, Jolivel V, Bourgault S, et al. Inhibitory effect of PACAP on caspase activity in neuronal apoptosis: a better understanding towards therapeutic applications in neurodegenerative diseases. J Mol Neurosci 2008;36:26-37. https://doi.org/10.1007/s12031-008-9087-1
  34. Honda T, Coppola S, Ghibelli L, et al. GSH depletion enhances adenoviral bax-induced apoptosis in lung cancer cells. Cancer Gene Therapy 2004;11:249-55. https://doi.org/10.1038/sj.cgt.7700684
  35. Cande C, Cecconi F, Dessen P, Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 2002;115:4727-34. https://doi.org/10.1242/jcs.00210
  36. Wu R, Wyatt E, Chawla K, et al. Hexokinase II knockdown results in exaggerated cardiac hypertrophy via increased ROS production. EMBO Mol Med 2012;4:633-46. https://doi.org/10.1002/emmm.201200240
  37. Chen J, Zhang S, Li Y, Tang Z, Kong W. Hexokinase 2 overexpression promotes the proliferation and survival of laryngeal squamous cell carcinoma. Tumor Biol 2014;35:3743-53. https://doi.org/10.1007/s13277-013-1496-2
  38. Zuccotti M, Merico V, Sacchi L, et al. Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Dev Biol 2008;8:97. https://doi.org/10.1186/1471-213X-8-97