DOI QR코드

DOI QR Code

Cumulus and granulosa cell biomarkers: a good predictor for successful oocyte and embryo developmental competence in human in vitro fertilization

  • Yu, Eun Jeong (Department of Obstetrics and Gynecology, CHA Fertility Center Seoul Station, CHA University School of Medicine) ;
  • Lyu, Sang Woo (Department of Obstetrics and Gynecology, CHA Gangnam Medical Center, CHA University School of Medicine)
  • 투고 : 2021.05.24
  • 심사 : 2021.06.15
  • 발행 : 2021.06.30

초록

The oocyte quality is of great importance in infertility as it reflects the follicle developmental potential and further affects the embryo development, clinical pregnancy outcomes. The analysis of gene expression in somatic cells is an important study to better clinical in vitro fertilization (IVF) outcomes in embryo selection reflecting the appropriate communication between the oocyte and somatic cells. Specifically, somatic cell transcriptomic technology can help assess biomarkers of oocyte and embryo ability. The present article aims to overview the basic aspect of folliculogenesis and review studies involving changes in candidate gene expression of cumulus or granulosa cell related to clinical outcomes in human IVF.

키워드

참고문헌

  1. Zhu L, Zhang Y, Liu Y, Zhang R, Wu Y, Huang Y, et al. Maternal and live-birth outcomes of pregnancies following assisted reproductive technology: a retrospective cohort study. Sci Rep 2016;6:35141. https://doi.org/10.1038/srep35141
  2. Seli E, Robert C, Sirard MA. OMICS in assisted reproduction: possibilities and pitfalls. Mol Hum Reprod 2010;16:513-30. https://doi.org/10.1093/molehr/gaq041
  3. Ferraretti AP, Goossens V, de Mouzon J, Bhattacharya S, Castilla JA, Korsak V, et al. Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE. Hum Reprod 2012;27:2571-84. https://doi.org/10.1093/humrep/des255
  4. Simon AL, Kiehl M, Fischer E, Proctor JG, Bush MR, Givens C, et al. Pregnancy outcomes from more than 1,800 in vitro fertilization cycles with the use of 24-chromosome single-nucleotide polymorphism-based preimplantation genetic testing for aneuploidy. Fertil Steril 2018;110:113-21. https://doi.org/10.1016/j.fertnstert.2018.03.026
  5. Edson MA, Nagaraja AK, Matzuk MM. The mammalian ovary from genesis to revelation. Endocr Rev 2009;30:624-712. https://doi.org/10.1210/er.2009-0012
  6. Picton H, Briggs D, Gosden R. The molecular basis of oocyte growth and development. Mol Cell Endocrinol 1998;145:27-37. https://doi.org/10.1016/S0303-7207(98)00166-X
  7. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000;21:200-14. https://doi.org/10.1210/edrv.21.2.0394
  8. Gougeon A, Chainy GB. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 1987;81:433-42. https://doi.org/10.1530/jrf.0.0810433
  9. Magoffin DA. Ovarian theca cell. Int J Biochem Cell Biol 2005;37:1344-9. https://doi.org/10.1016/j.biocel.2005.01.016
  10. Yamoto M, Shima K, Nakano R. Gonadotropin receptors in human ovarian follicles and corpora lutea throughout the menstrual cycle. Horm Res 1992;37 Suppl 1:5-11. https://doi.org/10.1159/000182335
  11. Soyal SM, Amleh A, Dean J. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 2000;127:4645-54. https://doi.org/10.1242/dev.127.21.4645
  12. Clarke HJ. Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle. Wiley Interdiscip Rev Dev Biol 2018;7:e294. https://doi.org/10.1002/wdev.294
  13. Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 2007;120(Pt 8):1330-40. https://doi.org/10.1242/jcs.000968
  14. Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 2002;99:2890-4. https://doi.org/10.1073/pnas.052658699
  15. Reynaud K, Driancourt MA. Oocyte attrition. Mol Cell Endocrinol 2000;163:101-8. https://doi.org/10.1016/S0303-7207(99)00246-4
  16. Choi Y, Rajkovic A. Genetics of early mammalian folliculogenesis. Cell Mol Life Sci 2006;63:579-90. https://doi.org/10.1007/s00018-005-5394-7
  17. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;11:461-71. https://doi.org/10.1093/humupd/dmi020
  18. Hutt KJ, McLaughlin EA, Holland MK. Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol Hum Reprod 2006;12:61-9. https://doi.org/10.1093/molehr/gal010
  19. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122:829-38. https://doi.org/10.1530/reprod/122.6.829
  20. Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008;14:159-77. https://doi.org/10.1093/humupd/dmm040
  21. Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod 2010;16:715-25. https://doi.org/10.1093/molehr/gaq031
  22. Kathirvel M, Soundian E, Kumanan V. Differential expression dynamics of Growth differentiation factor9 (GDF9) and Bone morphogenetic factor15 (BMP15) mRNA transcripts during in vitro maturation of buffalo (Bubalus bubalis) cumulus-oocyte complexes. Springerplus 2013;2:206. https://doi.org/10.1186/2193-1801-2-206
  23. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 1999;13:1018-34. https://doi.org/10.1210/me.13.6.1018
  24. Gui LM, Joyce IM. RNA interference evidence that growth differentiation factor-9 mediates oocyte regulation of cumulus expansion in mice. Biol Reprod 2005;72:195-9. https://doi.org/10.1095/biolreprod.104.033357
  25. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001;15:854-66. https://doi.org/10.1210/mend.15.6.0662
  26. Ebrahimi B, Valojerdi MR, Eftekhari-Yazdi P, Baharvand H, Farrokhi A. IVM and gene expression of sheep cumulus-oocyte complexes following different methods of vitrification. Reprod Biomed Online 2010;20:26-34. https://doi.org/10.1016/j.rbmo.2009.10.020
  27. Kaivo-oja N, Jeffery LA, Ritvos O, Mottershead DG. Smad signalling in the ovary. Reprod Biol Endocrinol 2006;4:21. https://doi.org/10.1186/1477-7827-4-21
  28. Mazerbourg S, Hsueh AJ. Genomic analyses facilitate identification of receptors and signalling pathways for growth differentiation factor 9 and related orphan bone morphogenetic protein/growth differentiation factor ligands. Hum Reprod Update 2006;12:373-83. https://doi.org/10.1093/humupd/dml014
  29. Reader KL, Heath DA, Lun S, McIntosh CJ, Western AH, Littlejohn RP, et al. Signalling pathways involved in the cooperative effects of ovine and murine GDF9+BMP15-stimulated thymidine uptake by rat granulosa cells. Reproduction 2011;142:123-31. https://doi.org/10.1530/REP-10-0490
  30. Horie K, Fujita J, Takakura K, Kanzaki H, Suginami H, Iwai M, et al. The expression of c-kit protein in human adult and fetal tissues. Hum Reprod 1993;8:1955-62. https://doi.org/10.1093/oxfordjournals.humrep.a137967
  31. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002;296:1655-7. https://doi.org/10.1126/science.296.5573.1655
  32. Sobinoff AP, Nixon B, Roman SD, McLaughlin EA. Staying alive: PI3K pathway promotes primordial follicle activation and survival in response to 3MC-induced ovotoxicity. Toxicol Sci 2012;128:258-71. https://doi.org/10.1093/toxsci/kfs137
  33. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008;319:611-3. https://doi.org/10.1126/science.1152257
  34. Eppig JJ. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 1991;13:569-74. https://doi.org/10.1002/bies.950131105
  35. Wigglesworth K, Lee KB, O'Brien MJ, Peng J, Matzuk MM, Eppig JJ. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc Natl Acad Sci U S A 2013;110:E3723-9. https://doi.org/10.1073/pnas.1314829110
  36. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009;136:1869-78. https://doi.org/10.1242/dev.035238
  37. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009;8:2741-7. https://doi.org/10.4161/cc.8.17.9471
  38. van Montfoort AP, Geraedts JP, Dumoulin JC, Stassen AP, Evers JL, Ayoubi TA. Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. Mol Hum Reprod 2008;14:157-68. https://doi.org/10.1093/molehr/gam088
  39. McKenzie LJ, Pangas SA, Carson SA, Kovanci E, Cisneros P, Buster JE, 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
  40. Anderson RA, Sciorio R, Kinnell H, Bayne RA, Thong KJ, de Sousa PA, et al. Cumulus gene expression as a predictor of human oocyte fertilisation, embryo development and competence to establish a pregnancy. Reproduction 2009;138:629-37. https://doi.org/10.1530/rep-09-0144
  41. Wathlet S, Adriaenssens T, Segers I, Verheyen G, Van de Velde H, Coucke W, et al. Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients. Hum Reprod 2011;26:1035-51. https://doi.org/10.1093/humrep/der036
  42. Cillo F, Brevini TA, Antonini S, Paffoni A, Ragni G, Gandolfi F. Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 2007;134:645-50. https://doi.org/10.1530/REP-07-0182
  43. Wathlet S, Adriaenssens T, Segers I, Verheyen G, Janssens R, Coucke W, et al. New candidate genes to predict pregnancy outcome in single embryo transfer cycles when using cumulus cell gene expression. Fertil Steril 2012;98:432-9.e1-4. https://doi.org/10.1016/j.fertnstert.2012.05.007
  44. Lundin K, Bergh C, Hardarson T. Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum Reprod 2001;16:2652-7. https://doi.org/10.1093/humrep/16.12.2652
  45. Shoukir Y, Campana A, Farley T, Sakkas D. Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Hum Reprod 1997;12:1531-6. https://doi.org/10.1093/humrep/12.7.1531
  46. Sakkas D, Shoukir Y, Chardonnens D, Bianchi PG, Campana A. Early cleavage of human embryos to the two-cell stage after intracytoplasmic sperm injection as an indicator of embryo viability. Hum Reprod 1998;13:182-7. https://doi.org/10.1093/humrep/13.1.182
  47. Feuerstein P, Cadoret V, Dalbies-Tran R, Guerif F, Bidault R, Royere D. Gene expression in human cumulus cells: one approach to oocyte competence. Hum Reprod 2007;22:3069-77. https://doi.org/10.1093/humrep/dem336
  48. Assou S, Haouzi D, Mahmoud K, Aouacheria A, Guillemin Y, Pantesco V, et al. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol Hum Reprod 2008;14:711-9. https://doi.org/10.1093/molehr/gan067
  49. Lee KS, Joo BS, Na YJ, Yoon MS, Choi OH, Kim WW. Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J Assist Reprod Genet 2001;18:490-8. https://doi.org/10.1023/A:1016649026353
  50. Assidi M, Montag M, Van der Ven K, Sirard MA. Biomarkers of human oocyte developmental competence expressed in cumulus cells before ICSI: a preliminary study. J Assist Reprod Genet 2011;28:173-88. https://doi.org/10.1007/s10815-010-9491-7
  51. Hamel M, Dufort I, Robert C, Leveille MC, Leader A, Sirard MA. Identification of follicular marker genes as pregnancy predictors for human IVF: new evidence for the involvement of luteinization process. Mol Hum Reprod 2010;16:548-56. https://doi.org/10.1093/molehr/gaq051
  52. Gebhardt KM, Feil DK, Dunning KR, Lane M, Russell DL. Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil Steril 2011;96:47-52.e2. https://doi.org/10.1016/j.fertnstert.2011.04.033