Effect of human granulosa cells vitrification on the expression of oocyte secreted factors

Batara Sirait; Budi Wiweko; R. Muharram; Ahmad Aulia Jusuf; Ichramsjah A. Rachman; Arief Boediono

doi:10.15562/bmj.v12i2.4600

Effect of human granulosa cells vitrification on the expression of oocyte secreted factors

Batara Sirait ,

Budi Wiweko ,

R. Muharram ,

Ahmad Aulia Jusuf ,

Ichramsjah A. Rachman ,

Arief Boediono ,

pdf |
DOI: https://doi.org/10.15562/bmj.v12i2.4600 |
Published: 2023-07-05

Abstract

Background: Oocyte vitrification is a helpful fertility preservation technique for women at risk of losing their ovarian functions. Meanwhile, its application extends with the emerging trend of delayed childbearing, postponed marriage, and further diverse ethical, medical, legal, and social implications. Whereas its effect on oocytes has been widely elucidated, the potential impact of this procedure on the biological functions of granulosa cells remains poorly understood. The present study aimed to assess vitrification’s effect on the granulosa cells (GCs).

Methods: 35 women with polycystic ovary syndromes who underwent in vitro fertilization (IVF) in Morula IVF Jakarta Clinic were recruited. The expression of prominent oocytes secreted factors (OSFs), including GDF-9 and BMP-15, were measured at messenger RNA (mRNA) levels. GCs from mature and immature oocytes were collected and calculated separately. Relative expression of GDF-9 and BMP-15 was quantified by a real-time quantitative PCR (RT-qPCR). All of the data was analyzed by using SPSS. Bivariate analysis used the Mann-Whitney test at a 95% confidence level. A significant p-value was ≤ 0.05.

Results: The mean age of subjects was 32,39 ± 3,33 years old, with the mean duration of infertility being six years. The mean BMI, anti-Mullerian hormone (AMH) level, and antral follicle count (AFC) were 24.04 kg/m2, 3.43 ng/mL, and 15 follicles, respectively. The basal FSH, LH, estradiol, and progesterone were at the normal level. The expression of GDF-9 decreased significantly (0.5-fold, p < 0.01) in the immature vitrified GC group but was not in the mature-vitrified GC group. Meanwhile, the expression of BMP-15 was stable in all examined groups (P>0.05).

Conclusion: Our results suggest that vitrification may alter oocyte maturation, as demonstrated by reduced GDF-9 expression in the immature vitrified GC group.

References

Chen C. Pregnancy After Human Oocyte Cryopreservation. Lancet. 1986;327(8486):884–6.
Pai H, Baid R, Palshetkar N, Pai A, Pai R, Palshetkar R. Oocyte Cryopreservation - Current Scenario and Future Perspectives: A Narrative Review. J Hum Reprod Sci. 2021 Oct;14(4):340.
Inhorn MC, Birenbaum-Carmeli D, Westphal LM, Doyle J, Gleicher N, Meirow D, et al. Ten pathways to elective egg freezing: a binational analysis. J Assist Reprod Genet. 2018 Nov;35(11):2003–11.
He X, Park EYH, Fowler A, Yarmush ML, Toner M. Vitrification by Ultra-fast Cooling at a Low Concentration of Cryoprotectants in a Quartz Microcapillary: A Study Using Murine Embryonic Stem Cells. Cryobiology. 2008 Jun;56(3):223.
Bojic S, Murray A, Bentley BL, Spindler R, Pawlik P, Cordeiro JL, et al. Winter is coming: the future of cryopreservation. BMC Biol 2021 191. 2021 Mar;19(1):1–20.
Zhang X, Catalano PN, Gurkan UA, Khimji I, Demirci U. Emerging technologies in medical applications of minimum volume vitrification. Nanomedicine (Lond). 2011 Aug;6(6):1115.
Chen H, Zhang L, Meng L, Liang L, Zhang C. Advantages of vitrification preservation in assisted reproduction and potential influences on imprinted genes. Clin Epigenetics. 2022 Dec;14(1).
Turathum B, Saikhun K, Sangsuwan P, Kitiyanant Y. Effects of vitrification on nuclear maturation, ultrastructural changes and gene expression of canine oocytes. Reprod Biol Endocrinol. 2010;8:1–9.
Rao BS, Mahesh YU, Charan KV, Suman K, Sekhar N, Shivaji S. Effect of vitrification on meiotic maturation and expression of genes in immature goat cumulus oocyte complexes. Cryobiology. 2012;64(3):176–84. Available from: http://dx.doi.org/10.1016/j.cryobiol.2012.01.005
Di Pietro C, Vento M, Guglielmino MR, Borz P, Santonocito M, Ragusa M, et al. Molecular profiling of human oocytes after vitrification strongly suggests that they are biologically comparable with freshly isolated gametes. Fertil Steril. 2010;94(7):2804–7.
D’Aurora M, Budani MC, Franchi S, Sarra A, Stuppia L, Tiboni GM, et al. Dynactin pathway-related gene expression is altered by aging, but not by vitrification. Reprod Toxicol. 2019 Sep;88:48–55.
Sirait B, Jusuf A, Wiweko B, Handayani N, Aubry D, Muharam R. Potential use of immature oocyte to improve fertility preservation outcome: A narrative review. J Hum Reprod Sci. 2022;15(1):3–11.
Jahromi BN, Mosallanezhad Z, Matloob N, Davari M, Ghobadifar MA. The potential role of granulosa cells in the maturation rate of immature human oocytes and embryo development: A co-culture study. Clin Exp Reprod Med. 2015;42(3):111–7.
Fontana J, Martínková S, Petr J, Žalmanová T, Trnka J. Metabolic cooperation in the ovarian follicle. Physiol Res. 2020 Feb;69(1):33–48.
Turathum B, Gao EM, Chian RC. The Function of Cumulus Cells in Oocyte Growth and Maturation and in Subsequent Ovulation and Fertilization. Cells. 2021 Sep;10(9).
Fauser BCJM, Tarlatzis, Fauser, Chang, Aziz, Legro, et al. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004 Jan;19(1):41–7.
Bowolaksono A, Sundari AM, Fauzi M, Maidarti M, Wiweko B, Mutia K, et al. Anti-Müllerian hormone independently affect mtDNA copy number in human granulosa cells. J Ovarian Res. 2022 Dec;15(1).
Azari M, Kafi M, Ebrahimi B, Fatehi R, Jamalzadeh M. Oocyte maturation, embryo development and gene expression following two different methods of bovine cumulus-oocyte complexes vitrification. Vet Res Commun. 2017;41(1):49–56. Available from: http://dx.doi.org/10.1007/s11259-016-9671-8
Mofarahe ZS, Novin MG, Salehnia M. Folliculogenesis-Associated Genes Expression in Human Vitrified Ovarian Tissue after Xenotransplantation in γ-Irradiated Mice. Cell J. 2020;22(3):350–7.
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(1):1–6.
Belli M, Shimasaki S. Molecular Aspects and Clinical Relevance of GDF9 and BMP15 in Ovarian Function [Internet]. 1st ed. Vol. 107, Vitamins and Hormones. Elsevier Inc.; 2018. 317–348 p. Available from: http://dx.doi.org/10.1016/bs.vh.2017.12.003
Abdel-Ghani MA, El-Sherry TM, Abdelhafeez HH. Effect of growth differentiation factor-9 (GDF-9) on the progression of buffalo follicles in vitrified-warmed ovarian tissues. Reprod Domest Anim. 2016 Oct;51(5):795–803.
De los Reyes M, Rojas C, Parraguez VH, Palomino J. Expression of growth differentiation factor 9 (GDF-9) during invitro maturation in canine oocytes. Theriogenology. 2013 Oct;80(6):587–96.
Mofarahe ZS, Salehnia M, Novin MG, Ghorbanmehr N, Fesharaki MG. Expression of Folliculogenesis-Related Genes inVitrified Human Ovarian Tissue afterTwo Weeks In Vitro Culture. Cell J. 2017;19(1):18.
Habibi A, Farrokhi N, Silva FM Da, Bettencourt BF, Bruges-Armas J, Amidi F, et al. The effects of vitrification on gene expression in mature mouse oocytes by nested quantitative PCR. J Assist Reprod Genet. 2010 Nov;27(11):599.

[1] Chen C. Pregnancy After Human Oocyte Cryopreservation. Lancet. 1986;327(8486):884–6.

[2] Pai H, Baid R, Palshetkar N, Pai A, Pai R, Palshetkar R. Oocyte Cryopreservation - Current Scenario and Future Perspectives: A Narrative Review. J Hum Reprod Sci. 2021 Oct;14(4):340.

[3] Inhorn MC, Birenbaum-Carmeli D, Westphal LM, Doyle J, Gleicher N, Meirow D, et al. Ten pathways to elective egg freezing: a binational analysis. J Assist Reprod Genet. 2018 Nov;35(11):2003–11.

[4] He X, Park EYH, Fowler A, Yarmush ML, Toner M. Vitrification by Ultra-fast Cooling at a Low Concentration of Cryoprotectants in a Quartz Microcapillary: A Study Using Murine Embryonic Stem Cells. Cryobiology. 2008 Jun;56(3):223.

[5] Bojic S, Murray A, Bentley BL, Spindler R, Pawlik P, Cordeiro JL, et al. Winter is coming: the future of cryopreservation. BMC Biol 2021 191. 2021 Mar;19(1):1–20.

[6] Zhang X, Catalano PN, Gurkan UA, Khimji I, Demirci U. Emerging technologies in medical applications of minimum volume vitrification. Nanomedicine (Lond). 2011 Aug;6(6):1115.

[7] Chen H, Zhang L, Meng L, Liang L, Zhang C. Advantages of vitrification preservation in assisted reproduction and potential influences on imprinted genes. Clin Epigenetics. 2022 Dec;14(1).

[8] Turathum B, Saikhun K, Sangsuwan P, Kitiyanant Y. Effects of vitrification on nuclear maturation, ultrastructural changes and gene expression of canine oocytes. Reprod Biol Endocrinol. 2010;8:1–9.

[9] Rao BS, Mahesh YU, Charan KV, Suman K, Sekhar N, Shivaji S. Effect of vitrification on meiotic maturation and expression of genes in immature goat cumulus oocyte complexes. Cryobiology. 2012;64(3):176–84. Available from: http://dx.doi.org/10.1016/j.cryobiol.2012.01.005

[10] Di Pietro C, Vento M, Guglielmino MR, Borz P, Santonocito M, Ragusa M, et al. Molecular profiling of human oocytes after vitrification strongly suggests that they are biologically comparable with freshly isolated gametes. Fertil Steril. 2010;94(7):2804–7.

[11] D’Aurora M, Budani MC, Franchi S, Sarra A, Stuppia L, Tiboni GM, et al. Dynactin pathway-related gene expression is altered by aging, but not by vitrification. Reprod Toxicol. 2019 Sep;88:48–55.

[12] Sirait B, Jusuf A, Wiweko B, Handayani N, Aubry D, Muharam R. Potential use of immature oocyte to improve fertility preservation outcome: A narrative review. J Hum Reprod Sci. 2022;15(1):3–11.

[13] Jahromi BN, Mosallanezhad Z, Matloob N, Davari M, Ghobadifar MA. The potential role of granulosa cells in the maturation rate of immature human oocytes and embryo development: A co-culture study. Clin Exp Reprod Med. 2015;42(3):111–7.

[14] Fontana J, Martínková S, Petr J, Žalmanová T, Trnka J. Metabolic cooperation in the ovarian follicle. Physiol Res. 2020 Feb;69(1):33–48.

[15] Turathum B, Gao EM, Chian RC. The Function of Cumulus Cells in Oocyte Growth and Maturation and in Subsequent Ovulation and Fertilization. Cells. 2021 Sep;10(9).

[16] Fauser BCJM, Tarlatzis, Fauser, Chang, Aziz, Legro, et al. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004 Jan;19(1):41–7.

[17] Bowolaksono A, Sundari AM, Fauzi M, Maidarti M, Wiweko B, Mutia K, et al. Anti-Müllerian hormone independently affect mtDNA copy number in human granulosa cells. J Ovarian Res. 2022 Dec;15(1).

[18] Azari M, Kafi M, Ebrahimi B, Fatehi R, Jamalzadeh M. Oocyte maturation, embryo development and gene expression following two different methods of bovine cumulus-oocyte complexes vitrification. Vet Res Commun. 2017;41(1):49–56. Available from: http://dx.doi.org/10.1007/s11259-016-9671-8

[19] Mofarahe ZS, Novin MG, Salehnia M. Folliculogenesis-Associated Genes Expression in Human Vitrified Ovarian Tissue after Xenotransplantation in γ-Irradiated Mice. Cell J. 2020;22(3):350–7.

[20] 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(1):1–6.

[21] Belli M, Shimasaki S. Molecular Aspects and Clinical Relevance of GDF9 and BMP15 in Ovarian Function [Internet]. 1st ed. Vol. 107, Vitamins and Hormones. Elsevier Inc.; 2018. 317–348 p. Available from: http://dx.doi.org/10.1016/bs.vh.2017.12.003

[22] Abdel-Ghani MA, El-Sherry TM, Abdelhafeez HH. Effect of growth differentiation factor-9 (GDF-9) on the progression of buffalo follicles in vitrified-warmed ovarian tissues. Reprod Domest Anim. 2016 Oct;51(5):795–803.

[23] De los Reyes M, Rojas C, Parraguez VH, Palomino J. Expression of growth differentiation factor 9 (GDF-9) during invitro maturation in canine oocytes. Theriogenology. 2013 Oct;80(6):587–96.

[24] Mofarahe ZS, Salehnia M, Novin MG, Ghorbanmehr N, Fesharaki MG. Expression of Folliculogenesis-Related Genes inVitrified Human Ovarian Tissue afterTwo Weeks In Vitro Culture. Cell J. 2017;19(1):18.

[25] Habibi A, Farrokhi N, Silva FM Da, Bettencourt BF, Bruges-Armas J, Amidi F, et al. The effects of vitrification on gene expression in mature mouse oocytes by nested quantitative PCR. J Assist Reprod Genet. 2010 Nov;27(11):599.

Effect of human granulosa cells vitrification on the expression of oocyte secreted factors

Abstract

References

How to Cite

Search Panel