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Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Research

Is there a correlation between follicle size and gene expression in cumulus cells and is gene expression an indicator of embryo development?

Authors: Semra Kahraman, Caroline Pirkevi Çetinkaya, Murat Çetinkaya, Mehmet Ali Tüfekçi, Cumhur Gökhan Ekmekçi, Markus Montag

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

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Abstract

Background

In an article published in 2017, we discussed the results of the first part of our study into the morphokinetic development of embryos in relation to follicle diameter and homogeneity of follicular development. Our findings showed that embryos coming from small follicles in heterogeneous cycles had significantly higher rates of arrest or failure to reach blastocyst than embryos coming from large follicles in homogenous cycles. The aim of this further study was to investigate the relationship between follicular size and gene expression of cumulus cells (CCs) and evaluate whether gene expression could be an indicator of embryo development.

Methods

This study was based on 2495 COCs from 184 patients. CC expressions of five genes (TNFAIP6, PTGS2, HAS2, PTX3 and GDF9) were studied by generalized linear mixed models (GLMMs) regarding follicular size. CC expressions were then separately analysed regarding patient-specific variables (age, BMI, AMH and follicular size) in relation to embryos reaching blastocyst (eRB) or top or good quality blastocysts (TQ + GQ) using GLMMs with logit link.

Results

Follicular size significantly correlated with the potential of an oocyte to develop into a blastocyst: oocytes developing from large follicles were more than twice as likely to develop into an eRB than oocytes from small follicles (p < 0.001). Gene expression of HAS2 and GDF9 correlated with blastocyst quality when separately evaluated with follicular size and the patient specific variables of age, BMI and AMH. However, no such correlation was found in other gene expressions studied.

Conclusions

Our findings suggest that differences in the expression of genes studied could be related to follicular size rather than to embryo quality. Although gene expression of HAS2 and GDF9 correlated with blastocyst quality, the only variable correlating with eRB and TQ and GQ blastocysts for each of these five models was follicular size.

Trial registration

This prospective cohort study was registered at clinicaltrials.gov (NCT02230449).
Appendix
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Literature
1.
go back to reference Kahraman S, Cetinkaya CP, Cetinkaya M, Yelke H, Colakoglu YK, Aygun M, et al. The effect of follicle size and homogeneity of follicular development on the morphokinetics of human embryos. J Assist Reprod Genet. 2017;34(7):895–903.CrossRefPubMedPubMedCentral Kahraman S, Cetinkaya CP, Cetinkaya M, Yelke H, Colakoglu YK, Aygun M, et al. The effect of follicle size and homogeneity of follicular development on the morphokinetics of human embryos. J Assist Reprod Genet. 2017;34(7):895–903.CrossRefPubMedPubMedCentral
2.
go back to reference 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(12):2869–74.CrossRefPubMed 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(12):2869–74.CrossRefPubMed
3.
go back to reference Zhang X, Jafari N, Barnes RB, Confino E, Milad M, Kazer RR. Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril. 2005;83(Suppl 1):1169–79.CrossRefPubMed Zhang X, Jafari N, Barnes RB, Confino E, Milad M, Kazer RR. Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril. 2005;83(Suppl 1):1169–79.CrossRefPubMed
4.
go back to reference 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(5):645–50.CrossRefPubMed 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(5):645–50.CrossRefPubMed
5.
go back to reference Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, et al. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 1997;91:197–208.CrossRefPubMed Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, et al. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 1997;91:197–208.CrossRefPubMed
6.
go back to reference Calder MD, Caveney AN, Westhusin ME, Watson AJ. Cyclooxygenase-2 and prostaglandin E(2) (PGE(2)) receptor messenger RNAs are affected by bovine oocyte maturation time and cumulus-oocyte complex quality, and PGE(2) induces moderate expansion of the bovine cumulus in vitro. Biol Reprod. 2001;65:135–40.CrossRefPubMed Calder MD, Caveney AN, Westhusin ME, Watson AJ. Cyclooxygenase-2 and prostaglandin E(2) (PGE(2)) receptor messenger RNAs are affected by bovine oocyte maturation time and cumulus-oocyte complex quality, and PGE(2) induces moderate expansion of the bovine cumulus in vitro. Biol Reprod. 2001;65:135–40.CrossRefPubMed
7.
go back to reference Sirois J, Sayasith K, Brown KA, Stock AE, Bouchard N, Dore M. Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum Reprod Update. 2004;10:373–85.CrossRefPubMed Sirois J, Sayasith K, Brown KA, Stock AE, Bouchard N, Dore M. Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum Reprod Update. 2004;10:373–85.CrossRefPubMed
8.
go back to reference Takahashi T, Morrow JD, Wang H, Dey SK. Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem. 2006;281:37117–29.CrossRefPubMed Takahashi T, Morrow JD, Wang H, Dey SK. Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem. 2006;281:37117–29.CrossRefPubMed
9.
go back to reference Fulop C, Kamath RV, Li Y, Otto JM, Salustri A, Olsen BR, et al. Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes. Gene. 1997;202(1–2):95–102.CrossRefPubMed Fulop C, Kamath RV, Li Y, Otto JM, Salustri A, Olsen BR, et al. Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes. Gene. 1997;202(1–2):95–102.CrossRefPubMed
10.
go back to reference Yoshioka S, Ochsner S, Russell DL, Ujioka T, Fujii S, Richards JS, et al. Expression of tumor necrosis factor-stimulated gene-6 in the rat ovary in response to an ovulatory dose of gonadotropin. Endocrinology. 2000;141(11):4114–9.CrossRefPubMed Yoshioka S, Ochsner S, Russell DL, Ujioka T, Fujii S, Richards JS, et al. Expression of tumor necrosis factor-stimulated gene-6 in the rat ovary in response to an ovulatory dose of gonadotropin. Endocrinology. 2000;141(11):4114–9.CrossRefPubMed
11.
go back to reference Trombly DJ, Woodruff TK, Mayo KE. Roles for transforming growth factor beta superfamily proteins in early folliculogenesis. Semin Reprod Med. 2009;27:14–23.CrossRefPubMedPubMedCentral Trombly DJ, Woodruff TK, Mayo KE. Roles for transforming growth factor beta superfamily proteins in early folliculogenesis. Semin Reprod Med. 2009;27:14–23.CrossRefPubMedPubMedCentral
12.
go back to reference Kedem A, Fisch B, Garor R, Ben-Zaken A, Gizunterman T, Felz C, et al. Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9. J Clin Endocrinol Metab. 2011;96(8):E1246–54.CrossRefPubMed Kedem A, Fisch B, Garor R, Ben-Zaken A, Gizunterman T, Felz C, et al. Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9. J Clin Endocrinol Metab. 2011;96(8):E1246–54.CrossRefPubMed
13.
go back to reference Paulini F, Melo EO. The role of oocyte-secreted factors GDF9 and BMP15 in follicular development and oogenesis. Reprod Domest Anim. 2011;46:354–61.CrossRefPubMed Paulini F, Melo EO. The role of oocyte-secreted factors GDF9 and BMP15 in follicular development and oogenesis. Reprod Domest Anim. 2011;46:354–61.CrossRefPubMed
14.
go back to reference Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.CrossRefPubMed Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.CrossRefPubMed
15.
go back to reference Hutt KJ, Albertini DF. An oocentric view of folliculogenesis and embryogenesis. Reprod BioMed Online. 2007;14(6):758–64.CrossRefPubMed Hutt KJ, Albertini DF. An oocentric view of folliculogenesis and embryogenesis. Reprod BioMed Online. 2007;14(6):758–64.CrossRefPubMed
16.
go back to reference 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(12):711–9.CrossRefPubMed 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(12):711–9.CrossRefPubMed
17.
go back to reference Assou S, Boumela I, Haouzi D, Anahory T, Dechaud H, De Vos J, et al. Dynamic changes in gene expression during human early embryo development: from fundamental aspects to clinical applications. Hum Reprod Update. 2011;17(2):272–90.CrossRefPubMed Assou S, Boumela I, Haouzi D, Anahory T, Dechaud H, De Vos J, et al. Dynamic changes in gene expression during human early embryo development: from fundamental aspects to clinical applications. Hum Reprod Update. 2011;17(2):272–90.CrossRefPubMed
18.
go back to reference Assou S, Haouzi D, Dechaud H, Gala A, Ferrieres A, Hamamah S. Comparative gene expression profiling in human cumulus cells according to ovarian gonadotropin treatments. Biomed Res Int. 2013;2013:354582.CrossRefPubMedPubMedCentral Assou S, Haouzi D, Dechaud H, Gala A, Ferrieres A, Hamamah S. Comparative gene expression profiling in human cumulus cells according to ovarian gonadotropin treatments. Biomed Res Int. 2013;2013:354582.CrossRefPubMedPubMedCentral
19.
go back to reference Ekart J, McNatty K, Hutton J, Pitman J. Ranking and selection of MII oocytes in human ICSI cycles using gene expression levels from associated cumulus cells. Hum Reprod. 2013;28(11):2930–42.CrossRefPubMed Ekart J, McNatty K, Hutton J, Pitman J. Ranking and selection of MII oocytes in human ICSI cycles using gene expression levels from associated cumulus cells. Hum Reprod. 2013;28(11):2930–42.CrossRefPubMed
20.
go back to reference Li Y, Li RQ, Ou SB, Ren L, Zhang NF, Wei LN, et al. Association between the proportion of dominant follicles and oocyte developmental competence. J Assist Reprod Genet. 2014;31(12):1599–604.CrossRefPubMedPubMedCentral Li Y, Li RQ, Ou SB, Ren L, Zhang NF, Wei LN, et al. Association between the proportion of dominant follicles and oocyte developmental competence. J Assist Reprod Genet. 2014;31(12):1599–604.CrossRefPubMedPubMedCentral
21.
go back to reference Li SH, Lin MH, Hwu YM, Lu CH, Yeh LY, Chen YJ, et al. Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development. Reprod Biol Endocrinol. 2015;13:93.CrossRefPubMedPubMedCentral Li SH, Lin MH, Hwu YM, Lu CH, Yeh LY, Chen YJ, et al. Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development. Reprod Biol Endocrinol. 2015;13:93.CrossRefPubMedPubMedCentral
22.
go back to reference Assidi M, Montag M, Sirard MA. Use of both cumulus cells’ transcriptomic markers and zona pellucida birefringence to select developmentally competent oocytes in human assisted reproductive technologies. BMC Genomics. 2015;16(Suppl 1):S9.CrossRefPubMedPubMedCentral Assidi M, Montag M, Sirard MA. Use of both cumulus cells’ transcriptomic markers and zona pellucida birefringence to select developmentally competent oocytes in human assisted reproductive technologies. BMC Genomics. 2015;16(Suppl 1):S9.CrossRefPubMedPubMedCentral
23.
go back to reference Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril. 2015;103(2):303–16.CrossRefPubMed Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril. 2015;103(2):303–16.CrossRefPubMed
24.
go back to reference Nivet AL, Léveillé MC, Leader A, Sirard MA. Transcriptional characteristics of different sized follicles in relation to embryo transferability: potential role of hepatocyte growth factor signalling. Mol Hum Reprod. 2016;22(7):475–84.CrossRefPubMedPubMedCentral Nivet AL, Léveillé MC, Leader A, Sirard MA. Transcriptional characteristics of different sized follicles in relation to embryo transferability: potential role of hepatocyte growth factor signalling. Mol Hum Reprod. 2016;22(7):475–84.CrossRefPubMedPubMedCentral
25.
go back to reference Arnot AM, Vandekerckhove P, DeBono MA, Rutherford AJ. Follicular volume and number during in-vitro fertilization: association with oocyte developmental capacity and pregnancy rate. Hum Reprod. 1995;10(2):256–61.CrossRefPubMed Arnot AM, Vandekerckhove P, DeBono MA, Rutherford AJ. Follicular volume and number during in-vitro fertilization: association with oocyte developmental capacity and pregnancy rate. Hum Reprod. 1995;10(2):256–61.CrossRefPubMed
26.
go back to reference Salha O, Nugent D, Dada T, Kaufmann S, Levett S, Jenner L, et al. The relationship between follicular fluid aspirate volume and oocyte maturity in in-vitro fertilization cycles. Hum Reprod. 1998;13(7):1901–6.CrossRefPubMed Salha O, Nugent D, Dada T, Kaufmann S, Levett S, Jenner L, et al. The relationship between follicular fluid aspirate volume and oocyte maturity in in-vitro fertilization cycles. Hum Reprod. 1998;13(7):1901–6.CrossRefPubMed
27.
go back to reference Farhi J, Orvieto R, Gavish O, Homburg R. The association between follicular size on human chorionic gonadotropin day and pregnancy rate in clomiphene citrate treated polycystic ovary syndrome patients. Gynecol Endocrinol. 2010;26(7):546–8.CrossRefPubMed Farhi J, Orvieto R, Gavish O, Homburg R. The association between follicular size on human chorionic gonadotropin day and pregnancy rate in clomiphene citrate treated polycystic ovary syndrome patients. Gynecol Endocrinol. 2010;26(7):546–8.CrossRefPubMed
29.
go back to reference Chang HM, Qiao J, Leung PC. Oocyte-somatic cell interactions in the human ovary-novel role of bone morphogenetic proteins and growth differentiation factors. Hum Reprod Update. 2016;23(1):1–18.CrossRefPubMedPubMedCentral Chang HM, Qiao J, Leung PC. Oocyte-somatic cell interactions in the human ovary-novel role of bone morphogenetic proteins and growth differentiation factors. Hum Reprod Update. 2016;23(1):1–18.CrossRefPubMedPubMedCentral
30.
go back to reference Patino LC, Beau I, Carlosama C, Buitrago JC, Gonzalez R, Suarez CF, et al. New mutations in non-syndromic primary ovarian insufficiency patients identified via whole-exome sequencing. Hum Reprod. 2017;32(7):1512–20.CrossRefPubMed Patino LC, Beau I, Carlosama C, Buitrago JC, Gonzalez R, Suarez CF, et al. New mutations in non-syndromic primary ovarian insufficiency patients identified via whole-exome sequencing. Hum Reprod. 2017;32(7):1512–20.CrossRefPubMed
31.
go back to reference 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(1):47–52.e2.CrossRefPubMed 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(1):47–52.e2.CrossRefPubMed
32.
go back to reference Kordus RJ, LaVoie HA. Granulosa cell biomarkers to predict pregnancy in ART: pieces to solve the puzzle. Reproduction. 2017;153(2):R69–83.CrossRefPubMed Kordus RJ, LaVoie HA. Granulosa cell biomarkers to predict pregnancy in ART: pieces to solve the puzzle. Reproduction. 2017;153(2):R69–83.CrossRefPubMed
33.
go back to reference Duffy DM, Dozier BL, Seachord CL. Prostaglandin dehydrogenase and prostaglandin levels in periovulatory follicles: implications for control of primate ovulation by prostaglandin E2. J Clin Endocrinol Metab. 2005;90:1021–7.CrossRefPubMed Duffy DM, Dozier BL, Seachord CL. Prostaglandin dehydrogenase and prostaglandin levels in periovulatory follicles: implications for control of primate ovulation by prostaglandin E2. J Clin Endocrinol Metab. 2005;90:1021–7.CrossRefPubMed
34.
go back to reference Russell DL, Salustri A. Extracellular matrix of the cumulus-oocyte complex. Semin Reprod Med. 2006;24:217–27.CrossRefPubMed Russell DL, Salustri A. Extracellular matrix of the cumulus-oocyte complex. Semin Reprod Med. 2006;24:217–27.CrossRefPubMed
35.
go back to reference Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, et al. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development. 2004;131:1577–86.CrossRefPubMed Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, et al. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development. 2004;131:1577–86.CrossRefPubMed
36.
go back to reference Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, et al. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol. 2002;16:1154–67.CrossRefPubMed Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, et al. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol. 2002;16:1154–67.CrossRefPubMed
37.
go back to reference Feuerstein P, Puard V, Chevalier C, Teusan R, Cadoret V, Guerif F, et al. Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors. PLoS One. 2012;7(7):e40449.CrossRefPubMedPubMedCentral Feuerstein P, Puard V, Chevalier C, Teusan R, Cadoret V, Guerif F, et al. Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors. PLoS One. 2012;7(7):e40449.CrossRefPubMedPubMedCentral
38.
go back to reference Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development. 2003;130:2253–61.CrossRefPubMed Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development. 2003;130:2253–61.CrossRefPubMed
39.
go back to reference Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008;23(5):1118–27.CrossRefPubMed Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008;23(5):1118–27.CrossRefPubMed
40.
go back to reference Silva JR, van den Hurk R, van Tol HT, Roelen BA, Figueiredo JR. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol Reprod Dev. 2005;70:11–9.CrossRefPubMed Silva JR, van den Hurk R, van Tol HT, Roelen BA, Figueiredo JR. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol Reprod Dev. 2005;70:11–9.CrossRefPubMed
41.
go back to reference Zhao SY, Qiao J, Chen YJ, Liu P, Li J, Yan J. Expression of growth differentiation factor-9 and bone morphogenetic protein-15 in oocytes and cumulus granulosa cells of patients with polycystic ovary syndrome. Fertil Steril. 2010;94:261–7.CrossRefPubMed Zhao SY, Qiao J, Chen YJ, Liu P, Li J, Yan J. Expression of growth differentiation factor-9 and bone morphogenetic protein-15 in oocytes and cumulus granulosa cells of patients with polycystic ovary syndrome. Fertil Steril. 2010;94:261–7.CrossRefPubMed
42.
go back to reference Hosoe M, Kaneyama K, Ushizawa K, Hayashi KG, Takahashi T. Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod Biol Endocrinol. 2011;9:33.CrossRefPubMedPubMedCentral Hosoe M, Kaneyama K, Ushizawa K, Hayashi KG, Takahashi T. Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod Biol Endocrinol. 2011;9:33.CrossRefPubMedPubMedCentral
43.
go back to reference Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, et al. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, et al. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral
44.
go back to reference Kenigsberg S, Bentov Y, Chalifa-Caspi V, Potashnik G, Ofir R, Birk OS. Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients. Mol Hum Reprod. 2009;15(2):89–103.CrossRefPubMed Kenigsberg S, Bentov Y, Chalifa-Caspi V, Potashnik G, Ofir R, Birk OS. Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients. Mol Hum Reprod. 2009;15(2):89–103.CrossRefPubMed
45.
go back to reference Cetinkaya M, Pirkevi C, Yelke H, Colakoglu YK, Atayurt Z, Kahraman S. Relative kinetic expressions defining cleavage synchronicity are better predictors of blastocyst formation and quality than absolute time points. J Assist Reprod Genet. 2015;32(1):27–35.CrossRefPubMed Cetinkaya M, Pirkevi C, Yelke H, Colakoglu YK, Atayurt Z, Kahraman S. Relative kinetic expressions defining cleavage synchronicity are better predictors of blastocyst formation and quality than absolute time points. J Assist Reprod Genet. 2015;32(1):27–35.CrossRefPubMed
46.
go back to reference Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–8.CrossRefPubMed Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–8.CrossRefPubMed
47.
go back to reference Rienzi L, Vajta G, Ubaldi F. Predictive value of oocyte morphology in human IVF: a systematic review of the literature. Hum Reprod Update. 2011;17(1):34–45.CrossRefPubMed Rienzi L, Vajta G, Ubaldi F. Predictive value of oocyte morphology in human IVF: a systematic review of the literature. Hum Reprod Update. 2011;17(1):34–45.CrossRefPubMed
48.
go back to reference Trounson A, Gosden R, Eichenlaub-Ritter U. Biology and pathology of the oocyte: role in fertility, medicine, and nuclear reprogramming. 2nd ed: Cambridge University Press; 2013. Trounson A, Gosden R, Eichenlaub-Ritter U. Biology and pathology of the oocyte: role in fertility, medicine, and nuclear reprogramming. 2nd ed: Cambridge University Press; 2013.
49.
go back to reference Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod. 1990;43:543–7.CrossRefPubMed Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod. 1990;43:543–7.CrossRefPubMed
50.
go back to reference Cruz M, Requena A, Agudo D, García-Velasco JA. Type of gonadotropin used during controlled ovarian stimulation induces differential gene expression in human cumulus cells: a randomized study. Eur J Obstet Gynecol Reprod Biol. 2017;215:124–33.CrossRefPubMed Cruz M, Requena A, Agudo D, García-Velasco JA. Type of gonadotropin used during controlled ovarian stimulation induces differential gene expression in human cumulus cells: a randomized study. Eur J Obstet Gynecol Reprod Biol. 2017;215:124–33.CrossRefPubMed
51.
go back to reference da Luz CM, da Broi MG, Donabela FC, Paro de Paz CC, Meola J, Navarro PA. PTGS2 down-regulation in cumulus cells of infertile women with endometriosis. Reprod BioMed Online. 2017;35(4):379–86.CrossRefPubMed da Luz CM, da Broi MG, Donabela FC, Paro de Paz CC, Meola J, Navarro PA. PTGS2 down-regulation in cumulus cells of infertile women with endometriosis. Reprod BioMed Online. 2017;35(4):379–86.CrossRefPubMed
52.
go back to reference McReynolds S, Dzieciatkowska M, McCallie BR, Mitchell SD, Stevens J, Hansen K, et al. Impact of maternal aging on the molecular signature of human cumulus cells. Fertil Steril. 2012;98(6):1574–80.e5.CrossRefPubMed McReynolds S, Dzieciatkowska M, McCallie BR, Mitchell SD, Stevens J, Hansen K, et al. Impact of maternal aging on the molecular signature of human cumulus cells. Fertil Steril. 2012;98(6):1574–80.e5.CrossRefPubMed
53.
go back to reference Al-Edani T, Assou S, Ferrieres A, Bringer Deutsch S, Gala A, Lecellier CH, et al. Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. Biomed Res Int. 2014;2014:964614.CrossRefPubMedPubMedCentral Al-Edani T, Assou S, Ferrieres A, Bringer Deutsch S, Gala A, Lecellier CH, et al. Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. Biomed Res Int. 2014;2014:964614.CrossRefPubMedPubMedCentral
54.
go back to reference Kedem A, Yung Y, Yerushalmi GM, Haas J, Maman E, Hanochi M, et al. Anti Müllerian hormone (AMH) level and expression in mural and cumulus cells in relation to age. J Ovarian Res. 2014;7:113.CrossRefPubMedPubMedCentral Kedem A, Yung Y, Yerushalmi GM, Haas J, Maman E, Hanochi M, et al. Anti Müllerian hormone (AMH) level and expression in mural and cumulus cells in relation to age. J Ovarian Res. 2014;7:113.CrossRefPubMedPubMedCentral
55.
go back to reference Robker RL, Akison LK, Bennett BD, Thrupp PN, Chura LR, Russell DL, et al. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab. 2009;94(5):1533–40.CrossRefPubMed Robker RL, Akison LK, Bennett BD, Thrupp PN, Chura LR, Russell DL, et al. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab. 2009;94(5):1533–40.CrossRefPubMed
56.
go back to reference Kava-Braverman A, Martínez F, Rodríguez I, Álvarez M, Barri PN, Coroleu B. What is a difficult transfer? Analysis of 7,714 embryo transfers: the impact of maneuvers during embryo transfers on pregnancy rate and a proposal of objective assessment. Fertil Steril. 2017;107(3):657–663.e1.CrossRefPubMed Kava-Braverman A, Martínez F, Rodríguez I, Álvarez M, Barri PN, Coroleu B. What is a difficult transfer? Analysis of 7,714 embryo transfers: the impact of maneuvers during embryo transfers on pregnancy rate and a proposal of objective assessment. Fertil Steril. 2017;107(3):657–663.e1.CrossRefPubMed
57.
go back to reference Jansen E, Laven JS, Dommerholt HB, Polman J, van Rijt C, van den Hurk C, et al. Abnormal gene expression profiles in human ovaries from polycystic ovary syndrome patients. Mol Endocrinol. 2004;18(12):3050–63.CrossRefPubMed Jansen E, Laven JS, Dommerholt HB, Polman J, van Rijt C, van den Hurk C, et al. Abnormal gene expression profiles in human ovaries from polycystic ovary syndrome patients. Mol Endocrinol. 2004;18(12):3050–63.CrossRefPubMed
Metadata
Title
Is there a correlation between follicle size and gene expression in cumulus cells and is gene expression an indicator of embryo development?
Authors
Semra Kahraman
Caroline Pirkevi Çetinkaya
Murat Çetinkaya
Mehmet Ali Tüfekçi
Cumhur Gökhan Ekmekçi
Markus Montag
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0388-0

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