Biological profile of the follicular fluid. A pilot study

Olesya N. Bespalova , Margarita O. Shengelia , Valeriya A. Zagaynova , Sergey V. Chepanov , Evgeniia M. Komarova , Igor Yu. Kogan

Journal of obstetrics and women's diseases ›› 2023, Vol. 72 ›› Issue (3) : 15 -26.

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Journal of obstetrics and women's diseases ›› 2023, Vol. 72 ›› Issue (3) : 15 -26. DOI: 10.17816/JOWD112564
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Biological profile of the follicular fluid. A pilot study

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Abstract

BACKGROUND: One of the most important research areas in the field of reproductive medicine is the search for biochemical and immunological parameters of oocyte quality and predicting the effectiveness of assisted reproductive technology protocols.

AIM: The aim of this study was to evaluate the expression of follicular fluid soluble human leukocyte antigen-G, human leukocyte antigen-E, human leukocyte antigen-C, progesterone-inducing blocking factor, and relaxin levels in women with reproductive disorders.

MATERIALS AND METHODS: This prospective cohort study included 22 patients undergoing infertility treatment in a superovulation stimulation protocol using gonadotropin-releasing hormone antagonists. The inclusion criteria were age from 25 to 39 years, tubal-peritoneal factor infertility, and voluntary participation informed consent. The levels of soluble human leukocyte antigen-G, human leukocyte antigen-E, human leukocyte antigen-C, progesterone-inducing blocking factor, and relaxin in follicular fluid samples were determined on the day of transvaginal follicle puncture by enzyme immunoassay.

RESULTS: We established an inverse correlation between the expression levels of progesterone-inducing blocking factor and relaxin (r = −0.450) in the follicular fluid, antibodies to thyroperoxidase (r = −0.649), and thyroid-stimulating hormone (r = −0.519). We also found a direct correlation between human leukocyte antigen-E parameters in the follicular fluid, age (r = 0.813) and Body Mass Index (r = 0.866), as well as between human leukocyte antigen-C expression levels and total testosterone (r = 0.960). No data were obtained on any significant correlations between the studied biomarkers and the number of received oocytes.

CONCLUSIONS: In this comprehensive study, we were the first who found the expression levels of five different follicular fluid components, namely, soluble human leukocyte antigen-G, human leukocyte antigen-E, human leukocyte antigen-C, progesterone-inducing blocking factor, and relaxin. Such a complex assessment of the follicular fluid can allow for establishing the quality of the oocyte to predict the onset of pregnancy in an in vitro fertilization protocol.

Keywords

human leukocyte antigen-C / soluble human leukocyte antigen-G / progesterone-inducing blocking factor / human leukocyte antigen-E / relaxin / in vitro fertilization / follicular fluid / oocyte / assisted reproductive technology effectiveness / infertility, reproductive disorders

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Olesya N. Bespalova, Margarita O. Shengelia, Valeriya A. Zagaynova, Sergey V. Chepanov, Evgeniia M. Komarova, Igor Yu. Kogan. Biological profile of the follicular fluid. A pilot study. Journal of obstetrics and women's diseases, 2023, 72(3): 15-26 DOI:10.17816/JOWD112564

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References

[1]

Ashworth CJ, Toma LM, Hunter MG. Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B Biol Sci. 2009;364(1534):3351–3361. DOI: 10.1098/rstb.2009.0184

[2]

Ashworth C.J., Toma L.M., Hunter M.G. Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability // Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2009. Vol. 364. No. 1534. P. 3351–3361. DOI: 10.1098/rstb.2009.0184

[3]

Fortune JE. Ovarian follicular growth and development in mammals. Biol Reprod. 1994;50(2):225–232. DOI: 10.1095/biolreprod50.2.225

[4]

Fortune J.E. Ovarian follicular growth and development in mammals // Biol. Reprod. 1994. Vol. 50. No. 2. P. 225–2232. DOI: 10.1095/biolreprod50.2.225

[5]

Leroy JL, Vanholder T, Delanghe JR, et al. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology. 2004;62(6):1131–1143. DOI: 10.1016/j.theriogenology.2003.12.017

[6]

Leroy J.L., Vanholder T., Delanghe J.R., et al. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum // Theriogenology. 2004. Vol. 62. No. 6. P. 1131–1143. DOI: 10.1016/j.theriogenology.2003.12.017

[7]

Sun Z, Wu H, Lian F, et al. Human follicular fluid metabolomics study of follicular development and oocyte quality. Chromatographia. 2017;80(6):901–909. DOI: 10.1007/s10337-017-3290-6

[8]

Sun Z., Wu H., Lian F., et al. Human follicular fluid metabolomics study of follicular development and oocyte quality // Chromatogra phia. 2017. Vol. 80. No. 6. P. 901–909. DOI: 10.1007/s10337-017-3290-6

[9]

Zakerkish F, Brännström M, Carlsohn E, et al. Proteomic analysis of follicular fluid during human ovulation. Acta Obstet Gynecol Scand. 2020;99(7):917–924. DOI: 10.1111/aogs.13805

[10]

Zakerkish F., Brännström M., Carlsohn E., et al. Proteomic analysis of follicular fluid during human ovulation // Acta Obstet. Gynecol. Scand. 2020. Vol. 99. No. 7. P. 917–924. DOI: 10.1111/aogs.13805

[11]

Poulsen LC, Pla I, Sanchez A, et al. Progressive changes in human follicular fluid composition over the course of ovulation: quantitative proteomic analyses. Mol Cell Endocrinol. 2019;495. DOI: 10.1016/j.mce.2019.110522

[12]

Poulsen L.C., Pla I., Sanchez A., et al. Progressive changes in human follicular fluid composition over the course of ovulation: quantitative proteomic analyses // Mol. Cell Endocrinol. 2019. Vol. 495. DOI: 10.1016/j.mce.2019.110522

[13]

Niu Z, Ye Y, Xia L, et al. Follicular fluid cytokine composition and oocyte quality of polycystic ovary syndrome patients with metabolic syndrome undergoing in vitro fertilization. Cytokine. 2017;91:180–186. DOI: 10.1016/j.cyto.2016.12.020

[14]

Niu Z., Ye Y., Xia L., et al. Follicular fluid cytokine composition and oocyte quality of polycystic ovary syndrome patients with metabolic syndrome undergoing in vitro fertilization // Cytokine. 2017. Vol. 91. P. 180–186. DOI: 10.1016/j.cyto.2016.12.020

[15]

Bogdanova MA, Vartanova IV, Gzgzyan AM. Ekstrakorporal’noe oplodotvorenie: prakticheskoe rukovodstvo dlya vrachei. Ed. by I.Yu. Kogan. Moscow: GEOTAR-Media; 2021. (In Russ.)

[16]

Богданова М.А., Вартанова И.В., Гзгзян А.М., и др. Экстракорпоральное оплодотворение: практическое руководство для врачей / под ред. И.Ю. Коган. Москва: ГЭОТАР-Медиа,2021.

[17]

Bakleycheva MO, Bespalova ON, Ivashchenko TE. The role of HLA class I (G, E and C) expression in early reproductive losses. Aku sherstvo i ginekologiya. 2020;(2):30–36. (In Russ.) DOI:10.18565/aig.2020.2.30-36

[18]

Баклейчева М.О., Беспалова О.Н., Иващенко Т.Э. Роль экспрессии HLA I класса (G, E и C) в ранних репродуктивных потерях // Акушерство и гинекология. 2020. № 2. C. 30–36. DOI: 10.18565/aig.2020.2.30-36

[19]

Hunt JS, Geraghty DE. Soluble HLA-G isoforms: technical deficiencies lead to misinterpretations. Mol Hum Reprod. 2005;11(10):715–717. DOI: 10.1093/molehr/gah223

[20]

Hunt J.S., Geraghty D.E. Soluble HLA-G isoforms: technical deficiencies lead to misinterpretations // Mol. Hum. Reprod. 2005. Vol. 11. No. 10. P. 715–717. DOI: 10.1093/molehr/gah223

[21]

Morandi F, Rouas-Freiss N, Pistoia V. The emerging role of soluble HLA-G in the control of chemotaxis. Cytokine Growth Factor Rev. 2014;25(3):327–335. DOI: 10.1016/j.cytogfr.2014.04.004

[22]

Morandi F., Rouas-Freiss N., Pistoia V. The emerging role of soluble HLA-G in the control of chemotaxis // Cytokine Growth Factor Rev. 2014. Vol. 25. No. 3. P. 327–335. DOI: 10.1016/j.cytogfr.2014.04.004

[23]

Ouji-Sageshima N, Yuui K, Nakanishi M, et al. sHLA-G and sHLA-I levels in follicular fluid are not associated with successful implantation. J Reprod Immunol. 2016;113:16–21. DOI: 10.1016/j.jri.2015.10.001

[24]

Ouji-Sageshima N., Yuui K., Nakanishi M, et al. sHLA-G and sHLA-I levels in follicular fluid are not associated with successful implantation // J. Reprod. Immunol. 2016. Vol. 113. P. 16–21. DOI: 10.1016/j.jri.2015.10.001

[25]

Rizzo R, Fuzzi B, Stignani M, et al. Soluble HLA-G molecules in follicular fluid: a tool for oocyte selection in IVF? J Reprod Immunol. 2007;74(1–2):133–142. DOI: 10.1016/j.jri.2007.02.005

[26]

Rizzo R., Fuzzi B., Stignani M., et al. Soluble HLA-G molecules in follicular fluid: a tool for oocyte selection in IVF? // J. Reprod. Immunol. 2007. Vol. 74. No. 1–2. P. 133–142. DOI: 10.1016/j.jri.2007.02.005

[27]

Shaikly VR, Morrison IE, Taranissi M, et al. Analysis of HLA-G in maternal plasma, follicular fluid, and preimplantation embryos reveal an asymmetric pattern of expression. J Immunol. 2008;180(6):4330–4337. DOI: 10.4049/jimmunol.180.6.4330

[28]

Shaikly V.R., Morrison I.E., Taranissi M., et al. Analysis of HLA-G in maternal plasma, follicular fluid, and preimplantation embryos reveal an asymmetric pattern of expression // J. Immunol. 2008. Vol. 180. No. 6. P. 4330–4337. DOI: 10.4049/jimmunol.180.6.4330

[29]

Jee BC, Suh CS, Kim SH, et al. Soluble human leukocyte antigen G level in fluid from single dominant follicle and the association with oocyte competence. Yonsei Med J. 2011;52(6):967–971. DOI: 10.3349/ymj.2011.52.6.967

[30]

Jee B.C., Suh C.S., Kim S.H., et al. Soluble human leukocyte antigen G level in fluid from single dominant follicle and the association with oocyte competence // Yonsei Med J. 2011. Vol. 52. No. 6. P. 967–971. DOI: 10.3349/ymj.2011.52.6.967

[31]

Vercammen M, Verloes A, Haentjens P, et al. Can soluble human leucocyte antigen-G predict successful pregnancy in assisted reproductive technology? Curr Opin Obstet Gynecol. 2009;21(3):285–290. DOI: 10.1097/gco.0b013e32832924cd

[32]

Vercammen M., Verloes A., Haentjens P., et al. Can soluble human leucocyte antigen-G predict successful pregnancy in assisted reproductive technology? // Curr. Opin. Obstet. Gynecol. 2009. Vol. 21. No. 3. P. 285–290. DOI: 10.1097/gco.0b013e32832924cd

[33]

Yao YQ, Barlow DH, Sargent IL. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J Immunol. 2005;175:8379–8385. DOI: 10.4049/jimmunol.175.12.8379

[34]

Yao Y.Q., Barlow D.H., Sargent I.L. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses // J. Immunol. 2005. Vol. 175. P. 8379–8385. DOI: 10.4049/jimmunol.175.12.8379

[35]

Guzeloglu-Kayisli O, Pauli S, Demir H, et al. Identification and characterization of human embryonic poly(A) binding protein (EPAB). Mol Hum Reprod. 2008;14:581–588. DOI: 10.1093/molehr/gan047

[36]

Guzeloglu-Kayisli O., Pauli S., Demir H., et al. Identification and characterization of human embryonic poly(A) binding protein (EPAB) // Mol. Hum. Reprod. 2008. Vol. 14. P. 581–588. DOI: 10.1093/molehr/gan047

[37]

Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988;332:459–461. DOI: 10.1038/332459a0

[38]

Braude P., Bolton V., Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development // Nature. 1988. Vol. 332. P. 459–461. DOI: 10.1038/332459a0

[39]

Noci I, Fuzzi B, Rizzo R, et al. Embryonic soluble HLA-G as a marker of developmental potential in embryos. Hum Reprod. 2005;20:138–146. DOI: 10.1093/humrep/deh572

[40]

Noci I., Fuzzi B., Rizzo R., et al. Embryonic soluble HLA-G as a marker of developmental potential in embryos // Hum. Reprod. 2005. Vol. 20. P. 138–146. DOI: 10.1093/humrep/deh572

[41]

Iwaszko M, Bogunia-Kubik K. Clinical significance of the HLA-E and CD94/NKG2 interaction. Arch Immunol Ther Exp. 2011;59(5):353–367. DOI: 10.1007/s00005-011-0137-y

[42]

Iwaszko M., Bogunia-Kubik K. Clinical significance of the HLA-E and CD94/NKG2 interaction // Arch. Immunol. Ther. Exp. (Warsz). 2011. Vol. 59. No. 5. P. 353–367. DOI: 10.1007/s00005-011-0137-y

[43]

Jiang L, Fei H, Jin X, et al. Extracellular vesicle-mediated secretion of HLA-E by trophoblasts maintains pregnancy by regulating the metabolism of decidual NK cells. Int J Biol Sci. 2021;17(15):4377–4395. DOI: 10.7150/ijbs.63390

[44]

Jiang L., Fei H., Jin X., et al. Extracellular vesicle-mediated secretion of HLA-E by trophoblasts maintains pregnancy by regulating the metabolism of decidual NK cells // Int. J. Biol. Sci. 2021. Vol. 17. No. 15. P. 4377–4395. DOI: 10.7150/ijbs.63390

[45]

Apps R, Meng Z, Del Prete GQ, et al. Relative expression levels of the HLA class-I proteins in normal and HIV-infected cells. J Immunol. 2015;194(8):3594–600. DOI: 10.4049/jimmunol.1403234

[46]

Apps R., Meng Z., Del Prete G.Q., et al. Relative expression levels of the HLA class-I proteins in normal and HIV-infected cells // J. Immunol. 2015. Vol. 194. No. 8. P. 3594–3600. DOI: 10.4049/jimmunol.1403234

[47]

Neisig A, Melief CJ, Neefjes J. Reduced cell surface expression of HLA-C molecules correlates with restricted peptide binding and stable TAP interaction. J Immunol. 1998;160(1):171–179.

[48]

Neisig A., Melief C.J., Neefjes J. Reduced cell surface expression of HLA-C molecules correlates with restricted peptide binding and stable TAP interaction // J. Immunol. 1998. Vol. 160. No. 1. P. 171–179.

[49]

Piekarska K, Radwan P, Tarnowska A, et al. ERAP, KIR, and HLA-C Profile in Recurrent Implantation Failure. Front Immunol. 2021;12. DOI: 10.3389/fimmu.2021.755624

[50]

Piekarska K., Radwan P., Tarnowska A., et al. ERAP, KIR, and HLA-C profile in recurrent implantation failure // Front Immunol. 2021. Vol. 12. DOI: 10.3389/fimmu.2021.755624

[51]

Sherwood OD. Relaxin’s physiological roles and other diverse actions. Endocr Rev. 2004;25(2):205–234. DOI: 10.1210/er.2003-0013

[52]

Sherwood O.D. Relaxin’s physiological roles and other diverse actions // Endocrine Rev. 2004. Vol. 25. No. 2. P. 205–234. DOI: 10.1210/er.2003-0013

[53]

Bagnell CA, Zhang Q, Downey B, et al. Sources and biological actions of relaxin in pigs. J Reprod Fertil. 1993;48:127–138.

[54]

Bagnell C.A., Zhang Q., Downey B., et al. Sources and biological actions of relaxin in pigs // J. Reprod. Fertil. 1993. Vol. 48. P. 127–138.

[55]

Ohleth KM, Zhang Q, Bagnell CA. Relaxin protein and gene expression in ovarian follicles of immature pigs. J Mol Endocrinol. 1998;21(2):179–187. DOI: 10.1677/jme.0.0210179

[56]

Ohleth K.M., Zhang Q., Bagnell C.A. Relaxin protein and gene expression in ovarian follicles of immature pigs // J. Mol. Endocrinol. 1998. Vol. 21. No. 2. P. 179–187. DOI: 10.1677/jme.0.0210179

[57]

Hwang JJ, Lin SW, Teng CH, et al. Relaxin modulates the ovulatory process and increases secretion of different gelatinases from granulosa and theca-interstitial cells in rats. Biol Reprod. 1996;55(6):1276–1283. DOI: 10.1095/biolreprod55.6.1276

[58]

Hwang J.J., Lin S.W., Teng C.H., et al. Relaxin modulates the ovulatory process and increases secretion of different gelatinases from granulosa and theca-interstitial cells in rats // Biol. Reprod. 1996. Vol. 55. No. 6. P. 1276–1283. DOI: 10.1095/biolreprod55.6.1276

[59]

Bespalova ON, Zagaynova VA, Kosyakova OV, et al. Blood serum and follicular fluid relaxin: a pilot study of the hormone effects on ovarian function and fertilization efficiency. Journal of Obstetrics and Women’s Diseases. 2020;69(5):59–68. (In Russ.) DOI: 10.17816/JOWD69559-68

[60]

Беспалова О.Н., Загайнова В.А., Косякова О.В., и др. Релаксин сыворотки крови и фолликулярной жидкости: пилотное исследование влияния гормона на функцию яичников и эффективность оплодотворения // Журнал акушерства и женских болезней. 2020. Т. 69. № 5. C. 59–68. DOI: 10.17816/JOWD69559-68

[61]

Feugang JM, Rodriguez-Munoz JC, Willard ST, et al. Examination of relaxin and its receptors expression in pig gametes and embryos. Reprod Biol Endocrinol. 2011;9:10. DOI: 10.1186/1477-7827-9-10

[62]

Feugang J.M., Rodriguez-Munoz J.C., Willard S.T., et al. Examination of relaxin and its receptors expression in pig gametes and embryos // Reprod. Biol. Endocrinol. 2011. Vol. 9. No. 10. P. 1–11. DOI: 10.1186/1477-7827-9-10

[63]

Adamczak R, Ukleja-Sokołowska N, Lis K, et al. Progesterone-induced blocking factor 1 and cytokine profile of follicular fluid of infertile women qualified to in vitro fertilization: The influence on fetus development and pregnancy outcome. Int J Immunopathol Pharmacol. 2022;36. DOI: 10.1177/03946320221111134

[64]

Adamczak R., Ukleja-Sokołowska N., Lis K., et al. Progesterone-induced blocking factor 1 and cytokine profile of follicular fluid of infertile women qualified to in vitro fertilization: the influence on fetus development and pregnancy outcome // Int. J. Immunopathol. Pharmacol. 2022. Vol. 36. P. 1–12. DOI: 10.1177/03946320221111134

[65]

Szekeres-Bartho J, Šućurović S, Mulac-Jeričević B. The role of extracellular vesicles and PIBF in embryo-maternal immune-interactions. Front Immunol. 2018;9. DOI: 10.3389/fimmu.2018.0289

[66]

Szekeres-Bartho J., Šućurović S., Mulac-Jeričević B. The role of extracellular vesicles and PIBF in embryo-maternal immune-interactions // Front. Immunol. 2018. Vol. 9. DOI: 10.3389/fimmu.2018.02890

[67]

Monteleone P, Parrini D, Faviana P, et al. Female infertility related to thyroid autoimmunity: the ovarian follicle hypothesis. Am J Reprod Immunol. 2011;66(2):108–114. DOI: 10.1111/j.1600-0897.2010.00961.x

[68]

Monteleone P., Parrini D., Faviana P., et al. Female infertility related to thyroid autoimmunity: the ovarian follicle hypo thesis // Am. J. Reprod. Immunol. 2011. Vol. 66. No. 2. P. 108–114. DOI: 10.1111/j.1600-0897.2010.00961.x

[69]

Chen CW, Huang YL, Tzeng CR, et al. Idiopathic low ovarian reserve is associated with more frequent positive thyroid peroxidase antibodies. Thyroid. 2017;27(9):1194–1200. DOI: 10.1089/thy.2017.0139

[70]

Chen C.W., Huang Y.L., Tzeng C.R., et al. Idiopathic low ovarian reserve is associated with more frequent positive thyroid peroxidase antibodies // Thyroid. 2017. Vol. 27. No. 9. P. 1194–1200. DOI: 10.1089/thy.2017.0139

[71]

Safaryan GK, Gzgzyan AM, Dzhemlikhanova LK, et al. The efficiency of IVF/ICSI protocols in female subclinical hypothyroidism and thyroid autoimmunity. Journal of Obstetrics and Women’s Diseases. 2019;68(4):83–94. (In Russ.) DOI: 10.17816/JOWD68483-94

[72]

Сафарян Г.Х., Гзгзян А.М., Джемлиханова Л.Х. Результативность протоколов ЭКО/ИКСИ у женщин с субклиническим гипотиреозом и носительством антител к щитовидной железе // Журнал акушерства и женских болезней. 2019. Т. 68. № 4. С. 83–94. DOI: 10.17816/JOWD68483-94

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