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Review

Proteomics in the study of female fertility: an update

, , & ORCID Icon
Pages 319-330 | Received 09 Mar 2023, Accepted 20 Oct 2023, Published online: 02 Nov 2023

References

  • Aslam B, Basit M, Nisar MA, et al. Proteomics: technologies and their applications. J Chromatogr Sci. 2017;55(2):182–196. doi: 10.1093/chromsci/bmw167
  • Da Broi MG, Giorgi VSI, Wang F, et al. Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. J Assist Reprod Genet. 2018;35(5):735–751. doi: 10.1007/s10815-018-1143-3
  • Benkhalifa M, Madkour A, Louanjli N, et al. From global proteome profiling to single targeted molecules of follicular fluid and oocyte: contribution to embryo development and IVF outcome. Expert Rev Proteomics. 2015;12(4):407–423. doi: 10.1586/14789450.2015.1056782
  • Pla I, Sanchez A, Pors SE, et al. Proteome of fluid from human ovarian small antral follicles reveals insights in folliculogenesis and oocyte maturation. Hum Reprod. 2021;36(3):756–770. doi: 10.1093/humrep/deaa335
  • Wang C, Fei X, Zhang H, et al. Proteomic analysis of the alterations in follicular fluid proteins during oocyte maturation in humans. Front Endocrinol. 2022;12(February):1–10. doi: 10.3389/fendo.2021.830691
  • la C PL, 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;495:110522. doi: 10.1016/j.mce.2019.110522.
  • Zamah AM, Hassis ME, Albertolle ME, et al. Proteomic analysis of human follicular fluid from fertile women. Clin Proteomics. 2015;12(1). doi: 10.1186/s12014-015-9077-6
  • 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
  • Kim S-M, Kim J-S. A review of mechanisms of implantation. Dev Reprod. 2017;21(4):351–359. doi: 10.12717/DR.2017.21.4.351
  • Messinis IE, Messini CI, Dafopoulos K. Novel aspects of the endocrinology of the menstrual cycle. Reprod Biomed Online. 2014;28(6):714–722. doi: 10.1016/j.rbmo.2014.02.003
  • Plant TM. 60 YEARS of NEUROENDOCRINOLOGY: the hypothalamo-pituitary–gonadal axis. J Endocrinol. 2016;226(2):T41–T54. doi: 10.1530/JOE-15-0113
  • Paule SG, Heng S, Samarajeewa N, et al. Podocalyxin is a key negative regulator of human endometrial epithelial receptivity for embryo implantation. Hum Reprod. 2021;36(5):1353–1366. doi: 10.1093/humrep/deab032
  • Segura-Benítez M, Carbajo-García MC, Corachán A, et al. Proteomic analysis of extracellular vesicles secreted by primary human epithelial endometrial cells reveals key proteins related to embryo implantation. Reprod Biol Endocrinol. 2022;20(1):1–16. doi: 10.1186/s12958-021-00879-x
  • Bissonnette L, Drissennek L, Antoine Y, et al. Human S100A10 plays a crucial role in the acquisition of the endometrial receptivity phenotype. Cell Adhes Migr. 2016;10(3):282–298. doi: 10.1080/19336918.2015.1128623
  • Evans J, Hutchison J, Salamonsen LA, et al. Proteomic insights into endometrial receptivity and embryo-endometrial epithelium interaction for implantation reveal critical determinants of fertility. Proteomics. 2020;20(1):1–13. doi: 10.1002/pmic.201900250
  • Pérez-Debén S, Bellver J, Alamá P, et al. iTRAQ comparison of proteomic profiles of endometrial receptivity. J Proteomics. 2019;203(April):103381. doi: 10.1016/j.jprot.2019.103381
  • Chen Q, Zhang A, Yu F, et al. Label-free proteomics uncovers energy metabolism and focal adhesion regulations responsive for endometrium receptivity. J Proteome Res. 2015;14(4):1831–1842. doi: 10.1021/acs.jproteome.5b00038
  • Bhutada S, Basak T, Savardekar L, et al. High mobility group box 1 (HMGB1) protein in human uterine fluid and its relevance in implantation. Hum Reprod. 2014;29(4):763–780. doi: 10.1093/humrep/det461
  • Kasvandik S, Saarma M, Kaart T, et al. Uterine fluid proteins for minimally invasive assessment of endometrial receptivity. J Clin Endocrinol Metab. 2020;105(1):219–230. doi: 10.1210/clinem/dgz019
  • Azkargorta M, Bregón-Villahoz M, Escobes I, et al. In-depth proteomics and natural peptidomics analyses reveal antibacterial peptides in human endometrial fluid. J Proteomics. 2020;216(January):103652. doi: 10.1016/j.jprot.2020.103652
  • Rai A, Poh QH, Fatmous M, et al. Dynamic regulation of key players of embryo implantation and fertility in human uterine extracellular vesicles during menstrual cycle Alin. J Neurophysiol. 2010;21(1):1–18.
  • Kanaka V, Proikakis S, Drakakis P, et al. Implementing a preimplantation proteomic approach to advance assisted reproduction technologies in the framework of predictive, preventive, and personalized medicine. EPMA J. 2022;13(2):237–260. doi: 10.1007/s13167-022-00282-5
  • Vander Borght M, Wyns C. Fertility and infertility: definition and epidemiology. Clin Biochem. 2018;62:2–10. doi: 10.1016/j.clinbiochem.2018.03.012
  • Hoeger KM, Dokras A, Piltonen T. Update on PCOS: consequences, challenges, and guiding treatment. J Clin Endocrinol Metab. 2021;106(3):E1071–83. doi: 10.1210/clinem/dgaa839
  • Butler AE, Moin AS, Sathyapalan T, et al. Components of the complement cascade differ in polycystic ovary syndrome. Int J Mol Sci. 2022;23(20):12232. doi: 10.3390/ijms232012232
  • Patil K, Yelamanchi S, Kumar M, et al. Quantitative mass spectrometric analysis to unravel glycoproteomic signature of follicular fluid in women with polycystic ovary syndrome. PLoS One. 2019;14(4):1–17. doi: 10.1371/journal.pone.0214742
  • Domingues TS, Bonetti TCS, Pimenta DC, et al. Original article proteomic profile of follicular fluid from patients with polycystic ovary syndrome (PCOS) submitted to in vitro fertilization (IVF) compared to oocyte donors. JBRA Assist Reprod. 2019;23(4):367–391. doi: 10.5935/1518-0557.20190041
  • Zhang J, Ding N, Xin W, et al. Quantitative proteomics reveals that a prognostic signature of the endometrium of the polycystic ovary syndrome women based on ferroptosis proteins. Front Endocrinol. 2022;13(July):1–13. doi: 10.3389/fendo.2022.871945
  • Zhang X, Xu X, Li P, et al. TMT based proteomic analysis of human follicular fluid from overweight/obese and normal-weight patients with polycystic ovary syndrome. Front Endocrinol. 2019;10(November):1–16. doi: 10.3389/fendo.2019.00821
  • Amjadi F, Mehdizadeh M, Ashrafi M, et al. Distinct changes in the proteome profile of endometrial tissues in polycystic ovary syndrome compared with healthy fertile women. Reprod Biomed Online. 2018;37(2):184–200. doi: 10.1016/j.rbmo.2018.04.043
  • Carvalho LML, Ferreira CN, De OD, et al. Haptoglobin levels, but not Hp1-Hp2 polymorphism, are associated with polycystic ovary syndrome. J Assist Reprod Genet. 2017;34(12):1691–1698. doi: 10.1007/s10815-017-1030-3
  • Rashid N, Nigam A, Jain SK, et al. Proteomic sift through serum and endometrium profiles unraveled signature proteins associated with subdued fertility and dampened endometrial receptivity in women with polycystic ovary syndrome. Cell Tissue Res. 2020;380(3):593–614. doi: 10.1007/s00441-020-03171-3
  • Li J, Jiang X, Li C, et al. Proteomic alteration of endometrial tissues during secretion in polycystic ovary syndrome may affect endometrial receptivity. Clin Proteomics. 2022;19(1):1–16. doi: 10.1186/s12014-022-09353-1
  • Alikhani M, Amjadi F, Mirzaei M, et al. Proteome analysis of endometrial tissue from patients with PCOS reveals proteins predicted to impact the disease. Mol Biol Rep. 2020;47(11):8763–8774. doi: 10.1007/s11033-020-05924-3
  • Rolla E. Endometriosis: advences and controversies in classification, pathogenesis, diagnosis, and treatment. F1000Res. 2019;8:1–28. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480968/
  • Manousopoulou A, Hamdan M, Fotopoulos M, et al. Integrated Eutopic Endometrium and Non-Depleted Serum Quantitative Proteomic Analysis Identifies Candidate Serological Markers of Endometriosis. Proteomics Clin Appl. 2019;13(3):e1800153. doi: 10.1002/prca.201800153
  • Ph D, Kasvandik S, Sc M. Perceived stress and fatigue among students in a doctor of chiropractic training program. J Chiropr Educ. 2016;31(1):8–13. doi: 10.7899/JCE-15-27
  • Chen X, Liu H, Sun W, et al. Elevated urine histone 4 levels in women with ovarian endometriosis revealed by discovery and parallel reaction monitoring proteomics. J Proteomics. 2019;204(1):103398. doi: 10.1016/j.jprot.2019.103398
  • Janša V, Klančič T, Pušić M, et al. Proteomic analysis of peritoneal fluid identified COMP and TGFBI as new candidate biomarkers for endometriosis. Sci Rep. 2021;11(1):1–14. doi: https://doi.org/10.1038/s41598-021-00299-2
  • Grande G, Vincenzoni F, Milardi D, et al. Cervical mucus proteome in endometriosis. Clin Proteomics. 2017;14(1):1–11. doi: 10.1186/s12014-017-9142-4
  • Ek M, Roth B, Engström G, et al. AXIN1 in plasma or serum is a potential new biomarker for endometriosis. Int J Mol Sci. 2019;20(1):189. doi: 10.3390/ijms20010189
  • Signorile PG, Baldi A. Serum biomarker for diagnosis of endometriosis. J Cell Physiol. 2014;229(11):1731–1735. doi: 10.1002/jcp.24620
  • Signorile PG, Baldi A. Supporting evidences for potential biomarkers of endometriosis detected in peripheral blood. Data BR. 2015;5:971–974. doi: 10.1016/j.dib.2015.10.047
  • Méar L, Com E, Fathallah K, et al. The eutopic endometrium proteome in endometriosis reveals candidate markers and molecular mechanisms of physiopathology. Diagnostics. 2022;12(2):419. doi: 10.3390/diagnostics12020419
  • A LLW, A RJN, A RLR. The impact of obesity on oocytes: evidence for lipotoxicity mechanisms. Reprod Fertil Dev. 2012;24(1):29–34. doi: 10.1071/RD11904
  • Metwally M, Preece R, Thomas J, et al. A proteomic analysis of the endometrium in obese and overweight women with recurrent miscarriage: preliminary evidence for an endometrial defect. Reprod Biol Endocrinol. 2014;12(1):1–10. doi: 10.1186/1477-7827-12-75
  • Liu X, Wang Y, Zhu P, et al. Human follicular fluid proteome reveals association between overweight status and oocyte maturation abnormality. Clin Proteomics. 2020;17(1):1–12. doi: 10.1186/s12014-020-09286-7
  • Fitzgerald HC, Evans J, Johnson N, et al. Idiopathic infertility in women is associated with distinct changes in proliferative phase uterine fluid proteins †. Biol Reprod. 2018;98(6):752–764. doi: 10.1093/biolre/ioy063
  • Manohar M. Proteomic identification and analysis of human endometrial proteins associated with unexplained infertility. J Proteomics Bioinform. 2014;7(11):359–366. doi: 10.4172/jpb.1000340
  • Manohar M, Khan H, Sirohi VK, et al. Alteration in endometrial proteins during early- and mid-secretory phases of the cycle in women with unexplained infertility. PLoS One. 2014;9(11):e111687. doi: 10.1371/journal.pone.0111687
  • Qu T, Yan M, Shen W, et al. Predictive serum markers for unexplained infertility in child-bearing aged women. Am J Reprod Immunol. 2020;83(1):0–2.
  • Baig M, Azhar A, Rehman R, et al. Relationship of serum leptin and reproductive hormones in unexplained infertile and fertile females. Cureus. 2019;11(12). doi: 10.7759/cureus.6524
  • Shen X, Liu X, Zhu P, et al. Proteomic analysis of human follicular fluid associated with successful in vitro fertilization. Reprod Biol Endocrinol. 2017;15(1). doi: 10.1186/s12958-017-0277-y
  • Nishihara T, Matsumoto K, Hosoi Y, et al. Evaluation of antioxidant status and oxidative stress markers in follicular fluid for human in vitro fertilization outcome. Reprod Med Biol. 2018;17(4):481–486. doi: 10.1002/rmb2.12229
  • Lewandowska AE, Macur K, Czaplewska P, et al. Qualitative and quantitative analysis of proteome and peptidome of human follicular fluid using multiple samples from single donor with LC–MS and SWATH methodology. J Proteome Res. 2017;16(8):3053–3067. doi: 10.1021/acs.jproteome.7b00366
  • Sun X, Jin J, Zhang YL, et al. Decreased histidine-rich glycoprotein and increased complement C4-B protein levels in follicular fluid predict the IVF outcomes of recurrent spontaneous abortion. Clin Proteomics. 2022;19(1):1–13. doi: 10.1186/s12014-022-09383-9
  • Chen F, Spiessens C, D’Hooghe T, et al. Follicular fluid biomarkers for human in vitro fertilization outcome: proof of principle. Proteome Sci. 2016;14(1). doi: 10.1186/s12953-016-0106-9
  • Artini PG, Scarf G, Marzi I, et al. Oxidative stress-related signaling pathways predict oocytes’ fertilization in vitro and embryo quality. IJMS. 2022;23(21):13442. doi: 10.3390/ijms232113442
  • Nuñez-Calonge R, Cortés S, Gutierrez Gonzalez LM, et al. Oxidative stress in follicular fluid of young women with low response compared with fertile oocyte donors. Reprod Biomed Online. 2016;32(4):446–456. doi: 10.1016/j.rbmo.2015.12.010
  • Nagy RA, van Montfoort APA, Groen H, et al. Anti-oxidative function of follicular fluid HDL and outcomes of modified natural cycle-IVF. Sci Rep. 2019;9(1). doi: 10.1038/s41598-019-49091-3
  • Machlin JH, Barishansky SJ, Kelsh J, et al. Fibroinflammatory signatures increase with age in the human ovary and follicular fluid. Int J Mol Sci. 2021;22(9):4902. doi: 10.3390/ijms22094902
  • Luddi A, Gori M, Marrocco C, et al. Matrix metalloproteinases and their inhibitors in human cumulus and granulosa cells as biomarkers for oocyte quality estimation. Fertil Steril. 2018;109(5):930–939.e3. doi: 10.1016/j.fertnstert.2018.01.030
  • Li S, Hu L, Zhang C. Urinary vitamin D-binding protein as a marker of ovarian reserve. Reprod Biol Endocrinol. 2021;9(1):1–9. doi: 10.1186/s12958-021-00762-9
  • Ciepiela P, Dulęba AJ, Kowaleczko E, et al. Vitamin D as a follicular marker of human oocyte quality and a serum marker of in vitro fertilization outcome. J Assist Reprod Genet. 2018;35(7):1265–1276. doi: 10.1007/s10815-018-1179-4
  • Nikas G. Cell-surface morphological events relevant to human implantation. Hum Reprod. 1999;14(SUPPL. 2):37–44. doi: 10.1093/humrep/14.suppl_2.37
  • Díaz-Gimeno P, Horcajadas JA, Martínez-Conejero JA, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011;95(1):50–60.e15. doi: 10.1016/j.fertnstert.2010.04.063
  • Garrido-Gómez T, Quiñonero A, Antúnez O, et al. Deciphering the proteomic signature of human endometrial receptivity. Hum Reprod. 2014;29(9):1957–1967. doi: 10.1093/humrep/deu171
  • Matorras R, Quevedo S, Corral B, et al. Proteomic pattern of implantative human endometrial fluid in in vitro fertilization cycles. Arch Gynecol Obstet. 2018;297(6):1577–1586. doi: 10.1007/s00404-018-4753-1
  • Azkargorta M, Escobes I, Iloro I, et al. Differential proteomic analysis of endometrial fluid suggests increased inflammation and impaired glucose metabolism in non-implantative IVF cycles and pinpoints PYGB as a putative implantation marker. Hum Reprod. 2018;33(10):1898–1906. doi: 10.1093/humrep/dey274
  • Hannan NJ, Stephens AN, Rainczuk A, et al. 2D-DiGE analysis of the human endometrial secretome reveals differences between receptive and nonreceptive states in fertile and infertile women. J Proteome Res. 2010;9(12):6256–6264. doi: 10.1021/pr1004828

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