Circular RNA expression profiles of ovarian granulosa cells in advanced-age women explain new mechanisms of ovarian aging

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Qiao J, Wang ZB, Feng HL et al. The root of reduced fertility in aged women and possible therapentic options: current status and future prospects. Mol. Aspects Med. 38, 54–85 (2014).
  MedlineGoogle Scholar
• 2. CDC. 2011 Assisted Reproductive Technology Fertility Clinic Success Rates Report. US Department of Health and Human Services, GA, USA, 24 (2013).
  Google Scholar
• 3. Marshall KL, Rivera RM. The effects of superovulation and reproductive aging on the epigenome of the oocyte and embryo. Mol. Reprod. Dev. 85(2), 90–105 (2018).
  Medline CASGoogle Scholar
• 4. Wei JW, Huang K, Yang C, Kang CS. Non-coding RNAs as regulators in epigenetics (review). Oncol. Rep. 37(1), 3–9 (2017).
  MedlineGoogle Scholar
• 5. Chen LL. The biogenesis and emerging roles of circular RNAs. Nat. Rev. Mol. Cell. Biol. 17(4), 205–211 (2016).
  Medline CASGoogle Scholar
• 6. Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nat. Biotechnol. 32(5), 453–461 (2014).
  Medline CASGoogle Scholar
• 7. Li X, Yang L, Chen LL. The biogenesis, functions, and challenges of circular RNAs. Mol. Cell. 71(3), 428–442 (2018). • Their study investigated the role of epigenetics in controlling gene expression and chromatin structure, suggesting that epigenetic abnormalities may be an important cause of fertility decline in older women.
  Medline CASGoogle Scholar
• 8. Wang Z, Sun A, Yan A et al. Circular RNA MTCL1 promotes advanced laryngeal squamous cell carcinoma progression by inhibiting C1QBP ubiquitin degradation and mediating beta-catenin activation. Mol. Cancer 21(1), 92 (2022).
  Medline CASGoogle Scholar
• 9. Du WW, Yang W, Chen Y et al. Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur. Heart J. 38(18), 1402–1412 (2017).
  Medline CASGoogle Scholar
• 10. Floris G, Zhang L, Follesa P, Sun T. Regulatory role of circular RNAs and neurological disorders. Mol. Neurobiol. 54(7), 5156–5165 (2017).
  Medline CASGoogle Scholar
• 11. Che Q, Liu M, Xu J et al. Characterization of circular RNA expression profiles in cumulus cells from patients with polycystic ovary syndrome. Fertil. Steril. 111(6), 1243–1251 (2019).
  Medline CASGoogle Scholar
• 12. Ma Z, Zhao H, Zhang Y, Liu X, Hao C. Novel circular RNA expression in the cumulus cells of patients with polycystic ovary syndrome. Arch. Gynecol. Obstet. 299(6), 1715–1725 (2019).
  Medline CASGoogle Scholar
• 13. Shen L, Zhang Y, Zhou W, Peng Z, Hong X, Zhang Y. Circular RNA expression in ovarian endometriosis. Epigenomics 10(5), 559–572 (2018).
  CASGoogle Scholar
• 14. Xu X, Jia SZ, Dai Y et al. The relationship of circular RNAs with ovarian endometriosis. Reprod. Sci. 25(8), 1292–1300 (2018).
  Medline CASGoogle Scholar
• 15. Gruner H, Cortes-Lopez M, Cooper DA, Bauer M, Miura P. CircRNA accumulation in the aging mouse brain. Sci. Rep. 6, 38907 (2016). • This preliminary report suggests that circular RNAs are closely related to aging.
  Medline CASGoogle Scholar
• 16. Panda AC, Grammatikakis I, Kim KM et al. Identification of senescence-associated circular RNAs (SAC-RNAs) reveals senescence suppressor CircPVT1. Nucleic Acids Res. 45(7), 4021–4035 (2017).
  Medline CASGoogle Scholar
• 17. Lukiw WJ. Circular RNA (circRNA) in Alzheimer's disease (AD). Front. Genet. 4, 307 (2013).
  MedlineGoogle Scholar
• 18. Huang G, Zhu H, Shi Y, Wu W, Cai H, Chen X. cir-ITCH plays an inhibitory role in colorectal cancer by regulating the Wnt/beta-catenin pathway. PLOS ONE 10(6), e0131225 (2015).
  MedlineGoogle Scholar
• 19. Cheng J, Huang J, Yuan S et al. Circular RNA expression profiling of human granulosa cells during maternal aging reveals novel transcripts associated with assisted reproductive technology outcomes. PLOS ONE 12(6), e0177888 (2017).
  MedlineGoogle Scholar
• 20. Liu X, Mai H, Chen P et al. Comparative analyses in transcriptome of human granulosa cells and follicular fluid micro-environment between poor ovarian responders with conventional controlled ovarian or mild ovarian stimulations. Reprod. Biol. Endocrinol. 20(1), 54 (2022).
  MedlineGoogle Scholar
• 21. Ma XK, Wang MR, Liu CX et al. CIRCexplorer3: a CLEAR pipeline for direct comparison of circular and linear RNA expression. Genomics Proteomics Bioinformatics 17(5), 511–521 (2019). • This is a software that can accurately identify circular RNAs by identifying back-splice junctions
  MedlineGoogle Scholar
• 22. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12(4), 357–360 (2015).
  Medline CASGoogle Scholar
• 23. Kim D, Salzberg SL. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol. 12(8), R72 (2011).
  Medline CASGoogle Scholar
• 24. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7), 923–930 (2014).
  Medline CASGoogle Scholar
• 25. Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41(10), e108 (2013).
  Medline CASGoogle Scholar
• 26. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12), 550 (2014).
  MedlineGoogle Scholar
• 27. Zhou Y, Zhou B, Pache L et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun. 10(1), 1523 (2019).
  MedlineGoogle Scholar
• 28. Liu M, Wang Q, Shen J, Yang BB, Ding X. Circbank: a comprehensive database for circRNA with standard nomenclature. RNA Biol. 16(7), 899–905 (2019).
  MedlineGoogle Scholar
• 29. Chen Y, Wang X. miRDB: an online database for prediction of functional microRNA targets. Nucleic Acids Res. 48(D1), D127–D131 (2020).
  Medline CASGoogle Scholar
• 30. Hsu SD, Lin FM, Wu WY et al. miRTarBase: a database curates experimentally validated microRNA-target interactions. Nucleic Acids Res. 39(Database issue), D163–169 (2011).
  Medline CASGoogle Scholar
• 31. Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. Elife 4 (2015).
  Google Scholar
• 32. Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5), 284–287 (2012).
  Medline CASGoogle Scholar
• 33. Zhong Y, Du Y, Yang X et al. Circular RNAs function as ceRNAs to regulate and control human cancer progression. Mol. Cancer 17(1), 79 (2018).
  MedlineGoogle Scholar
• 34. Martin JA, Hamilton BE, Osterman MJ, Curtin SC, Matthews TJ. Births: final data for 2013. Natl Vital Stat. Rep. 64(1), 1–65 (2015).
  Google Scholar
• 35. Navot D, Bergh PA, Williams MA et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337(8754), 1375–1377 (1991). •• This preliminary report suggests that the follicular microenvironment is a major determinant of oocyte quality and is recognized as a key factor limiting female fertility.
  Medline CASGoogle Scholar
• 36. Tatone C, Amicarelli F, Carbone MC et al. Cellular and molecular aspects of ovarian follicle ageing. Hum. Reprod. Update 14(2), 131–142 (2008). •• This review proposes that age-related dysfunction results from the physiological accumulation of irreparable damage to biomolecules from unavoidable side effects of normal metabolism.
  Medline CASGoogle Scholar
• 37. Pacella L, Zander-Fox DL, Armstrong DT, Lane M. Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil. Steril. 98(4), e981–982 (2012).
  Google Scholar
• 38. Brzezinski A, Saada A, Miller H, Brzezinski-Sinai NA, Ben-Meir A. Is the aging human ovary still ticking?: expression of clock-genes in luteinized granulosa cells of young and older women. J. Ovarian Res. 11(1), 95 (2018). •• This preliminary report suggests that molecular clock genes are present in human lutealized granulosa cells.
  Medline CASGoogle Scholar
• 39. Maiese K. Disease onset and aging in the world of circular RNAs. J. Transl. Sci. 2(6), 327–329 (2016).
  MedlineGoogle Scholar
• 40. Huang Q, Liu B, Jiang R et al. G-CSF-mobilized peripheral blood mononuclear cells combined with platelet-rich plasma accelerate restoration of ovarian function in cyclophosphamide-induced POI ratsdagger. Biol. Reprod. 101(1), 91–101 (2019). •• This preliminary report suggests that abnormal differentiation and activity of monocytes have been considered to be closely related to the decline of ovarian function.
  MedlineGoogle Scholar
• 41. Piwecka M, Glazar P, Hernandez-Miranda LR et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357(6357),eaam8526 (2017).
  MedlineGoogle Scholar
• 42. Hansen TB, Jensen TI, Clausen BH et al. Natural RNA circles function as efficient microRNA sponges. Nature 495(7441), 384–388 (2013).
  Medline CASGoogle Scholar
• 43. Gougeon A. Ovarian follicular growth in humans: ovarian ageing and population of growing follicles. Maturitas 30(2), 137–142 (1998). • This preliminary report suggests that during ovarian aging, granulosa cells showed a gradual decrease in mitotic activity
  Medline CASGoogle Scholar
• 44. Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol. Reprod. 65(1), 141–150 (2001).
  Medline CASGoogle Scholar
• 45. Wainer-Katsir K, Zou JY, Linial M. Extended fertility and longevity: the genetic and epigenetic link. Fertil. Steril. 103(5), 1117–1124 (2015).
  MedlineGoogle Scholar