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CLINICAL: RESEARCH COMMUNICATIONS

Age-related differential gene expression in granulosa cells and its effects on fertility using high-throughput transcriptomics

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Pages 190-202 | Received 19 Aug 2021, Accepted 09 Jan 2022, Published online: 24 Mar 2022

References

  • American College of Obstetricians and Gynecologists Committee on Gynecologic Practice and Practice Committee. 2014. Female Age-Related Fertility Decline. Committee Opinion No. 589. Obstet Gynecol 123:719–721.
  • Attali E, Yogev Y. 2021. The impact of advanced maternal age on pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 70:2–9.
  • Balasch J, Gratacós E. 2012. Delayed childbearing: effects on fertility and the outcome of pregnancy. Curr Opin Obstet Gynecol. 24(3):187–193.
  • Battaglia DE, Goodwin P, Klein NA, Soules MR. 1996. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 11:2217–2222.
  • Bellaver B, Souza DG, Souza DO, Quincozes-Santos A. 2017. Hippocampal astrocyte cultures from adult and aged rats reproduce changes in glial functionality observed in the aging brain. Mol Neurobiol 54:2969–2985.
  • Boots CE, Jungheim ES. 2015. Inflammation and human ovarian follicular dynamics. Semin Reprod Med 33:270–275.
  • Briley SM, Jasti S, McCracken JM, Hornick JE, Fegley B, Pritchard MT, Duncan FE. 2016. Reproductive age-associated fibrosis in the stroma of the mammalian ovary. Reproduction 152:245–260.
  • Camell CD, Günther P, Lee A, Goldberg EL, Spadaro O, Youm YH, Bartke A, Hubbard GB, Ikeno Y, Ruddle NH, et al. 2019. Aging induces an Nlrp3 inflammasome-dependent expansion of adipose B cells that impairs metabolic homeostasis. Cell Metab 30:1024–1039. e1026.
  • Centers for Disease Control and Prevention, American Society for Reproductive Medicine Society for ART 2012. 2010 assisted reproductive technology: fertility clinic success rates report. Atlanta (GA): Centers for Disease Control and Prevention, American Society for Reproductive Medicine Society for ART; [accessed year month date]. https://www.cdc.gov/art/ART2010/PDFs/ART_2010_Clinic_Report-Full.pdf.
  • Chandra A, Copen CE, Stephen EH. 2013. Infertility and impaired fecundity in the United States, 1982-2010: data from the National Survey of Family Growth. Natl Health Stat Rep 2013:1–18, 1 p following 19.
  • Charo LM, Homer MV, Natarajan L, Haunschild C, Chung K, Mao JJ, DeMichele AM, Su HI. 2021. Drug metabolising enzyme polymorphisms and chemotherapy-related ovarian failure in young breast cancer survivors. J Obstet Gynaecol 41:447–452.
  • Chung KW, Lee EK, Kim DH, An HJ, Kim ND, Im DS, Lee J, Yu BP, Chung HY. 2015. Age-related sensitivity to endotoxin-induced liver inflammation: implication of inflammasome/IL-1β for steatohepatitis. Aging Cell 14:524–533.
  • Dou X, Sun Y, Li J, Zhang J, Hao D, Liu W, Wu R, Kong F, Peng X, Li J. 2017. Short-term rapamycin treatment increases ovarian lifespan in young and middle-aged female mice. Aging Cell 16:825–836.
  • Franceschi C, Campisi J. 2014. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol A Biol Sci Med Sci 69:S4–S9.
  • Frederiksen LE, Ernst A, Brix N, Braskhøj Lauridsen LL, Roos L, Ramlau-Hansen CH, Ekelund CK. 2018. Risk of adverse pregnancy outcomes at advanced maternal age. Obstet Gynecol 131:457–463.
  • Fréour T, Miossec C, Bach-Ngohou K, Dejoie T, Flamant M, Maillard O, Denis MG, Barriere P, Bruley Des Varannes S, Bourreille A, et al. 2012. Ovarian reserve in young women of reproductive age with Crohn's disease. Inflamm Bowel Dis 18:1515–1522.
  • Furman D, Chang J, Lartigue L, Bolen CR, Haddad F, Gaudilliere B, Ganio EA, Fragiadakis GK, Spitzer MH, Douchet I, et al. 2017. Expression of specific inflammasome gene modules stratifies older individuals into two extreme clinical and immunological states. Nat Med 23:174–184.
  • Furman D, Jojic V, Kidd B, Shen-Orr S, Price J, Jarrell J, Tse T, Huang H, Lund P, Maecker HT, et al. 2013. Apoptosis and other immune biomarkers predict influenza vaccine responsiveness. Mol Syst Biol 9:659.
  • Furtado GE, Uba Chupel M, Minuzzi L, Patrício M, Loureiro M, Bandelow S, Hogervorst E, Ferreira JP, Teixeira AM. 2020. Exploring the potential of salivary and blood immune biomarkers to elucidate physical frailty in institutionalized older women. Exp Gerontol 129:110759.
  • Gill SK, Broussard C, Devine O, Green RF, Rasmussen SA, Reefhuis J, and the National Birth Defects Prevention Study 2012. Association between maternal age and birth defects of unknown etiology: United States, 1997–2007. Birth Defects Res A Clin Mol Teratol 94:1010–1018.
  • Gillies PJ, Richardson NA, Walshe J, Stephenson SA, Dawson RA, Harkin DG. 2018. Demonstration of P-selectin expression and potential function in human corneal epithelial cells. Exp Eye Res 176:196–206.
  • Hansen M, Kurinczuk JJ, Milne E, de Klerk N, Bower C. 2013. Assisted reproductive technology and birth defects: a systematic review and meta-analysis. Hum Reprod Update 19:330–353.
  • Hayes JD, Pulford DJ. 1995. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600.
  • Heffner LJ. 2004. Advanced maternal age–how old is too old? N Engl J Med 351:1927–1929.
  • Howcroft TK, Campisi J, Louis GB, Smith MT, Wise B, Wyss-Coray T, Augustine AD, McElhaney JE, Kohanski R, Sierra F. 2013. The role of inflammation in age-related disease. Aging 5:84–93.
  • Jiang T, Cadenas E. 2014. Astrocytic metabolic and inflammatory changes as a function of age. Aging Cell 13:1059–1067.
  • Jiang P, Sheng Y, Ji L. 2013. The age-related change of glutathione antioxidant system in mice liver. Toxicol Mech Methods 23:396–401.
  • Kim DH, Lee B, Lee J, Kim ME, Lee JS, Chung JH, Yu BP, Dong HH, Chung HY. 2019. FoxO6-mediated IL-1β induces hepatic insulin resistance and age-related inflammation via the TF/PAR2 pathway in aging and diabetic mice. Redox Biol 24:101184.
  • Li Y, Zhao W, Zhao Z, Wu J, Chen L, Ma Y, Li Q, Lu D, Jin L, Wang J. 2015. Association study on IL1B gene polymorphisms and the risk of non-small cell lung cancer. Chinese Master's Theses Full-text Database. Fudan University 89:232–237.
  • Liao CR, Wang SN, Zhu SY, Wang YQ, Li ZZ, Liu ZY, Jiang WS, Chen JT, Wu Q. 2020. Advanced oxidation protein products increase TNF-α and IL-1β expression in chondrocytes via NADPH oxidase 4 and accelerate cartilage degeneration in osteoarthritis progression. Redox Biol 28:101306.
  • Lim MA, Lee J, Park JS, Jhun JY, Moon YM, Cho ML, Kim HY. 2014. Increased Th17 differentiation in aged mice is significantly associated with high IL-1β level and low IL-2 expression. Exp Gerontol 49:55–62.
  • Lliberos C, Liew SH, Zareie P, La Gruta NL, Mansell A, Hutt K. 2021. Evaluation of inflammation and follicle depletion during ovarian ageing in mice. Sci Rep 11:278.
  • Messerschmidt L, Fischer S, Wiedemann P, Bringmann A, Hollborn M. 2019. Osmotic induction of cyclooxygenase-2 in RPE cells: Stimulation of inflammasome activation. Mol Vis 25:329–344.
  • Nakamura Y, Aihara R, Iwata H, Kuwayama T, Shirasuna K. 2021. IL1B triggers inflammatory cytokine production in bovine oviduct epithelial cells and induces neutrophil accumulation via CCL2. Am J Reprod Immunol 85:e13365.
  • Nakamura Y, Iwata H, Kuwayama T, Shirasuna K. 2019. S100A8, which increases with age, induces cellular senescence-like changes in bovine oviduct epithelial cells. Am J Reprod Immunol 82:e13163.
  • Nasu K, Itoh H, Yuge A, Kawano Y, Yoshimatsu J, Narahara H. 2006. Interleukin-1beta regulates vascular endothelial growth factor and soluble fms-like tyrosine kinase-1 secretion by human oviductal epithelial cells and stromal fibroblasts. Gynecol Endocrinol 22:495–500.
  • OECD Family Database 2019. Age of mothers at childbirth and age-specific fertility. OECD; [accessed year month date]. https://www.oecd.org/els/soc/sf_2_3_age_mothers_childbirth.pdf.
  • Pence BD, Yarbro JR. 2019. Classical monocytes maintain ex vivo glycolytic metabolism and early but not later inflammatory responses in older adults. Immun Ageing 16:3.
  • Perheentupa A, Huhtaniemi I. 2009. Aging of the human ovary and testis. Mol Cell Endocrinol 299:2–13.
  • Polimanti R, Carboni C, Baesso I, Piacentini S, Iorio A, De Stefano GF, Fuciarelli M. 2013. Genetic variability of glutathione S-transferase enzymes in human populations: functional inter-ethnic differences in detoxification systems. Gene 512:102–107.
  • Prince CS, Noren Hooten N, Mode NA, Zhang Y, Ejiogu N, Becker KG, Zonderman AB, Evans MK. 2019. Frailty in middle age is associated with frailty status and race-specific changes to the transcriptome. Aging 11:5518–5534.
  • Qiao J, Yang R. 2017. Clinical outcome of assisted reproductive technology in women at advanced maternal age. Chinese J Practical Gynecol Obst 33:64–67.
  • Qin J, Liu X, Sheng X, Wang H, Gao S. 2016. Assisted reproductive technology and the risk of pregnancy-related complications and adverse pregnancy outcomes in singleton pregnancies: a meta-analysis of cohort studies. Fertil Steril 105:73–85. e71–76.
  • Reproductive Medicine Committee of Chinese Medical Doctor Association. 2017. Guidelines for the diagnosis and treatment of infertility in older women. Chinese J Reprod Contraception 37:87–100.
  • Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. 2009. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 7:40.
  • Sauer MV. 2015. Reproduction at an advanced maternal age and maternal health. Fertil Steril 103:1136–1143.
  • Schmitt V, Rink L, Uciechowski P. 2013. The Th17/Treg balance is disturbed during aging. Exp Gerontol 48:1379–1386.
  • Schwartz D, Mayaux MJ. 1982. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med 306:404–406.
  • Sheen JJ, Wright JD, Goffman D, Kern-Goldberger AR, Booker W, Siddiq Z, D'Alton ME, Friedman AM. 2018. Maternal age and risk for adverse outcomes. Am J Obstet Gynecol 219:390.e391–390.e315.
  • Shen-Orr SS, Furman D, Kidd BA, Hadad F, Lovelace P, Huang Y-W, Rosenberg-Hasson Y, Mackey S, Grisar FAG, Pickman Y, et al. 2016. Defective signaling in the JAK-STAT pathway tracks with chronic inflammation and cardiovascular risk in aging humans. Cell Syst 3:374–384. e374.
  • Shi L, Zhao Y, Fei C, Guo J, Jia Y, Wu D, Wu L, Chang C. 2019. Cellular senescence induced by S100A9 in mesenchymal stromal cells through NLRP3 inflammasome activation. Aging 11:9626–9642.
  • Sparkman NL, Buchanan JB, Dos Santos NL, Johnson RW, Burton MD. 2019. Aging sensitizes male mice to cognitive dysfunction induced by central HIV-1 gp120. Exp Gerontol 126:110694.
  • Strange RC, Spiteri MA, Ramachandran S, Fryer AA. 2001. Glutathione-S-transferase family of enzymes. Mut Res 482:21–26.
  • Sun Y, Zhu YM. 2014. Aged infertile couples, perplexity of modern assisted reproductive technology. Chinese J Family Plan Gynecotokology 6:1–3.
  • Sweeney C, McClure GY, Fares MY, Stone A, Coles BF, Thompson PA, Korourian S, Hutchins LF, Kadlubar FF, Ambrosone CB. 2000. Association between survival after treatment for breast cancer and glutathione S-transferase P1 Ile105Val polymorphism. Cancer Res 60:5621–5624.
  • Tanaka H, Ohtsu A, Shiratsuki S, Kawahara-Miki R, Iwata H, Kuwayama T, Shirasuna K. 2016. Age-dependent changes in inflammation and extracellular matrix in bovine oviduct epithelial cells during the post-ovulatory phase. Mol Reprod Dev 83:815–826.
  • Uri-Belapolsky S, Shaish A, Eliyahu E, Grossman H, Levi M, Chuderland D, Ninio-Many L, Hasky N, Shashar D, Almog T, et al. 2014. Interleukin-1 deficiency prolongs ovarian lifespan in mice. Proc Natl Acad Sci USA 111:12492–12497.
  • Vannuccini S, Clifton VL, Fraser IS, Taylor HS, Critchley H, Giudice LC, Petraglia F. 2016. Infertility and reproductive disorders: impact of hormonal and inflammatory mechanisms on pregnancy outcome. Hum Reprod Update 22:104–115.
  • Wang G, Zhou Y, Wang Y, Li D, Liu J, Zhang F. 2019. Age-associated dopaminergic neuron loss and midbrain glia cell phenotypic polarization. Neuroscience 415:89–96.
  • Watanabe S, Kawamoto S, Ohtani N, Hara E. 2017. Impact of senescence-associated secretory phenotype and its potential as a therapeutic target for senescence-associated diseases. Cancer Sci 108:563–569.
  • Winger EE, Reed JL, Ashoush S, Ahuja S, El-Toukhy T, Taranissi M. 2008. Treatment with adalimumab (Humira) and intravenous immunoglobulin improves pregnancy rates in women undergoing IVF. Am J Reprod Immunol 61:113–120.
  • Xu S, Hou D, Liu J, Ji L. 2018. Age-associated changes in GSH S-transferase gene/proteins in livers of rats. Redox Rep 23:213–218.
  • Yao K, Zhao YF. 2018. Aging modulates microglia phenotypes in neuroinflammation of MPTP-PD mice. Exp Gerontol 111:86–93.
  • Yo K, Rünger TM. 2018. The long non-coding RNA FLJ46906 binds to the transcription factors NF-κB and AP-1 and regulates expression of aging-associated genes. Aging 10:2037–2050.
  • Zhang Z, Schlamp F, Huang L, Clark H, Brayboy L. 2020. Inflammaging is associated with shifted macrophage ontogeny and polarization in the aging mouse ovary. Reproduction 159:325–337.
  • Zhong JF. 2019. Comparison of aging-related gene expression in different tissues of Omi/HtrA2 knockout mice. Chinese Master's Theses Full-text Database: Jilin University.