Interleukin-22 promotes proliferation and reverses LPS-induced apoptosis and steroidogenesis attenuation in human ovarian granulosa cells: implications for polycystic ovary syndrome pathogenesis

References

• Rotterdam ESHER/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril. 2003;81(1):19–25.
   Web of Science ®Google Scholar
• Lizneva D, Suturina L, Walker W, et al. Criteria, prevalence, and phenotypes of polycystic ovary syndrome. Fertil Steril. 2016;106(1):6–15. doi:10.1016/j.fertnstert.2016.05.003.
   PubMed Web of Science ®Google Scholar
• Kelly CC, Lyall H, Petrie JR, et al. Low grade chronic inflammation in women with polycystic ovarian syndrome. J Clin Endocrinol Metab. 2001;86(6):2453–2455. doi:10.1210/jcem.86.6.7580.
   PubMed Web of Science ®Google Scholar
• Möhlig M, Spranger J, Osterhoff M, et al. The polycystic ovary syndrome per se is not associated with increased chronic inflammation. Eur J Endocrinol. 2004;150(4):525–532. doi:10.1530/eje.0.1500525.
   PubMed Web of Science ®Google Scholar
• Escobar-Morreale HF, Luque-Ramírez M, González F. Circulating inflammatory markers in polycystic ovary syndrome: a systematic review and meta-analysis. Fertil Steril. 2011;95(3):1048–1058.e2. e1041-1042. doi:10.1016/j.fertnstert.2010.11.036.
   PubMed Web of Science ®Google Scholar
• Kaipia A, Chun SY, Eisenhauer K, et al. Tumor necrosis factor-alpha and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles. Endocrinology. 1996;137(11):4864–4870. doi:10.1210/endo.137.11.8895358.
   PubMed Web of Science ®Google Scholar
• Soboloff J, Sasaki H, Tsang BK. Follicular stage-dependent tumor necrosis factor alpha-induced hen granulosa cell integrin production and survival in the presence of transforming growth factor alpha in vitro. Biol Reprod. 2001;65(2):477–487. doi:10.1095/biolreprod65.2.477.
   PubMed Web of Science ®Google Scholar
• Thackray VG. Sex, microbes, and polycystic ovary syndrome. Trends Endocrinol Metab. 2019;30(1):54–65. doi:10.1016/j.tem.2018.11.001.
   PubMed Web of Science ®Google Scholar
• Karuputhula NB, Chattopadhyay R, Chakravarty B, et al. Oxidative status in granulosa cells of infertile women undergoing IVF. Syst Biol Reprod Med. 2013;59(2):91–98. doi:10.3109/19396368.2012.743197.
   PubMed Web of Science ®Google Scholar
• Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122(6):829–838. doi:10.1530/rep.0.1220829.
   PubMed Web of Science ®Google Scholar
• Dudakov JA, Hanash AM, van den Brink MR. Interleukin-22: immunobiology and pathology. Annu Rev Immunol. 2015;33(1):747–785. doi:10.1146/annurev-immunol-032414-112123.
   PubMedGoogle Scholar
• Lindemans CA, Calafiore M, Mertelsmann AM, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature. 2015;528(7583):560–564. doi:10.1038/nature16460.
   PubMed Web of Science ®Google Scholar
• Wolk K, Witte E, Witte K, et al. Biology of interleukin-22. Semin Immunopathol. 2010;32(1):17–31. doi:10.1007/s00281-009-0188-x.
   PubMed Web of Science ®Google Scholar
• McGee HM, Schmidt BA, Booth CJ, et al. IL-22 promotes fibroblast-mediated wound repair in the skin. J Invest Dermatol. 2013;133(5):1321–1329. doi:10.1038/jid.2012.463.
   PubMed Web of Science ®Google Scholar
• Wang X, Ota N, Manzanillo P, et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature. 2014;514(7521):237–241. doi:10.1038/nature13564.
   PubMed Web of Science ®Google Scholar
• Abadpour S, Halvorsen B, Sahraoui A, et al. Interleukin-22 reverses human islet dysfunction and apoptosis triggered by hyperglycemia and LIGHT. J Mol Endocrinol. 2018;60(3):171–183. doi:10.1530/JME-17-0182.
   PubMed Web of Science ®Google Scholar
• Kolumam G, Wu X, Lee WP, et al. IL-22R ligands IL-20, IL-22, and IL-24 promote wound healing in diabetic db/db mice. PLOS One. 2017;12(1):e0170639. doi:10.1371/journal.pone.0170639.
   PubMed Web of Science ®Google Scholar
• Feng D, Park O, Radaeva S, et al. Interleukin-22 ameliorates cerulein-induced pancreatitis in mice by inhibiting the autophagic pathway. Int J Biol Sci. 2012;8(2):249–257. doi:10.7150/ijbs.3967.
   PubMed Web of Science ®Google Scholar
• Sabat R, Ouyang W, Wolk K. Therapeutic opportunities of the IL-22-IL-22R1 system. Nat Rev Drug Discov. 2014;13(1):21–38. doi:10.1038/nrd4176.
   PubMed Web of Science ®Google Scholar
• Rutz S, Wang X, Ouyang W. The IL-20 subfamily of cytokines–from host defence to tissue homeostasis. Nat Rev Immunol. 2014;14(12):783–795. doi:10.1038/nri3766.
   PubMed Web of Science ®Google Scholar
• Xie Q, Huang C, Li J. Interleukin-22 and rheumatoid arthritis: emerging role in pathogenesis and therapy. Autoimmunity. 2015;48(2):69–72. doi:10.3109/08916934.2014.959165.
   PubMed Web of Science ®Google Scholar
• Kim J, Krueger JG. The immunopathogenesis of psoriasis. Dermatol Clin. 2015;33(1):13–23. doi:10.1016/j.det.2014.09.002.
   PubMed Web of Science ®Google Scholar
• Qi X, Nie Q, Pang Y, et al. IL-22 and its interaction with amino acid and glycolipid metabolite in polycystic ovary syndrome (PCOS) patients. Chin Med J. 2022;135(10):1258–1260. doi:10.1097/CM9.0000000000001915.
   PubMed Web of Science ®Google Scholar
• Rotterdam ESHER/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2003;19(1):41–47.
   Web of Science ®Google Scholar
• Yan MQ, Wang Y, Wang Z, et al. Mitoguardin2 is associated with hyperandrogenism and regulates steroidogenesis in human ovarian granulosa cells. J Endocr Soc. 2023;7(5):bvad034.
   PubMed Web of Science ®Google Scholar
• Qi X, Yun C, Sun L, et al. Gut microbiota-bile acid-interleukin-22 axis orchestrates polycystic ovary syndrome. Nat Med. 2019;25(8):1225–1233. doi:10.1038/s41591-019-0509-0.
   PubMed Web of Science ®Google Scholar
• De Simone V, Franzè E, Ronchetti G, et al. Th17-type cytokines, IL-6 and TNF-α synergistically activate STAT3 and NF-kB to promote colorectal cancer cell growth. Oncogene. 2015;34(27):3493–3503. doi:10.1038/onc.2014.286.
   PubMed Web of Science ®Google Scholar
• Aggor FEY, Break TJ, Trevejo-Nuñez G, et al. Oral epithelial IL-22/STAT3 signaling licenses IL-17-mediated immunity to oral mucosal candidiasis. Sci Immunol. 2020;5(48):eaba0570. doi:10.1126/sciimmunol.aba0570.
   PubMed Web of Science ®Google Scholar
• González F. Inflammation in polycystic ovary syndrome: underpinning of insulin resistance and ovarian dysfunction. Steroids. 2012;77(4):300–305. doi:10.1016/j.steroids.2011.12.003.
   PubMed Web of Science ®Google Scholar
• Huang J, Chen P, Xiang Y, et al. Gut microbiota dysbiosis-derived macrophage pyroptosis causes polycystic ovary syndrome via steroidogenesis disturbance and apoptosis of granulosa cells. Int Immunopharmacol. 2022;107:108717. doi:10.1016/j.intimp.2022.108717.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Ran Y, Kong L, et al. Decreased SFRP5 correlated with excessive metabolic inflammation in polycystic ovary syndrome could be reversed by metformin: implication of its role in dysregulated metabolism. J Ovarian Res. 2021;14(1):97. doi:10.1186/s13048-021-00847-4.
   PubMed Web of Science ®Google Scholar
• Hines IN, Kremer M, Isayama F, et al. Impaired liver regeneration and increased oval cell numbers following T cell-mediated hepatitis. Hepatology. 2007;46(1):229–241. doi:10.1002/hep.21674.
   PubMed Web of Science ®Google Scholar
• Mühl H, Scheiermann P, Bachmann M, et al. IL-22 in tissue-protective therapy. Br J Pharmacol. 2013;169(4):761–771. doi:10.1111/bph.12196.
   PubMed Web of Science ®Google Scholar
• Zhuang L, Ma W, Yan J, et al. Evaluation of the effects of IL‑22 on the proliferation and differentiation of keratinocytes in vitro. Mol Med Rep. 2020;22(4):2715–2722. doi:10.3892/mmr.2020.11348.
   PubMed Web of Science ®Google Scholar
• Lejeune D, Dumoutier L, Constantinescu S, et al. Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10. J Biol Chem. 2002;277(37):33676–33682. doi:10.1074/jbc.M204204200.
   PubMed Web of Science ®Google Scholar
• Yu J, Xiao Z, Zhao R, et al. Paeoniflorin suppressed IL-22 via p38 MAPK pathway and exerts anti-psoriatic effect. Life Sci. 2017;180:17–22. doi:10.1016/j.lfs.2017.04.019.
   PubMed Web of Science ®Google Scholar
• Li H, Zhang Q, Wu Q, et al. Interleukin-22 secreted by cancer-associated fibroblasts regulates the proliferation and metastasis of lung cancer cells via the PI3K-Akt-mTOR signaling pathway. Am J Tran Re. 2019;11(7):4077–4088.
   PubMed Web of Science ®Google Scholar
• Zhang W, Chen Y, Wei H, et al. Antiapoptotic activity of autocrine interleukin-22 and therapeutic effects of interleukin-22-small interfering RNA on human lung cancer xenografts. Clin Cancer Res. 2008;14(20):6432–6439. doi:10.1158/1078-0432.CCR-07-4401.
   PubMed Web of Science ®Google Scholar
• Wang B, Han D, Li F, et al. Elevated IL-22 in psoriasis plays an anti-apoptotic role in keratinocytes through mediating Bcl-xL/Bax. Apoptosis. 2020;25(9–10):663–673. doi:10.1007/s10495-020-01623-3.
   PubMed Web of Science ®Google Scholar
• Havelock JC, Rainey WE, Carr BR. Ovarian granulosa cell lines. Mol Cell Endocrinol. 2004;228(1-2):67–78. doi:10.1016/j.mce.2004.04.018.
   PubMed Web of Science ®Google Scholar
• Sanchez AM, Vanni VS, Bartiromo L, et al. Is the oocyte quality affected by endometriosis? A review of the literature. J Ovarian Res. 2017;10(1):43. doi:10.1186/s13048-017-0341-4.
   PubMedGoogle Scholar
• Das M, Djahanbakhch O, Hacihanefioglu B, et al. Granulosa cell survival and proliferation are altered in polycystic ovary syndrome. J Clin Endocrinol Metab. 2008;93(3):881–887. doi:10.1210/jc.2007-1650.
   PubMed Web of Science ®Google Scholar
• Wang M, Sun J, Xu B, et al. Functional characterization of microRNA-27a-3p expression in human polycystic ovary syndrome. Endocrinology. 2018;159(1):297–309. doi:10.1210/en.2017-00219.
   PubMed Web of Science ®Google Scholar
• Mehta, Anu, Onteru, Suneel Kumar, Singh, Dheer Ravinder,. HDAC inhibitor prevents LPS mediated inhibition of CYP19A1 expression and 17β-estradiol production in granulosa cells. Mol Cell Endocrinol. 2015; 414:73–81. doi:10.1016/j.mce.2015.07.002.
   PubMed Web of Science ®Google Scholar
• Qu X, Yan L, Guo R, et al. ROS-Induced GATA4 and GATA6 downregulation inhibits StAR expression in LPS-treated porcine granulosa-lutein cells. Oxid Med Cell Longev. 2019;2019:5432792–5432714. doi:10.1155/2019/5432792.
   PubMed Web of Science ®Google Scholar
• Stephanou A, Brar BK, Knight RA, et al. Opposing actions of STAT-1 and STAT-3 on the Bcl-2 and Bcl-x promoters. Cell Death Differ. 2000;7(3):329–330. doi:10.1038/sj.cdd.4400656.
   PubMed Web of Science ®Google Scholar
• Masuda M, Suzui M, Yasumatu R, et al. Constitutive activation of signal transducers and activators of transcription 3 correlates with cyclin D1 overexpression and may provide a novel prognostic marker in head and neck squamous cell carcinoma. Cancer Res. 2002;62(12):3351–3355.
   PubMed Web of Science ®Google Scholar
• Bowman T, Broome MA, Sinibaldi D, et al. Stat3-mediated myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc Natl Acad Sci U S A. 2001;98(13):7319–7324. doi:10.1073/pnas.131568898.
   PubMed Web of Science ®Google Scholar
• Murray PJ. The JAK-STAT signaling pathway: input and output integration. J Immunol. 2007;178(5):2623–2629. doi:10.4049/jimmunol.178.5.2623.
   PubMed Web of Science ®Google Scholar
• El Kasmi KC, Smith AM, Williams L, et al. Cutting edge: a transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway. J Immunol. 2007;179(11):7215–7219. doi:10.4049/jimmunol.179.11.7215.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yang Q, Wang H, et al. NAD + deficiency and mitochondrial dysfunction in granulosa cells of women with polycystic ovary syndrome‡. Biol Reprod. 2021;105(2):371–380. doi:10.1093/biolre/ioab078.
   PubMed Web of Science ®Google Scholar
• Li M, Zhao H, Zhao SG, et al. The HMGA2-IMP2 pathway promotes granulosa cell proliferation in polycystic ovary syndrome. J Clin Endocrinol Metab. 2019;104(4):1049–1059. doi:10.1210/jc.2018-00544.
   PubMed Web of Science ®Google Scholar
• Zhou R, Li S, Liu J, et al. Up-regulated FHL2 inhibits ovulation through interacting with androgen receptor and ERK1/2 in polycystic ovary syndrome. EBioMedicine. 2020;52:102635. doi:10.1016/j.ebiom.2020.102635.
   PubMed Web of Science ®Google Scholar
• Nishi Y, Yanase T, Mu Y, et al. Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology. 2001;142(1):437–445. doi:10.1210/endo.142.1.7862.
   PubMed Web of Science ®Google Scholar