46
Views
0
CrossRef citations to date
0
Altmetric
Review Article

The administration of human amniotic epithelial cells in premature ovarian insufficiency: From preclinical to clinical

, , , , &
Article: 2382818 | Received 13 Mar 2024, Accepted 12 Jul 2024, Published online: 22 Jul 2024

References

  • Golezar S, Ramezani Tehrani F, Khazaei S, et al. The global prevalence of primary ovarian insufficiency and early menopause: a meta-analysis. Climacteric. 2019;22(4):403–411. doi: 10.1080/13697137.2019.1574738.
  • Ishizuka B. Current understanding of the etiology, symptomatology, and treatment options in premature ovarian insufficiency (POI). Front Endocrinol (Lausanne). 2021;12:626924. doi: 10.3389/fendo.2021.626924.
  • Maclaran K, Panay N. Current concepts in premature ovarian insufficiency. Womens Health (Lond). 2015;11(2):169–182. doi: 10.2217/whe.14.82.
  • Ke H, Tang S, Guo T, et al. Landscape of pathogenic mutations in premature ovarian insufficiency. Nat Med. 2023;29(2):483–492. doi: 10.1038/s41591-022-02194-3.
  • Cohen LE. Cancer treatment and the ovary: the effects of chemotherapy and radiation. Ann N Y Acad Sci. 2008;1135(1):123–125. doi: 10.1196/annals.1429.023.
  • Ebrahimi M, Akbari Asbagh F. Pathogenesis and causes of premature ovarian failure: an update. Int J Fertil Steril. 2011;5(2):54–65.
  • Chon SJ, Umair Z, Yoon MS. Premature ovarian insufficiency: past, present, and future. Front Cell Dev Biol. 2021;9:672890. doi: 10.3389/fcell.2021.672890.
  • Wesevich V, Kellen AN, Pal L. Recent advances in understanding primary ovarian insufficiency. F1000Res. 2020;9:1101. doi: 10.12688/f1000research.26423.1.
  • Angarita AM, Johnson CA, Fader AN, et al. Fertility preservation: a key survivorship issue for young women with cancer. Front Oncol. 2016;6:102. doi: 10.3389/fonc.2016.00102.
  • Huang QY, Chen SR, Chen JM, et al. Therapeutic options for premature ovarian insufficiency: an updated review. Reprod Biol Endocrinol. 2022;20(1):28. doi: 10.1186/s12958-022-00892-8.
  • Miki T, Lehmann T, Cai H, et al. Stem cell characteristics of amniotic epithelial cells. Stem Cells. 2005;23(10):1549–1559. doi: 10.1634/stemcells.2004-0357.
  • Yao X, Guo Y, Wang Q, et al. The paracrine effect of transplanted human amniotic epithelial cells on ovarian function improvement in a mouse model of chemotherapy-induced primary ovarian insufficiency. Stem Cells Int. 2016;2016:4148923–4148914. doi: 10.1155/2016/4148923.
  • Zhang Q, Bu S, Sun J, et al. Paracrine effects of human amniotic epithelial cells protect against chemotherapy-induced ovarian damage. Stem Cell Res Ther. 2017; Nov 288(1):270. doi: 10.1186/s13287-017-0721-0.
  • Zhang Q, Huang Y, Sun J, et al. Immunomodulatory effect of human amniotic epithelial cells on restoration of ovarian function in mice with autoimmune ovarian disease. Acta Biochim Biophys Sin (Shanghai). 2019;51(8):845–855. doi: 10.1093/abbs/gmz065.
  • Zhang Q, Sun J, Huang Y, et al. Human amniotic epithelial cell-derived exosomes restore ovarian function by transferring MicroRNAs against apoptosis. Mol Ther Nucleic Acids. 2019;16:407–418. doi: 10.1016/j.omtn.2019.03.008.
  • Zhang Q, Xu M, Yao X, et al. Human amniotic epithelial cells inhibit granulosa cell apoptosis induced by chemotherapy and restore the fertility. Stem Cell Res Ther. 2015;6(1):152. doi: 10.1186/s13287-015-0148-4.
  • Zhang Y, Ouyang X, You S, et al. Effect of human amniotic epithelial cells on ovarian function, fertility and ovarian reserve in primary ovarian insufficiency rats and analysis of underlying mechanisms by mRNA sequencing. Am J Transl Res. 2020;12(7):3234–3254.
  • Akle CA, Adinolfi M, Welsh KI, et al. Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet. 1981;2(8254):1003–1005. doi: 10.1016/s0140-6736(81)91212-5.
  • Yang PJ, Yuan WX, Liu J, et al. Biological characterization of human amniotic epithelial cells in a serum-free system and their safety evaluation. Acta Pharmacol Sin. 2018;39(8):1305–1316. doi: 10.1038/aps.2018.22.
  • Ferdousi F, Isoda H. Regulating early biological events in human amniotic epithelial stem cells using natural bioactive compounds: extendable multidirectional research avenues. Front Cell Dev Biol. 2022;10:865810. doi: 10.3389/fcell.2022.865810.
  • Li J, Qiu C, Wei Y, et al. Human amniotic epithelial stem cell-derived retinal pigment epithelium cells repair retinal degeneration. Front Cell Dev Biol. 2021;9:737242. doi: 10.3389/fcell.2021.737242.
  • Miki T. Stem cell characteristics and the therapeutic potential of amniotic epithelial cells. Am J Reprod Immunol. 2018;80(4):e13003. doi: 10.1111/aji.13003.
  • Wang F, Wang L, Yao X, et al. Human amniotic epithelial cells can differentiate into granulosa cells and restore folliculogenesis in a mouse model of chemotherapy-induced premature ovarian failure. Stem Cell Res Ther. 2013;4(5):124. doi: 10.1186/scrt335.
  • Liesveld JL, Sharma N, Aljitawi OS. Stem cell homing: from physiology to therapeutics. Stem Cells. 2020;38(10):1241–1253. doi: 10.1002/stem.3242.
  • Evans MA, Lim R, Kim HA, et al. Acute or delayed systemic administration of human amnion epithelial cells improves outcomes in experimental stroke. Stroke. 2018;49(3):700–709. doi: 10.1161/STROKEAHA.117.019136.
  • Ozaki Y, Nishimura M, Sekiya K, et al. Comprehensive analysis of chemotactic factors for bone marrow mesenchymal stem cells. Stem Cells Dev. 2007;16(1):119–129. doi: 10.1089/scd.2006.0032.
  • Bu S, Zhang Q, Wang Q, et al. Human amniotic epithelial cells inhibit growth of epithelial ovarian cancer cells via TGF‑β1-mediated cell cycle arrest. Int J Oncol. 2017;51(5):1405–1414. doi: 10.3892/ijo.2017.4123.
  • Kakishita K, Nakao N, Sakuragawa N, et al. Implantation of human amniotic epithelial cells prevents the degeneration of nigral dopamine neurons in rats with 6-hydroxydopamine lesions. Brain Res. 2003;980(1):48–56. doi: 10.1016/s0006-8993(03)02875-0.
  • Wang G, Zhao F, Yang D, et al. Human amniotic epithelial cells regulate osteoblast differentiation through the secretion of TGFβ1 and microRNA-34a-5p. Int J Mol Med. 2018;41(2):791–799. doi: 10.3892/ijmm.2017.3261.
  • Wu B, Gao F, Lin J, et al. Conditioned medium of human amniotic epithelial cells alleviates experimental allergic conjunctivitis mainly by IL-1ra and IL-10. Front Immunol. 2021;12:774601. doi: 10.3389/fimmu.2021.774601.
  • Wu Q, Fang T, Lang H, et al. Comparison of the proliferation, migration and angiogenic properties of human amniotic epithelial and mesenchymal stem cells and their effects on endothelial cells. Int J Mol Med. 2017;39(4):918–926. doi: 10.3892/ijmm.2017.2897.
  • Zhang J, Li H, Yang H, et al. Human amniotic epithelial cells alleviate a mouse model of parkinson’s disease mainly by neuroprotective, anti-oxidative and anti-inflammatory factors. J Neuroimmune Pharmacol. 2021;16(3):620–633. doi: 10.1007/s11481-020-09969-w.
  • Gao Y, Chen J, Ji R, et al. USP25 regulates the proliferation and apoptosis of ovarian granulosa cells in polycystic ovary syndrome by modulating the PI3K/AKT pathway via deubiquitinating PTEN. Front Cell Dev Biol. 2021;9:779718. doi: 10.3389/fcell.2021.779718.
  • Gong Y, Luo S, Fan P, et al. Growth hormone activates PI3K/Akt signaling and inhibits ROS accumulation and apoptosis in granulosa cells of patients with polycystic ovary syndrome. Reprod Biol Endocrinol. 2020;18(1):121. doi: 10.1186/s12958-020-00677-x.
  • Hall SE, Upton RMO, McLaughlin EA, et al. Phosphoinositide 3-kinase/protein kinase B (PI3K/AKT) and Janus kinase/signal transducer and activator of transcription (JAK/STAT) follicular signalling is conserved in the mare ovary. Reprod Fertil Dev. 2018;30(4):624–633. doi: 10.1071/RD17024.
  • Huang YH, Dong LP, Cui YG, et al. MiR-520h inhibits viability and facilitates apoptosis of KGN cells through modulating IL6R and the JAK/STAT pathway. Reprod Biol. 2022;22(1):100607. doi: 10.1016/j.repbio.2022.100607.
  • López-Onieva L, Fernández-Miñán A, González-Reyes A. Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary. Development. 2008;135(3):533–540. doi: 10.1242/dev.016121.
  • Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018;75(2):193–208. doi: 10.1007/s00018-017-2595-9.
  • Moeinabadi-Bidgoli K, Rezaee M, Rismanchi H, et al. Mesenchymal stem cell-derived antimicrobial peptides as potential anti-neoplastic agents: new insight into anticancer mechanisms of stem cells and exosomes. Front Cell Dev Biol. 2022;10:900418. doi: 10.3389/fcell.2022.900418.
  • van Niel G, Porto-Carreiro I, Simoes S, et al. Exosomes: a common pathway for a specialized function. J Biochem. 2006;140(1):13–21. doi: 10.1093/jb/mvj128.
  • Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30(1):255–289. doi: 10.1146/annurev-cellbio-101512-122326.
  • Gurunathan S, Kang MH, Jeyaraj M, et al. Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells. 2019;8(4):307. doi: 10.3390/cells8040307.
  • Kalluri R. The biology and function of exosomes in cancer. J Clin Invest. 2016;126(4):1208–1215. doi: 10.1172/JCI81135.
  • Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 2014;29:116–125. doi: 10.1016/j.ceb.2014.05.004.
  • Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008;8(19):4083–4099. doi: 10.1002/pmic.200800109.
  • Lu Y, Huang W, Li M, et al. Exosome-based carrier for RNA Delivery: progress and challenges. Pharmaceutics. 2023;15(2):598. doi: 10.3390/pharmaceutics15020598.
  • Herberts CA, Kwa MS, Hermsen HP. Risk factors in the development of stem cell therapy. J Transl Med. 2011;9(1):29. doi: 10.1186/1479-5876-9-29.
  • Srinivasan RC, Kannisto K, Strom SC, et al. Evaluation of different routes of administration and biodistribution of human amnion epithelial cells in mice. Cytotherapy. 2019;21(1):113–124. doi: 10.1016/j.jcyt.2018.10.007.
  • Yan L, Wu Y, Li L, et al. Clinical analysis of human umbilical cord mesenchymal stem cell allotransplantation in patients with premature ovarian insufficiency. Cell Prolif. 2020;53(12):e12938.
  • Ding L, Yan G, Wang B, et al. Transplantation of UC-MSCs on collagen scaffold activates follicles in dormant ovaries of POF patients with long history of infertility. Sci China Life Sci. 2018;61(12):1554–1565. doi: 10.1007/s11427-017-9272-2.
  • Mashayekhi M, Mirzadeh E, Chekini Z, et al. Evaluation of safety, feasibility and efficacy of intra-ovarian transplantation of autologous adipose derived mesenchymal stromal cells in idiopathic premature ovarian failure patients: non-randomized clinical trial, phase I, first in human. J Ovarian Res. 2021;14(1):5. doi: 10.1186/s13048-020-00743-3.
  • Edessy M, Hosni HN, Shady Y, et al. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Med Int. 2016;3(1):19–23. doi: 10.5530/ami.2016.1.7.
  • Zafardoust S, Kazemnejad S, Darzi M, et al. Improvement of pregnancy rate and live birth rate in poor ovarian responders by intraovarian administration of autologous menstrual blood derived- mesenchymal stromal cells: phase I/II clinical trial. Stem Cell Rev Rep. 2020;16(4):755–763. doi: 10.1007/s12015-020-09969-6.
  • Kuchakzadeh F, Ai J, Ebrahimi-Barough S. Tissue engineering and stem cell-based therapeutic strategies for premature ovarian insufficiency. Regen Ther. 2024;25:10–23. doi: 10.1016/j.reth.2023.11.007.
  • Zhang S, Zhu D, Mei X, et al. Advances in biomaterials and regenerative medicine for primary ovarian insufficiency therapy. Bioact Mater. 2021;6(7):1957–1972. doi: 10.1016/j.bioactmat.2020.12.008.
  • Vosdoganes P, Wallace EM, Chan ST, et al. Human amnion epithelial cells repair established lung injury. Cell Transplant. 2013;22(8):1337–1349. doi: 10.3727/096368912X657657.
  • Yang Y, Li L, Yan T, et al. Evaluation of safety and efficacy of amniotic mesenchymal stem cells for POI in animals. Reprod Sci. 2024;31(4):1159–1169. doi: 10.1007/s43032-023-01417-3.
  • Esteban MA, Wang T, Qin B, et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell. 2010;6(1):71–79. doi: 10.1016/j.stem.2009.12.001.
  • Gao Y, Han Z, Li Q, et al. Vitamin C induces a pluripotent state in mouse embryonic stem cells by modulating microRNA expression. Febs J. 2015;282(4):685–699. doi: 10.1111/febs.13173.
  • Wu H, Wu Y, Ai Z, et al. Vitamin C enhances Nanog expression via activation of the JAK/STAT signaling pathway. Stem Cells. 2014;32(1):166–176. doi: 10.1002/stem.1523.
  • Hou S, Ding C, Shen H, et al. Vitamin C improves the therapeutic potential of human amniotic epithelial cells in premature ovarian insufficiency disease. Stem Cell Res Ther. 2020;11(1):159. doi: 10.1186/s13287-020-01666-y.
  • Huang Y, Ma Z, Kuang X, et al. Sodium alginate-bioglass-encapsulated hAECs restore ovarian function in premature ovarian failure by stimulating angiogenic factor secretion. Stem Cell Res Ther. 2021;12(1):223. doi: 10.1186/s13287-021-02280-2.
  • Sanders JE, Hawley J, Levy W, et al. Pregnancies following high-dose cyclophosphamide with or without high-dose busulfan or total-body irradiation and bone marrow transplantation. Blood. 1996;87(7):3045–3052. doi: 10.1182/blood.V87.7.3045.bloodjournal8773045.
  • Hershlag A, Schuster MW. Return of fertility after autologous stem cell transplantation. Fertil Steril. 2002;77(2):419–421. doi: 10.1016/s0015-0282(01)02987-9.
  • Bao R, Xu P, Wang Y, et al. Bone marrow derived mesenchymal stem cells transplantation rescues premature ovarian insufficiency induced by chemotherapy. Gynecol Endocrinol. 2018;34(4):320–326. doi: 10.1080/09513590.2017.1393661.
  • Kang X, Chen Y, Xin X, et al. Human amniotic epithelial cells and their derived exosomes protect against cisplatin-induced acute kidney injury without compromising its antitumor activity in mice. Front Cell Dev Biol. 2021;9:752053. doi: 10.3389/fcell.2021.752053.
  • Kang NH, Yi BR, Lim SY, et al. Human amniotic membrane-derived epithelial stem cells display anticancer activity in BALB/c female nude mice bearing disseminated breast cancer xenografts. Int J Oncol. 2012;40(6):2022–2028.
  • Bolouri MR, Ghods R, Zarnani K, et al. Human amniotic epithelial cells exert anti-cancer effects through secretion of immunomodulatory small extracellular vesicles (sEV). Cancer Cell Int. 2022;22(1):329. doi: 10.1186/s12935-022-02755-z.
  • Evron A, Goldman S, Shalev E. Human amniotic epithelial cells differentiate into cells expressing germ cell specific markers when cultured in medium containing serum substitute supplement. Reprod Biol Endocrinol. 2012;10(1):108. doi: 10.1186/1477-7827-10-108.
  • Wang F, Liu XJ, Wang H, et al. [Preliminary research on the differentiation of human amniotic epithelial cells into female germ cells]. Sichuan Da Xue Xue Bao Yi Xue Ban. 2013;44(3):357–361.
  • Wang H, Wang F, Bai LP, et al. Trans-differentiation of human amniotic epithelial cells into follicle-like structure. Sichuan Da Xue Xue Bao Yi Xue Ban. 2017;48(4):531–536.
  • Peserico A, Barboni B, Russo V, et al. AEC and AFMSC transplantation preserves fertility of experimentally induced rat varicocele by expressing differential regenerative mechanisms. Int J Mol Sci. 2023;24(10):8737. doi: 10.3390/ijms24108737.
  • Guo K, Li CH, Wang XY, et al. Germ stem cells are active in postnatal mouse ovary under physiological conditions. Mol Hum Reprod. 2016;22(5):316–328. doi: 10.1093/molehr/gaw015.
  • Johnson J, Canning J, Kaneko T, et al. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428(6979):145–150. doi: 10.1038/nature02316.
  • Martin JJ, Woods DC, Tilly JL. Implications and current limitations of oogenesis from female germline or oogonial stem cells in adult mammalian ovaries. Cells. 2019;8(2):93. doi: 10.3390/cells8020093.
  • Wagner M, Yoshihara M, Douagi I, et al. Single-cell analysis of human ovarian cortex identifies distinct cell populations but no oogonial stem cells. Nat Commun. 2020;11(1):1147. doi: 10.1038/s41467-020-14936-3.
  • Un B, Cetinkaya-Un B, Akpolat M, et al. The effects of human amnion membrane-derived mesenchymal stem cells conditioned medium on ionizing radiation-induced premature ovarian failure and endoplasmic reticulum stress-related apoptosis mechanism. Eur J Obstet Gynecol Reprod Biol. 2023;288:191–197. doi: 10.1016/j.ejogrb.2023.08.001.
  • Cui L, Bao H, Liu Z, et al. hUMSCs regulate the differentiation of ovarian stromal cells via TGF-β(1)/Smad3 signaling pathway to inhibit ovarian fibrosis to repair ovarian function in POI rats. Stem Cell Res Ther. 2020;11(1):386. doi: 10.1186/s13287-020-01904-3.
  • Koike N, Sugimoto J, Okabe M, et al. Distribution of amniotic stem cells in human term amnion membrane. Microscopy (Oxf). 2022;71(1):66–76. doi: 10.1093/jmicro/dfab035.
  • Motedayyen H, Esmaeil N, Tajik N, et al. Method and key points for isolation of human amniotic epithelial cells with high yield, viability and purity. BMC Res Notes. 2017;10(1):552. doi: 10.1186/s13104-017-2880-6.
  • Zhu D, Krause M, Yawno T, et al. Assessing the impact of gestational age of donors on the efficacy of amniotic epithelial cell-derived extracellular vesicles in experimental bronchopulmonary dysplasia. Stem Cell Res Ther. 2022;13(1):196. doi: 10.1186/s13287-022-02874-4.
  • Tian YB, Wang NX, Xu Y, et al. Hyaluronic acid ameliorates the proliferative ability of human amniotic epithelial cells through activation of TGF-β/BMP signaling. PeerJ. 2020;8:e10104. doi: 10.7717/peerj.10104.
  • Wolbank S, van Griensven M, Grillari-Voglauer R, et al. Alternative sources of adult stem cells: human amniotic membrane. Adv Biochem Eng Biotechnol. 2010;123:1–27. doi: 10.1007/10_2010_71.
  • Zhou K, Koike C, Yoshida T, et al. Establishment and characterization of immortalized human amniotic epithelial cells. Cell Reprogram. 2013;15(1):55–67. doi: 10.1089/cell.2012.0021.