Abstract
Premature ovarian failure (POF) is characterized by amenorrhea, hypergonadotropism and hypoestrogenism before the age of 40, which affects 1% of women in the general population. POF is complex and heterogeneous due to its pathogenetic mechanisms. It is one of the significant causes of female infertility. Although many treatments are available for POF, these therapies are less efficient and trigger many side effects. Therefore, to find effective therapeutics for POF is urgently required. Due to stem cells having self-renewal and regeneration potential, they may be effective for the treatment of ovarian failure and consequently infertility. Recent studies have found that stem cells therapy may be able to restore the ovarian structure and function in animal models of POF and provide an effective treatment method. The present review summarizes the biological roles and the possible signaling mechanisms of the different stem cells in POF ovary. Further study on the precise mechanisms of stem cells on POF may provide novel insights into the female reproduction, which not only enhances the understanding of the physiological roles but also supports effective therapy for recovering ovarian functions against infertility.
Keywords: Premature ovarian failure, stem cells, ovary, gonadotropin, amenorrhea, hypergonadotropism, hypoestrogenism.
[1]
Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol 1986; 67(4): 604-6.
[PMID: 3960433]
[PMID: 3960433]
[2]
Colao E, Granata T, Vismara MF, et al. A case of premature ovarian failure in a 33-year-old woman. Case Rep Genet 2013; 2013 573841
[http://dx.doi.org/10.1155/2013/573841] [PMID: 23509644]
[http://dx.doi.org/10.1155/2013/573841] [PMID: 23509644]
[3]
Laml T, Preyer O, Umek W, Hengstschlager M, Hanzal H. Genetic disorders in premature ovarian failure. Hum Reprod Update 2002; 8(5): 483-91.
[http://dx.doi.org/10.1093/humupd/8.5.483] [PMID: 12398227]
[http://dx.doi.org/10.1093/humupd/8.5.483] [PMID: 12398227]
[4]
Goswami D, Conway GS. Premature ovarian failure. Hum Reprod Update 2005; 11(4): 391-410.
[http://dx.doi.org/10.1093/humupd/dmi012] [PMID: 15919682]
[http://dx.doi.org/10.1093/humupd/dmi012] [PMID: 15919682]
[5]
Zhu L, Li J, Xing N, Han D, Kuang H, Ge P. American ginseng regulates gene expression to protect against premature ovarian failure in rats. BioMed Res Int 2015; 2015 767124
[http://dx.doi.org/10.1155/2015/767124] [PMID: 25705687]
[http://dx.doi.org/10.1155/2015/767124] [PMID: 25705687]
[6]
Welt CK. Primary ovarian insufficiency: a more accurate term for premature ovarian failure. Clin Endocrinol (Oxf) 2008; 68(4): 499-509.
[http://dx.doi.org/10.1111/j.1365-2265.2007.03073.x] [PMID: 17970776]
[http://dx.doi.org/10.1111/j.1365-2265.2007.03073.x] [PMID: 17970776]
[7]
Rebar RW. Premature ovarian failure. Obstet Gynecol 2009; 113(6): 1355-63.
[http://dx.doi.org/10.1097/AOG.0b013e3181a66843] [PMID: 19461434]
[http://dx.doi.org/10.1097/AOG.0b013e3181a66843] [PMID: 19461434]
[8]
Roberts H, Hickey M. Managing the menopause: An update. Maturitas 2016; 86: 53-8.
[http://dx.doi.org/10.1016/j.maturitas.2016.01.007] [PMID: 26921929]
[http://dx.doi.org/10.1016/j.maturitas.2016.01.007] [PMID: 26921929]
[9]
Wang C, Chen M, Fu F, Huang M. Gonadotropin-Releasing Hormone Analog Cotreatment for the Preservation of Ovarian Function during Gonadotoxic Chemotherapy for Breast Cancer: A Meta-Analysis. PLoS One 2013; 8(6) e66360
[http://dx.doi.org/10.1371/journal.pone.0066360] [PMID: 23805216]
[http://dx.doi.org/10.1371/journal.pone.0066360] [PMID: 23805216]
[10]
Badawy A, Elnashar A, El-Ashry M, Shahat M. Gonadotropin-releasing hormone agonists for prevention of chemotherapy-induced ovarian damage: prospective randomized study. Fertil Steril 2009; 91(3): 694-7.
[http://dx.doi.org/10.1016/j.fertnstert.2007.12.044] [PMID: 18675959]
[http://dx.doi.org/10.1016/j.fertnstert.2007.12.044] [PMID: 18675959]
[11]
Bidet M, Bachelot A, Touraine P. Premature ovarian failure: predictability of intermittent ovarian function and response to ovulation induction agents. Curr Opin Obstet Gynecol 2008; 20(4): 416-20.
[http://dx.doi.org/10.1097/GCO.0b013e328306a06b] [PMID: 18660695]
[http://dx.doi.org/10.1097/GCO.0b013e328306a06b] [PMID: 18660695]
[12]
Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004; 428(6979): 145-50.
[http://dx.doi.org/10.1038/nature02316] [PMID: 15014492]
[http://dx.doi.org/10.1038/nature02316] [PMID: 15014492]
[13]
Johnson J, Bagley J, Skaznik-Wikiel M, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 2005; 122(2): 303-15.
[http://dx.doi.org/10.1016/j.cell.2005.06.031] [PMID: 16051153]
[http://dx.doi.org/10.1016/j.cell.2005.06.031] [PMID: 16051153]
[14]
Kolios G, Moodley Y. Introduction to stem cells and regenerative medicine. Respiration 2013; 85(1): 3-10.
[http://dx.doi.org/10.1159/000345615] [PMID: 23257690]
[http://dx.doi.org/10.1159/000345615] [PMID: 23257690]
[15]
Muscari C, Bonafè F, Martin-Suarez S, et al. Restored perfusion and reduced inflammation in the infarcted heart after grafting stem cells with a hyaluronan-based scaffold. J Cell Mol Med 2013; 17(4): 518-30.
[http://dx.doi.org/10.1111/jcmm.12039] [PMID: 23480821]
[http://dx.doi.org/10.1111/jcmm.12039] [PMID: 23480821]
[16]
Liu T, Huang Y, Guo L, Cheng W, Zou G. CD44+/CD105+ human amniotic fluid mesenchymal stem cells survive and proliferate in the ovary long-term in a mouse model of chemotherapy-induced premature ovarian failure. Int J Med Sci 2012; 9(7): 592-602.
[http://dx.doi.org/10.7150/ijms.4841] [PMID: 23028242]
[http://dx.doi.org/10.7150/ijms.4841] [PMID: 23028242]
[17]
Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7(2): 211-28.
[http://dx.doi.org/10.1089/107632701300062859] [PMID: 11304456]
[http://dx.doi.org/10.1089/107632701300062859] [PMID: 11304456]
[18]
Varma MJ, Breuls RG, Schouten TE, et al. Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 2007; 16(1): 91-104.
[http://dx.doi.org/10.1089/scd.2006.0026] [PMID: 17348807]
[http://dx.doi.org/10.1089/scd.2006.0026] [PMID: 17348807]
[19]
Lee RH, Kim B, Choi I, et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 2004; 14(4-6): 311-24.
[http://dx.doi.org/10.1159/000080341] [PMID: 15319535]
[http://dx.doi.org/10.1159/000080341] [PMID: 15319535]
[20]
Sun M, Wang S, Li Y, et al. Adipose-derived stem cells improved mouse ovary function after chemotherapy-induced ovary failure. Stem Cell Res Ther 2013; 4(4): 80.
[http://dx.doi.org/10.1186/scrt231] [PMID: 23838374]
[http://dx.doi.org/10.1186/scrt231] [PMID: 23838374]
[21]
Prusa AR, Marton E, Rosner M, Bernaschek G, Hengstschläger M. Oct-4-expressing cells in human amniotic fluid: a new source for stem cell research? Hum Reprod 2003; 18(7): 1489-93.
[http://dx.doi.org/10.1093/humrep/deg279] [PMID: 12832377]
[http://dx.doi.org/10.1093/humrep/deg279] [PMID: 12832377]
[22]
Kaviani A, Perry TE, Dzakovic A, Jennings RW, Ziegler MM, Fauza DO. The amniotic fluid as a source of cells for fetal tissue engineering. J Pediatr Surg 2001; 36(11): 1662-5.
[http://dx.doi.org/10.1053/jpsu.2001.27945] [PMID: 11685697]
[http://dx.doi.org/10.1053/jpsu.2001.27945] [PMID: 11685697]
[23]
De Coppi P, Bartsch G Jr, Siddiqui MM, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 2007; 25(1): 100-6.
[http://dx.doi.org/10.1038/nbt1274] [PMID: 17206138]
[http://dx.doi.org/10.1038/nbt1274] [PMID: 17206138]
[24]
Karlmark KR, Freilinger A, Marton E, Rosner M, Lubec G, Hengstschläger M. Activation of ectopic Oct-4 and Rex-1 promoters in human amniotic fluid cells. Int J Mol Med 2005; 16(6): 987-92.
[http://dx.doi.org/10.3892/ijmm.16.6.987] [PMID: 16273276]
[http://dx.doi.org/10.3892/ijmm.16.6.987] [PMID: 16273276]
[25]
De Coppi P, Callegari A, Chiavegato A, et al. Amniotic fluid and bone marrow derived mesenchymal stem cells can be converted to smooth muscle cells in the cryo-injured rat bladder and prevent compensatory hypertrophy of surviving smooth muscle cells. J Urol 2007; 177(1): 369-76.
[http://dx.doi.org/10.1016/j.juro.2006.09.103] [PMID: 17162093]
[http://dx.doi.org/10.1016/j.juro.2006.09.103] [PMID: 17162093]
[26]
De Gemmis P, Lapucci C, Bertelli M, et al. A real-time PCR approach to evaluate adipogenic potential of amniotic fluid-derived human mesenchymal stem cells. Stem Cells Dev 2006; 15(5): 719-28.
[http://dx.doi.org/10.1089/scd.2006.15.719] [PMID: 17105407]
[http://dx.doi.org/10.1089/scd.2006.15.719] [PMID: 17105407]
[27]
In ’t Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004; 22(7): 1338-45.
[http://dx.doi.org/10.1634/stemcells.2004-0058] [PMID: 15579651]
[http://dx.doi.org/10.1634/stemcells.2004-0058] [PMID: 15579651]
[28]
Xiao GY, Liu IH, Cheng CC, et al. Amniotic fluid stem cells prevent follicle atresia and rescue fertility of mice with premature ovarian failure induced by chemotherapy. PLoS One 2014; 9(9) e106538
[http://dx.doi.org/10.1371/journal.pone.0106538] [PMID: 25198549]
[http://dx.doi.org/10.1371/journal.pone.0106538] [PMID: 25198549]
[29]
Lai D, Wang F, Chen Y, Wang L, Wang Y, Cheng W. Human amniotic fluid stem cells have a potential to recover ovarian function in mice with chemotherapy-induced sterility. BMC Dev Biol 2013; 13: 34.
[http://dx.doi.org/10.1186/1471-213X-13-34] [PMID: 24006896]
[http://dx.doi.org/10.1186/1471-213X-13-34] [PMID: 24006896]
[30]
Yoon BS, Moon JH, Jun EK, et al. Secretory profiles and wound healing effects of human amniotic fluid-derived mesenchymal stem cells. Stem Cells Dev 2010; 19(6): 887-902.
[http://dx.doi.org/10.1089/scd.2009.0138] [PMID: 19686050]
[http://dx.doi.org/10.1089/scd.2009.0138] [PMID: 19686050]
[31]
Mirabella T, Hartinger J, Lorandi C, Gentili C, van Griensven M, Cancedda R. Proangiogenic soluble factors from amniotic fluid stem cells mediate the recruitment of endothelial progenitors in a model of ischemic fasciocutaneous flap. Stem Cells Dev 2012; 21(12): 2179-88.
[http://dx.doi.org/10.1089/scd.2011.0639] [PMID: 22225409]
[http://dx.doi.org/10.1089/scd.2011.0639] [PMID: 22225409]
[32]
Cheng FC, Tai MH, Sheu ML, et al. Enhancement of regeneration with glia cell line-derived neurotrophic factor-transduced human amniotic fluid mesenchymal stem cells after sciatic nerve crush injury. J Neurosurg 2010; 112(4): 868-79.
[http://dx.doi.org/10.3171/2009.8.JNS09850] [PMID: 19817545]
[http://dx.doi.org/10.3171/2009.8.JNS09850] [PMID: 19817545]
[33]
Liu T, Xu F, Du X, et al. Establishment and characterization of multi-drug resistant, prostate carcinoma-initiating stem-like cells from human prostate cancer cell lines 22RV1. Mol Cell Biochem 2010; 340(1-2): 265-73.
[http://dx.doi.org/10.1007/s11010-010-0426-5] [PMID: 20224986]
[http://dx.doi.org/10.1007/s11010-010-0426-5] [PMID: 20224986]
[34]
Liu T, Zou G, Gao Y, et al. High efficiency of reprogramming CD34+ cells derived from human amniotic fluid into induced pluripotent stem cells with Oct4. Stem Cells Dev 2012; 21(12): 2322-32.
[http://dx.doi.org/10.1089/scd.2011.0715] [PMID: 22264161]
[http://dx.doi.org/10.1089/scd.2011.0715] [PMID: 22264161]
[35]
Liu T, Guo L, Liu Z, Huang Y, Cheng W. Induction of dopaminergic neuronal-like cells from CD44+ human amniotic fluids that are ameliorative to behavioral recovery in a Parkinson’s disease rat model. Int J Mol Med 2011; 28(5): 745-52.
[http://dx.doi.org/10.3892/ijmm.2011.732] [PMID: 21720700]
[http://dx.doi.org/10.3892/ijmm.2011.732] [PMID: 21720700]
[36]
Zou G, Liu T, Zhang L, et al. Induction of pancreatic β-cell-like cells from CD44+/CD105+ human amniotic fluids via epigenetic regulation of the pancreatic and duodenal homeobox factor 1 promoter. DNA Cell Biol 2011; 30(9): 739-48.
[http://dx.doi.org/10.1089/dna.2010.1144] [PMID: 21612404]
[http://dx.doi.org/10.1089/dna.2010.1144] [PMID: 21612404]
[37]
Xiao GY, Cheng CC, Chiang YS, Cheng WT, Liu IH, Wu SC. Exosomal miR-10a derived from amniotic fluid stem cells preserves ovarian follicles after chemotherapy. Sci Rep 2016; 6: 23120.
[http://dx.doi.org/10.1038/srep23120] [PMID: 26979400]
[http://dx.doi.org/10.1038/srep23120] [PMID: 26979400]
[38]
Jiang W, Kong L, Ni Q, et al. miR-146a ameliorates liver ischemia/reperfusion injury by suppressing IRAK1 and TRAF6. PLoS One 2014; 9(7) e101530
[http://dx.doi.org/10.1371/journal.pone.0101530] [PMID: 24987958]
[http://dx.doi.org/10.1371/journal.pone.0101530] [PMID: 24987958]
[39]
Ibrahim AG, Cheng K, Marbán E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports 2014; 2(5): 606-19.
[http://dx.doi.org/10.1016/j.stemcr.2014.04.006] [PMID: 24936449]
[http://dx.doi.org/10.1016/j.stemcr.2014.04.006] [PMID: 24936449]
[40]
Assou S, Al-edani T, Haouzi D, et al. MicroRNAs: new candidates for the regulation of the human cumulus-oocyte complex. Hum Reprod 2013; 28(11): 3038-49.
[http://dx.doi.org/10.1093/humrep/det321] [PMID: 23904466]
[http://dx.doi.org/10.1093/humrep/det321] [PMID: 23904466]
[41]
Whittle WL, Gibb W, Challis JR. The characterization of human amnion epithelial and mesenchymal cells: the cellular expression, activity and glucocorticoid regulation of prostaglandin output. Placenta 2000; 21(4): 394-401.
[http://dx.doi.org/10.1053/plac.1999.0482] [PMID: 10833375]
[http://dx.doi.org/10.1053/plac.1999.0482] [PMID: 10833375]
[42]
Vosdoganes P, Lim R, Koulaeva E, et al. Human amnion epithelial cells modulate hyperoxia-induced neonatal lung injury in mice. Cytotherapy 2013; 15(8): 1021-9.
[http://dx.doi.org/10.1016/j.jcyt.2013.03.004] [PMID: 23643416]
[http://dx.doi.org/10.1016/j.jcyt.2013.03.004] [PMID: 23643416]
[43]
Vosdoganes P, Wallace EM, Chan ST, Acharya R, Moss TJ, Lim R. Human amnion epithelial cells repair established lung injury. Cell Transplant 2013; 22(8): 1337-49.
[http://dx.doi.org/10.3727/096368912X657657] [PMID: 23044339]
[http://dx.doi.org/10.3727/096368912X657657] [PMID: 23044339]
[44]
He F, Zhou A, Feng S. Use of human amniotic epithelial cells in mouse models of bleomycin-induced lung fibrosis: A systematic review and meta-analysis. PLoS One 2018; 13(5) e0197658
[http://dx.doi.org/10.1371/journal.pone.0197658] [PMID: 29772024]
[http://dx.doi.org/10.1371/journal.pone.0197658] [PMID: 29772024]
[45]
Murphy S, Lim R, Dickinson H, et al. Human amnion epithelial cells prevent bleomycin-induced lung injury and preserve lung function. Cell Transplant 2011; 20(6): 909-23.
[http://dx.doi.org/10.3727/096368910X543385] [PMID: 21092408]
[http://dx.doi.org/10.3727/096368910X543385] [PMID: 21092408]
[46]
Wu ZY, Hui GZ, Lu Y, Wu X, Guo LH. Transplantation of human amniotic epithelial cells improves hindlimb function in rats with spinal cord injury. Chin Med J (Engl) 2006; 119(24): 2101-7.
[http://dx.doi.org/10.1097/00029330-200612020-00013] [PMID: 17199962]
[http://dx.doi.org/10.1097/00029330-200612020-00013] [PMID: 17199962]
[47]
Lin JS, Zhou L, Sagayaraj A, et al. Hepatic differentiation of human amniotic epithelial cells and in vivo therapeutic effect on animal model of cirrhosis. J Gastroenterol Hepatol 2015; 30(11): 1673-82.
[http://dx.doi.org/10.1111/jgh.12991] [PMID: 25973537]
[http://dx.doi.org/10.1111/jgh.12991] [PMID: 25973537]
[48]
Wu Z, Hui G, Lu Y, Liu T, Huang Q, Guo L. Human amniotic epithelial cells express specific markers of nerve cells and migrate along the nerve fibers in the corpus callosum. Neural Regen Res 2012; 7(1): 41-5.
[PMID: 25806057]
[PMID: 25806057]
[49]
Fang CH, Jin J, Joe JH, et al. In vivo differentiation of human amniotic epithelial cells into cardiomyocyte-like cells and cell transplantation effect on myocardial infarction in rats: comparison with cord blood and adipose tissue-derived mesenchymal stem cells. Cell Transplant 2012; 21(8): 1687-96.
[http://dx.doi.org/10.3727/096368912X653039] [PMID: 22776022]
[http://dx.doi.org/10.3727/096368912X653039] [PMID: 22776022]
[50]
Miki T, Lehmann T, Cai H, Stolz DB, Strom SC. Stem cell characteristics of amniotic epithelial cells. Stem Cells 2005; 23(10): 1549-59.
[http://dx.doi.org/10.1634/stemcells.2004-0357] [PMID: 16081662]
[http://dx.doi.org/10.1634/stemcells.2004-0357] [PMID: 16081662]
[51]
Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 2007; 77(3): 577-88.
[http://dx.doi.org/10.1095/biolreprod.106.055244] [PMID: 17494917]
[http://dx.doi.org/10.1095/biolreprod.106.055244] [PMID: 17494917]
[52]
Wang F, Wang L, Yao X, Lai D, Guo L. 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.
[http://dx.doi.org/10.1186/scrt335] [PMID: 24406076]
[http://dx.doi.org/10.1186/scrt335] [PMID: 24406076]
[53]
Koizumi NJ, Inatomi TJ, Sotozono CJ, Fullwood NJ, Quantock AJ, Kinoshita S. Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res 2000; 20(3): 173-7.
[http://dx.doi.org/10.1076/0271-3683(200003)2031-9FT173] [PMID: 10694891]
[http://dx.doi.org/10.1076/0271-3683(200003)2031-9FT173] [PMID: 10694891]
[54]
Zhang Q, Xu M, Yao X, Li T, Wang Q, Lai D. Human amniotic epithelial cells inhibit granulosa cell apoptosis induced by chemotherapy and restore the fertility. Stem Cell Res Ther 2015; 6: 152.
[http://dx.doi.org/10.1186/s13287-015-0148-4] [PMID: 26303743]
[http://dx.doi.org/10.1186/s13287-015-0148-4] [PMID: 26303743]
[55]
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; 8(1): 270.
[http://dx.doi.org/10.1186/s13287-017-0721-0] [PMID: 29179771]
[http://dx.doi.org/10.1186/s13287-017-0721-0] [PMID: 29179771]
[56]
Lee HJ, Selesniemi K, Niikura Y, et al. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J Clin Oncol 2007; 25(22): 3198-204.
[http://dx.doi.org/10.1200/JCO.2006.10.3028] [PMID: 17664466]
[http://dx.doi.org/10.1200/JCO.2006.10.3028] [PMID: 17664466]
[57]
Fu X, He Y, Xie C, Liu W. Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage. Cytotherapy 2008; 10(4): 353-63.
[http://dx.doi.org/10.1080/14653240802035926] [PMID: 18574768]
[http://dx.doi.org/10.1080/14653240802035926] [PMID: 18574768]
[58]
Badawy A, Sobh MA, Ahdy M, Abdelhafez MS. Bone marrow mesenchymal stem cell repair of cyclophosphamide-induced ovarian insufficiency in a mouse model. Int J Womens Health 2017; 9: 441-7.
[http://dx.doi.org/10.2147/IJWH.S134074] [PMID: 28670143]
[http://dx.doi.org/10.2147/IJWH.S134074] [PMID: 28670143]
[59]
Liu J, Zhang H, Zhang Y, et al. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells 2014; 37(12): 865-72.
[http://dx.doi.org/10.14348/molcells.2014.0145] [PMID: 25410907]
[http://dx.doi.org/10.14348/molcells.2014.0145] [PMID: 25410907]
[60]
Kupcova Skalnikova H. Proteomic techniques for characterisation of mesenchymal stem cell secretome. Biochimie 2013; 95(12): 2196-211.
[http://dx.doi.org/10.1016/j.biochi.2013.07.015] [PMID: 23880644]
[http://dx.doi.org/10.1016/j.biochi.2013.07.015] [PMID: 23880644]
[61]
Janga SC, Vallabhaneni S. MicroRNAs as post-transcriptional machines and their interplay with cellular networks. Adv Exp Med Biol 2011; 722: 59-74.
[http://dx.doi.org/10.1007/978-1-4614-0332-6_4] [PMID: 21915782]
[http://dx.doi.org/10.1007/978-1-4614-0332-6_4] [PMID: 21915782]
[62]
Chan JK, Blansit K, Kiet T, et al. The inhibition of miR-21 promotes apoptosis and chemosensitivity in ovarian cancer. Gynecol Oncol 2014; 132(3): 739-44.
[http://dx.doi.org/10.1016/j.ygyno.2014.01.034] [PMID: 24472409]
[http://dx.doi.org/10.1016/j.ygyno.2014.01.034] [PMID: 24472409]
[63]
Shang C, Guo Y, Hong Y, Liu YH, Xue YX. MiR-21 up-regulation mediates glioblastoma cancer stem cells apoptosis and proliferation by targeting FASLG. Mol Biol Rep 2015; 42(3): 721-7.
[http://dx.doi.org/10.1007/s11033-014-3820-3] [PMID: 25394756]
[http://dx.doi.org/10.1007/s11033-014-3820-3] [PMID: 25394756]
[64]
Pennelli G, Galuppini F, Barollo S, et al. The PDCD4/miR-21 pathway in medullary thyroid carcinoma. Hum Pathol 2015; 46(1): 50-7.
[http://dx.doi.org/10.1016/j.humpath.2014.09.006] [PMID: 25316501]
[http://dx.doi.org/10.1016/j.humpath.2014.09.006] [PMID: 25316501]
[65]
Carletti MZ, Fiedler SD, Christenson LK. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol Reprod 2010; 83(2): 286-95.
[http://dx.doi.org/10.1095/biolreprod.109.081448] [PMID: 20357270]
[http://dx.doi.org/10.1095/biolreprod.109.081448] [PMID: 20357270]
[66]
Fu X, He Y, Wang X, et al. Overexpression of miR-21 in stem cells improves ovarian structure and function in rats with chemotherapy-induced ovarian damage by targeting PDCD4 and PTEN to inhibit granulosa cell apoptosis. Stem Cell Res Ther 2017; 8(1): 187.
[http://dx.doi.org/10.1186/s13287-017-0641-z] [PMID: 28807003]
[http://dx.doi.org/10.1186/s13287-017-0641-z] [PMID: 28807003]
[67]
Díaz-Prado S, Muiños-López E, Hermida-Gómez T, et al. Multilineage differentiation potential of cells isolated from the human amniotic membrane. J Cell Biochem 2010; 111(4): 846-57.
[http://dx.doi.org/10.1002/jcb.22769] [PMID: 20665539]
[http://dx.doi.org/10.1002/jcb.22769] [PMID: 20665539]
[68]
Soncini M, Vertua E, Gibelli L, et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007; 1(4): 296-305.
[http://dx.doi.org/10.1002/term.40] [PMID: 18038420]
[http://dx.doi.org/10.1002/term.40] [PMID: 18038420]
[69]
Parolini O, Alviano F, Bagnara GP, et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells 2008; 26(2): 300-11.
[http://dx.doi.org/10.1634/stemcells.2007-0594] [PMID: 17975221]
[http://dx.doi.org/10.1634/stemcells.2007-0594] [PMID: 17975221]
[70]
Malek A, Bersinger NA. Human placental stem cells: biomedical potential and clinical relevance. J Stem Cells 2011; 6(2): 75-92.
[PMID: 22997848]
[PMID: 22997848]
[71]
Ling L, Feng X, Wei T, et al. Effects of low-intensity pulsed ultrasound (LIPUS)-pretreated human amnion-derived mesenchymal stem cell (hAD-MSC) transplantation on primary ovarian insufficiency in rats. Stem Cell Res Ther 2017; 8(1): 283.
[http://dx.doi.org/10.1186/s13287-017-0739-3] [PMID: 29258619]
[http://dx.doi.org/10.1186/s13287-017-0739-3] [PMID: 29258619]
[72]
Wang J, Wang CD, Zhang N, et al. Mechanical stimulation orchestrates the osteogenic differentiation of human bone marrow stromal cells by regulating HDAC1. Cell Death Dis 2016; 7e2221
[http://dx.doi.org/10.1038/cddis.2016.112] [PMID: 27171263]
[http://dx.doi.org/10.1038/cddis.2016.112] [PMID: 27171263]
[73]
Harrison A, Lin S, Pounder N, Mikuni-Takagaki Y. Mode & mechanism of low intensity pulsed ultrasound (LIPUS) in fracture repair. Ultrasonics 2016; 70: 45-52.
[http://dx.doi.org/10.1016/j.ultras.2016.03.016] [PMID: 27130989]
[http://dx.doi.org/10.1016/j.ultras.2016.03.016] [PMID: 27130989]
[74]
Sena K, Angle SR, Kanaji A, et al. Low-intensity pulsed ultrasound (LIPUS) and cell-to-cell communication in bone marrow stromal cells. Ultrasonics 2011; 51(5): 639-44.
[http://dx.doi.org/10.1016/j.ultras.2011.01.007] [PMID: 21333315]
[http://dx.doi.org/10.1016/j.ultras.2011.01.007] [PMID: 21333315]
[75]
Coords M, Breitbart E, Paglia D, et al. The effects of low-intensity pulsed ultrasound upon diabetic fracture healing. J Orthop Res 2011; 29(2): 181-8.
[http://dx.doi.org/10.1002/jor.21223] [PMID: 20886648]
[http://dx.doi.org/10.1002/jor.21223] [PMID: 20886648]
[76]
Babitha V, Yadav VP, Chouhan VS, et al. Luteinizing hormone, insulin like growth factor-1, and epidermal growth factor stimulate vascular endothelial growth factor production in cultured bubaline granulosa cells. Gen Comp Endocrinol 2014; 198: 1-12.
[http://dx.doi.org/10.1016/j.ygcen.2013.12.004] [PMID: 24361167]
[http://dx.doi.org/10.1016/j.ygcen.2013.12.004] [PMID: 24361167]
[77]
Mao J, Smith MF, Rucker EB, et al. Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro. J Anim Sci 2004; 82(7): 1967-75.
[http://dx.doi.org/10.2527/2004.8271967x] [PMID: 15309943]
[http://dx.doi.org/10.2527/2004.8271967x] [PMID: 15309943]
[78]
Uzumcu M, Pan Z, Chu Y, Kuhn PE, Zachow R. Immunolocalization of the hepatocyte growth factor (HGF) system in the rat ovary and the anti-apoptotic effect of HGF in rat ovarian granulosa cells in vitro. Reproduction 2006; 132(2): 291-9.
[http://dx.doi.org/10.1530/rep.1.00989] [PMID: 16885537]
[http://dx.doi.org/10.1530/rep.1.00989] [PMID: 16885537]
[79]
Kestendjieva S, Kyurkchiev D, Tsvetkova G, et al. Characterization of mesenchymal stem cells isolated from the human umbilical cord. Cell Biol Int 2008; 32(7): 724-32.
[http://dx.doi.org/10.1016/j.cellbi.2008.02.002] [PMID: 18396423]
[http://dx.doi.org/10.1016/j.cellbi.2008.02.002] [PMID: 18396423]
[80]
Karahuseyinoglu S, Cinar O, Kilic E, et al. Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cells 2007; 25(2): 319-31.
[http://dx.doi.org/10.1634/stemcells.2006-0286] [PMID: 17053211]
[http://dx.doi.org/10.1634/stemcells.2006-0286] [PMID: 17053211]
[81]
Bieback K, Brinkmann I. Mesenchymal stromal cells from human perinatal tissues: From biology to cell therapy. World J Stem Cells 2010; 2(4): 81-92.
[http://dx.doi.org/10.4252/wjsc.v2.i4.81] [PMID: 21607124]
[http://dx.doi.org/10.4252/wjsc.v2.i4.81] [PMID: 21607124]
[82]
Liu Y, Mu R, Wang S, et al. Therapeutic potential of human umbilical cord mesenchymal stem cells in the treatment of rheumatoid arthritis. Arthritis Res Ther 2010; 12(6): R210.
[http://dx.doi.org/10.1186/ar3187] [PMID: 21080925]
[http://dx.doi.org/10.1186/ar3187] [PMID: 21080925]
[83]
Song D, Zhong Y, Qian C, et al. Human Umbilical Cord Mesenchymal Stem Cells Therapy in Cyclophosphamide-Induced Premature Ovarian Failure Rat Model. BioMed Res Int 2016. 20162517514
[http://dx.doi.org/10.1155/2016/2517514] [PMID: 27047962]
[http://dx.doi.org/10.1155/2016/2517514] [PMID: 27047962]
[84]
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): 1554-65.
[http://dx.doi.org/10.1007/s11427-017-9272-2] [PMID: 29546669]
[http://dx.doi.org/10.1007/s11427-017-9272-2] [PMID: 29546669]
[85]
Wang S, Yu L, Sun M, et al. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. BioMed Res Int 2013. 2013690491
[http://dx.doi.org/10.1155/2013/690491] [PMID: 23998127]
[http://dx.doi.org/10.1155/2013/690491] [PMID: 23998127]
[86]
Abd-Allah SH, Shalaby SM, Pasha HF, et al. Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy 2013; 15(1): 64-75.
[http://dx.doi.org/10.1016/j.jcyt.2012.08.001] [PMID: 23260087]
[http://dx.doi.org/10.1016/j.jcyt.2012.08.001] [PMID: 23260087]
[87]
Chen CP. Placental villous mesenchymal cells trigger trophoblast invasion. Cell Adhes Migr 2014; 8(2): 94-7.
[http://dx.doi.org/10.4161/cam.28347] [PMID: 24622731]
[http://dx.doi.org/10.4161/cam.28347] [PMID: 24622731]
[88]
Luan X, Li G, Wang G, Wang F, Lin Y. Human placenta-derived mesenchymal stem cells suppress T cell proliferation and support the culture expansion of cord blood CD34+ cells: a comparison with human bone marrow-derived mesenchymal stem cells. Tissue Cell 2013; 45(1): 32-8.
[http://dx.doi.org/10.1016/j.tice.2012.09.002] [PMID: 23107983]
[http://dx.doi.org/10.1016/j.tice.2012.09.002] [PMID: 23107983]
[89]
Yin N, Zhao W, Luo Q, Yuan W, Luan X, Zhang H. Restoring Ovarian Function With Human Placenta-Derived Mesenchymal Stem Cells in Autoimmune-Induced Premature Ovarian Failure Mice Mediated by Treg Cells and Associated Cytokines. Reprod Sci 2018; 25(7): 1073-82.
[http://dx.doi.org/10.1177/1933719117732156] [PMID: 28954601]
[http://dx.doi.org/10.1177/1933719117732156] [PMID: 28954601]
[90]
Zhang H, Luo Q, Lu X, et al. Effects of hPMSCs on granulosa cell apoptosis and AMH expression and their role in the restoration of ovary function in premature ovarian failure mice. Stem Cell Res Ther 2018; 9(1): 20.
[http://dx.doi.org/10.1186/s13287-017-0745-5] [PMID: 29386068]
[http://dx.doi.org/10.1186/s13287-017-0745-5] [PMID: 29386068]
[91]
Yin N, Wang Y, Lu X, et al. hPMSC transplantation restoring ovarian function in premature ovarian failure mice is associated with change of Th17/Tc17 and Th17/Treg cell ratios through the PI3K/Akt signal pathway. Stem Cell Res Ther 2018; 9(1): 37.
[http://dx.doi.org/10.1186/s13287-018-0772-x] [PMID: 29444704]
[http://dx.doi.org/10.1186/s13287-018-0772-x] [PMID: 29444704]
[92]
Meng X, Ichim TE, Zhong J, et al. Endometrial regenerative cells: a novel stem cell population. J Transl Med 2007; 5: 57.
[http://dx.doi.org/10.1186/1479-5876-5-57] [PMID: 18005405]
[http://dx.doi.org/10.1186/1479-5876-5-57] [PMID: 18005405]
[93]
Patel AN, Park E, Kuzman M, Benetti F, Silva FJ, Allickson JG. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant 2008; 17(3): 303-11.
[http://dx.doi.org/10.3727/096368908784153922] [PMID: 18522233]
[http://dx.doi.org/10.3727/096368908784153922] [PMID: 18522233]
[94]
Wu X, Luo Y, Chen J, et al. Transplantation of human menstrual blood progenitor cells improves hyperglycemia by promoting endogenous progenitor differentiation in type 1 diabetic mice. Stem Cells Dev 2014; 23(11): 1245-57.
[http://dx.doi.org/10.1089/scd.2013.0390] [PMID: 24499421]
[http://dx.doi.org/10.1089/scd.2013.0390] [PMID: 24499421]
[95]
Akyash F, Aflatoonian A, Rezazadeh Valojerdi M, Sadeghian Nodoushan F, Aflatoonian R, Aflatoonian B. In Vitro Isolation, Culture and Identification of Human Endometrial Mesenchymal Stem/Stromal Cells (EnMSCs). Cell J 2015; 17(Suppl. 1): 21-2.
[96]
Akyash F, Sadeghian-Nodoushan F, Aflatoonian B. Isolation, Culture and Characterization of Human Endometrial Mesenchymal Stem/Stromal Cells (EnMSCs): A Mini Review. Austin J In Vitro Fertili 2016; 3(1): 1025.
[97]
Lai D, Wang F, Yao X, Zhang Q, Wu X, Xiang C. Human endometrial mesenchymal stem cells restore ovarian function through improving the renewal of germline stem cells in a mouse model of premature ovarian failure. J Transl Med 2015; 13: 155.
[http://dx.doi.org/10.1186/s12967-015-0516-y] [PMID: 25964118]
[http://dx.doi.org/10.1186/s12967-015-0516-y] [PMID: 25964118]
[98]
Wang Z, Wang Y, Yang T, Li J, Yang X. Study of the reparative effects of menstrual-derived stem cells on premature ovarian failure in mice. Stem Cell Res Ther 2017; 8(1): 11.
[http://dx.doi.org/10.1186/s13287-016-0458-1] [PMID: 28114977]
[http://dx.doi.org/10.1186/s13287-016-0458-1] [PMID: 28114977]
[99]
Lin J, Xiang D, Zhang JL, Allickson J, Xiang C. Plasticity of human menstrual blood stem cells derived from the endometrium. J Zhejiang Univ Sci B 2011; 12(5): 372-80.
[http://dx.doi.org/10.1631/jzus.B1100015] [PMID: 21528491]
[http://dx.doi.org/10.1631/jzus.B1100015] [PMID: 21528491]
[100]
Liu T, Huang Y, Zhang J, et al. Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev 2014; 23(13): 1548-57.
[http://dx.doi.org/10.1089/scd.2013.0371] [PMID: 24593672]
[http://dx.doi.org/10.1089/scd.2013.0371] [PMID: 24593672]
[101]
Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 2012; 338(6109): 971-5.
[http://dx.doi.org/10.1126/science.1226889] [PMID: 23042295]
[http://dx.doi.org/10.1126/science.1226889] [PMID: 23042295]
[102]
Hayashi K, Saitou M. Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nat Protoc 2013; 8(8): 1513-24.
[http://dx.doi.org/10.1038/nprot.2013.090] [PMID: 23845963]
[http://dx.doi.org/10.1038/nprot.2013.090] [PMID: 23845963]
[103]
Leng L, Tan Y, Gong F, et al. Differentiation of primordial germ cells from induced pluripotent stem cells of primary ovarian insufficiency. Hum Reprod 2015; 30(3): 737-48.
[http://dx.doi.org/10.1093/humrep/deu358] [PMID: 25586786]
[http://dx.doi.org/10.1093/humrep/deu358] [PMID: 25586786]
[104]
Wen Y, He W, Jiang M, Zeng M, Cai L. Deriving cells expressing markers of female germ cells from premature ovarian failure patient-specific induced pluripotent stem cells. Regen Med 2017; 12(2): 143-52.
[http://dx.doi.org/10.2217/rme-2016-0074] [PMID: 28244827]
[http://dx.doi.org/10.2217/rme-2016-0074] [PMID: 28244827]
[105]
Shi Y, Massagué J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003; 113(6): 685-700.
[http://dx.doi.org/10.1016/S0092-8674(03)00432-X] [PMID: 12809600]
[http://dx.doi.org/10.1016/S0092-8674(03)00432-X] [PMID: 12809600]
[106]
Shirazi R, Zarnani AH, Soleimani M, Abdolvahabi MA, Nayernia K, Ragerdi Kashani I. BMP4 can generate primordial germ cells from bone-marrow-derived pluripotent stem cells. Cell Biol Int 2012; 36(12): 1185-93.
[http://dx.doi.org/10.1042/CBI20110651] [PMID: 22988836]
[http://dx.doi.org/10.1042/CBI20110651] [PMID: 22988836]
[107]
Taha MF, Javeri A, Majidizadeh T, Valojerdi MR. Both BMP4 and serum have significant roles in differentiation of embryonic stem cells to primitive and definitive endoderm. Cytotechnology 2016; 68(4): 1315-24.
[http://dx.doi.org/10.1007/s10616-015-9891-8] [PMID: 26008149]
[http://dx.doi.org/10.1007/s10616-015-9891-8] [PMID: 26008149]
[108]
Le Bouffant R, Guerquin MJ, Duquenne C, et al. Meiosis initiation in the human ovary requires intrinsic retinoic acid synthesis. Hum Reprod 2010; 25(10): 2579-90.
[http://dx.doi.org/10.1093/humrep/deq195] [PMID: 20670969]
[http://dx.doi.org/10.1093/humrep/deq195] [PMID: 20670969]
[109]
Liu T, Qin W, Huang Y, Zhao Y, Wang J. Induction of estrogen-sensitive epithelial cells derived from human-induced pluripotent stem cells to repair ovarian function in a chemotherapy-induced mouse model of premature ovarian failure. DNA Cell Biol 2013; 32(12): 685-98.
[http://dx.doi.org/10.1089/dna.2013.2032] [PMID: 24032550]
[http://dx.doi.org/10.1089/dna.2013.2032] [PMID: 24032550]
[110]
Zhang X, Ladd A, Dragoescu E, Budd WT, Ware JL, Zehner ZE. MicroRNA-17-3p is a prostate tumor suppressor in vitro and in vivo, and is decreased in high grade prostate tumors analyzed by laser capture microdissection. Clin Exp Metastasis 2009; 26(8): 965-79.
[http://dx.doi.org/10.1007/s10585-009-9287-2] [PMID: 19771525]
[http://dx.doi.org/10.1007/s10585-009-9287-2] [PMID: 19771525]
[111]
Dong P, Kaneuchi M, Watari H, et al. MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Mol Cancer 2011; 10: 99.
[http://dx.doi.org/10.1186/1476-4598-10-99] [PMID: 21851624]
[http://dx.doi.org/10.1186/1476-4598-10-99] [PMID: 21851624]
[112]
Cheng CW, Wang HW, Chang CW, et al. MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res Treat 2012; 134(3): 1081-93.
[http://dx.doi.org/10.1007/s10549-012-2034-4] [PMID: 22476851]
[http://dx.doi.org/10.1007/s10549-012-2034-4] [PMID: 22476851]
Article Metrics
85
4