Mesenchymal stem cells for restoration of ovarian function

Sook Young Yoon, Sook Young Yoon

Abstract

With the progress of regenerative medicine, mesenchymal stem cells (MSCs) have received attention as a way to restore ovarian function. It has been reported that MSCs derived from bone marrow, adipose, umbilical cord blood, menstrual blood, and amniotic fluid improved ovarian function. In light of previous studies and advances in this field, there are increased expectations regarding the utilization of MSCs to restore ovarian function. This review summarizes recent research into potential applications of MSCs in women with infertility or primary ovarian insufficiency, including cases where these conditions are induced by anticancer therapy.

Keywords: Mesenchymal stem cell; Ovarian function.

Conflict of interest statement

Conflict of interest

No potential conflict of interest relevant to this article was reported.

References

    1. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641–50.
    1. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization of cells with osteogenic potential from human marrow. Bone. 1992;13:81–8.
    1. Nakahara H, Bruder SP, Goldberg VM, Caplan AI. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop Relat Res. 1990:223–32.
    1. Samsonraj RM, Raghunath M, Nurcombe V, Hui JH, van Wijnen AJ, Cool SM. Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Transl Med. 2017;6:2173–85.
    1. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells: the International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.
    1. Weiss ML, Troyer DL. Stem cells in the umbilical cord. Stem Cell Rev. 2006;2:155–62.
    1. Yi T, Song SU. Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications. Arch Pharm Res. 2012;35:213–21.
    1. Wei X, Yang X, Han ZP, Qu FF, Shao L, Shi YF. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol Sin. 2013;34:747–54.
    1. Caplan AI. Mesenchymal stem cells: time to change the name! Stem Cells Transl Med. 2017;6:1445–51.
    1. Cosgrove CM, Salani R. Ovarian effects of radiation and cytotoxic chemotherapy damage. Best Pract Res Clin Obstet Gynaecol. 2019;55:37–48.
    1. Nelson LM. Clinical practice: primary ovarian insufficiency. N Engl J Med. 2009;360:606–14.
    1. Sukur YE, Kivancli IB, Ozmen B. Ovarian aging and premature ovarian failure. J Turk Ger Gynecol Assoc. 2014;15:190–6.
    1. Ben-Aharon I, Shalgi R. What lies behind chemotherapy-induced ovarian toxicity? Reproduction. 2012;144:153–63.
    1. Yuksel A, Bildik G, Senbabaoglu F, Akin N, Arvas M, Unal F, et al. The magnitude of gonadotoxicity of chemotherapy drugs on ovarian follicles and granulosa cells varies depending upon the category of the drugs and the type of granulosa cells. Hum Reprod. 2015;30:2926–35.
    1. Zheng W, Nagaraju G, Liu Z, Liu K. Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary. Mol Cell Endocrinol. 2012;356:24–30.
    1. Bertoldo MJ, Walters KA, Ledger WL, Gilchrist RB, Mermillod P, Locatelli Y. In-vitro regulation of primordial follicle activation: challenges for fertility preservation strategies. Reprod Biomed Online. 2018;36:491–9.
    1. Chang EM, Lim E, Yoon S, Jeong K, Bae S, Lee DR, et al. Cisplatin induces overactivation of the dormant primordial follicle through PTEN/AKT/FOXO3a pathway which leads to loss of ovarian reserve in mice. PLoS One. 2015;10:e0144245.
    1. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science. 2008;319:611–3.
    1. Fazeli Z, Abedindo A, Omrani MD, Ghaderian SMH. Mesenchymal stem cells (MSCs) therapy for recovery of fertility: a systematic review. Stem Cell Rev. 2018;14:1–12.
    1. Gabr H, Elkheir WA, El-Gazzar A. Autologous stem cell transplantation in patients with idiopathic premature ovarian failure. J Tissue Sci Eng. 2016;7(3 Suppl):27.
    1. Edessy M, Hosni HN, Shady Y, Waf Y, Bakr S, Kamel M. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Med Int. 2016;3:19–23.
    1. Ding C, Zou Q, Wang F, Wu H, Chen R, Lv J, et al. Human amniotic mesenchymal stem cells improve ovarian function in natural aging through secreting hepatocyte growth factor and epidermal growth factor. Stem Cell Res Ther. 2018;9:55.
    1. Grady ST, Watts AE, Thompson JA, Penedo MC, Konganti K, Hinrichs K. Effect of intra-ovarian injection of mesenchymal stem cells in aged mares. J Assist Reprod Genet. 2018 Nov 23; doi: 10.1007/s10815-018-1371-6. [Epub].
    1. Kalhori Z, Azadbakht M, Soleimani Mehranjani M, Shariatzadeh MA. Improvement of the folliculogenesis by transplantation of bone marrow mesenchymal stromal cells in mice with induced polycystic ovary syndrome. Cytotherapy. 2018;20:1445–58.
    1. Feng P, Li P, Tan J. Human menstrual blood-derived stromal cells promote recovery of premature ovarian insufficiency via regulating the ECM-dependent FAK/AKT signaling. Stem Cell Rev. 2018 Dec 17; doi: 10.1007/s12015-018-9867-0. [Epub].
    1. Bao R, Xu P, Wang Y, Wang J, Xiao L, Li G, et al. Bone marrow derived mesenchymal stem cells transplantation rescues premature ovarian insufficiency induced by chemotherapy. Gynecol Endocrinol. 2018;34:320–6.
    1. Ling L, Feng X, Wei T, Wang Y, Wang Y, Zhang W, 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;8:283.
    1. Mohamed SA, Shalaby SM, Abdelaziz M, Brakta S, Hill WD, Ismail N, et al. Human mesenchymal stem cells partially reverse infertility in chemotherapy-induced ovarian failure. Reprod Sci. 2018;25:51–63.
    1. 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;25:1073–82.
    1. Elfayomy AK, Almasry SM, El-Tarhouny SA, Eldomiaty MA. Human umbilical cord blood-mesenchymal stem cells transplantation renovates the ovarian surface epithelium in a rat model of premature ovarian failure: possible direct and indirect effects. Tissue Cell. 2016;48:370–82.
    1. Gabr H, Rateb MA, El Sissy MH, Ahmed Seddiek H, Ali Abdelhameed Gouda S. The effect of bone marrow-derived mesenchymal stem cells on chemotherapy induced ovarian failure in albino rats. Microsc Res Tech. 2016;79:938–47.
    1. Pan Y, Zhang L, Zhang X, Hu C, Liu R. Biological and biomechanical analysis of two types of mesenchymal stem cells for intervention in chemotherapy-induced ovarian dysfunction. Arch Gynecol Obstet. 2017;295:247–52.
    1. Song D, Zhong Y, Qian C, Zou Q, Ou J, Shi Y, et al. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamideinduced premature ovarian failure rat model. Biomed Res Int. 2016;2016:2517514.
    1. Su J, Ding L, Cheng J, Yang J, Li X, Yan G, et al. Transplantation of adipose-derived stem cells combined with collagen scaffolds restores ovarian function in a rat model of premature ovarian insufficiency. Hum Reprod. 2016;31:1075–86.
    1. 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.
    1. Fouad H, Sabry D, Elsetohy K, Fathy N. Therapeutic efficacy of amniotic membrane stem cells and adipose tissue stem cells in rats with chemically induced ovarian failure. J Adv Res. 2016;7:233–41.
    1. Kilic S, Pinarli F, Ozogul C, Tasdemir N, Naz Sarac G, Delibasi T. Protection from cyclophosphamide-induced ovarian damage with bone marrow-derived mesenchymal stem cells during puberty. Gynecol Endocrinol. 2014;30:135–40.
    1. Liu T, Huang Y, Zhang J, Qin W, Chi H, Chen J, et al. Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev. 2014;23:1548–57.
    1. Liu J, Zhang H, Zhang Y, Li N, Wen Y, Cao F, et al. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells. 2014;37:865–72.
    1. Xiao GY, Liu IH, Cheng CC, Chang CC, Lee YH, Cheng WT, 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:e106538.
    1. Takehara Y, Yabuuchi A, Ezoe K, Kuroda T, Yamadera R, Sano C, et al. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab Invest. 2013;93:181–93.
    1. Wang S, Yu L, Sun M, Mu S, Wang C, Wang D, et al. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. Biomed Res Int. 2013;2013:690491.
    1. 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;4:124.
    1. Zhang Y, Xia X, Yan J, Yan L, Lu C, Zhu X, et al. Mesenchymal stem cell-derived angiogenin promotes primodial follicle survival and angiogenesis in transplanted human ovarian tissue. Reprod Biol Endocrinol. 2017;15:18.
    1. Abd-Allah SH, Shalaby SM, Pasha HF, El-Shal AS, Raafat N, Shabrawy SM, et al. Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy. 2013;15:64–75.
    1. Guo JQ, Gao X, Lin ZJ, Wu WZ, Huang LH, Dong HY, et al. BMSCs reduce rat granulosa cell apoptosis induced by cisplatin and perimenopause. BMC Cell Biol. 2013;14:18.
    1. 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;9:592–602.
    1. 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;10:353–63.
    1. Sheikhansari G, Aghebati-Maleki L, Nouri M, Jadidi-Niaragh F, Yousefi M. Current approaches for the treatment of premature ovarian failure with stem cell therapy. Biomed Pharmacother. 2018;102:254–62.
    1. De Becker A, Riet IV. Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy? World J Stem Cells. 2016;8:73–87.
    1. He Y, Chen D, Yang L, Hou Q, Ma H, Xu X. The therapeutic potential of bone marrow mesenchymal stem cells in premature ovarian failure. Stem Cell Res Ther. 2018;9:263.
    1. Gadkari R, Zhao L, Teklemariam T, Hantash BM. Human embryonic stem cell derived-mesenchymal stem cells: an alternative mesenchymal stem cell source for regenerative medicine therapy. Regen Med. 2014;9:453–65.
    1. Lian Q, Lye E, Suan Yeo K, Khia Way Tan E, Salto-Tellez M, Liu TM, et al. Derivation of clinically compliant MSCs from CD105+, CD24- differentiated human ESCs. Stem Cells. 2007;25:425–36.
    1. Trivedi P, Hematti P. Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol. 2008;36:350–9.
    1. Volarevic V, Markovic BS, Gazdic M, Volarevic A, Jovicic N, Arsenijevic N, et al. Ethical and safety issues of stem cell-based therapy. Int J Med Sci. 2018;15:36–45.
    1. de Rham C, Villard J. Potential and limitation of HLA-based banking of human pluripotent stem cells for cell therapy. J Immunol Res. 2014;2014:518135.
    1. Zhao C, Ikeya M. Generation and Applications of induced pluripotent stem cell-derived mesenchymal stem cells. Stem Cells Int. 2018;2018:9601623.
    1. Huang-Doran I, Zhang CY, Vidal-Puig A. Extracellular vesicles: novel mediators of cell communication in metabolic disease. Trends Endocrinol Metab. 2017;28:3–18.
    1. Willis GR, Kourembanas S, Mitsialis SA. Toward exosome-based therapeutics: isolation, heterogeneity, and fit-for-purpose potency. Front Cardiovasc Med. 2017;4:63.
    1. Huang B, Lu J, Ding C, Zou Q, Wang W, Li H. Exosomes derived from human adipose mesenchymal stem cells improve ovary function of premature ovarian insufficiency by targeting SMAD. Stem Cell Res Ther. 2018;9:216.
    1. Sun L, Li D, Song K, Wei J, Yao S, Li Z, et al. Exosomes derived from human umbilical cord mesenchymal stem cells protect against cisplatin-induced ovarian granulosa cell stress and apoptosis in vitro. Sci Rep. 2017;7:2552.
    1. Doeppner TR, Bahr M, Hermann DM, Giebel B. Concise review: extracellular vesicles overcoming limitations of cell therapies in ischemic stroke. Stem Cells Transl Med. 2017;6:2044–52.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe