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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Review Article

Mesenchymal Stem Cell-based Therapy and Female Infertility: Limitations and Advances

Author(s): Ghazal Ghajari, Arefe Heydari and Masoud Ghorbani*

Volume 18, Issue 3, 2023

Published on: 19 August, 2022

Page: [322 - 338] Pages: 17

DOI: 10.2174/1574888X17666220511142930

Price: $65

Abstract

Infertility in women can be caused by various female reproductive diseases such as premature ovarian failure (POF), polycystic ovary syndrome (PCOS), endometriosis and Asherman syndrome that affect couples' quality of life and lead to mental, emotional, and physical problems. In recent years, clinical researchers have sought infertility treatments using new methods that are more effective and noninvasive than the old methods.

Today, stem cell-based therapy has been introduced as a promising method and an alternative to the old strategy of infertility treatment. Understanding the main features and functional perspective of mesenchymal stem cells (MSCs) in the future of infertility by physicians is crucial.

Mesenchymal stem cells (MSCs) are multipotent stem cells with a high proliferation range, abundant source and multidirectional differentiation potential. They have a high potential for the treatment of injured tissues in regenerative medicine through cell homing, secretion of active factors, and participation in immune regulation. At present, due to fewer ethical restrictions on the use of mesenchymal stem cells compared to embryonic stem cells, more attention has been paid to these cells as a new treatment for gynecological disorders. In this paper, we first review the various type of female reproductive disorders along with their common treatment methods, then we evaluate the recent advances in the application of MSCs in the diseases related to infertility and improve the reproductive health of women worldwide.

Keywords: pluripotent stem cell, female reproduction, assisted reproductive technologies, biotechnologies of reproduction.

Graphical Abstract

[1]
Ghaebi M, Abdolmohammadi-Vahid S, Ahmadi M, et al. T cell subsets in peripheral blood of women with recurrent implantation failure. J Reprod Immunol 2019; 131: 21-9.
[http://dx.doi.org/10.1016/j.jri.2018.11.002] [PMID: 30471511]
[2]
Ghajari G, Nabiuni M, Amini E. The association between testicular toxicity induced by Li2Co3 and protective effect of Ganoderma lucidum: Alteration of Bax & c-Kit genes expression. Tissue Cell 2021; 72: 101552.
[http://dx.doi.org/10.1016/j.tice.2021.101552] [PMID: 33992978]
[3]
Sun H, Gong T-T, Jiang Y-T, Zhang S, Zhao Y-H, Wu Q-J. Global, regional, and national prevalence and disability-adjusted life-years for infertility in 195 countries and territories, 1990-2017: results from a global burden of disease study, 2017. Aging (Albany NY) 2019; 11(23): 10952-91.
[http://dx.doi.org/10.18632/aging.102497] [PMID: 31790362]
[4]
Ramírez González, Juan Andrés, et al. Overview of the female reproductive system Exercise and Human Reproduction. 2016; pp. 19-46.
[5]
Rendi MH, Muehlenbachs A, Garcia RL, Boyd KL. Female reproductive system Comparative anatomy and histology. Elsevier 2012; pp. 253-84.
[http://dx.doi.org/10.1016/B978-0-12-381361-9.00017-2]
[6]
Richards JS, Pangas SA. The ovary: basic biology and clinical implications. J Clin Invest 2010; 120(4): 963-72.
[http://dx.doi.org/10.1172/JCI41350] [PMID: 20364094]
[7]
Jones RE, Lopez KH. Human reproductive biology. Academic Press 2013.
[8]
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.
[http://dx.doi.org/10.1016/j.biopha.2018.03.056] [PMID: 29567538]
[9]
Persani L, Rossetti R, Cacciatore C. Genes involved in human premature ovarian failure. J Mol Endocrinol 2010; 45(5): 257-79.
[http://dx.doi.org/10.1677/JME-10-0070] [PMID: 20668067]
[10]
Zhao Y, Ma J, Yi P, et al. Human umbilical cord mesenchymal stem cells restore the ovarian metabolome and rescue premature ovarian insufficiency in mice. Stem Cell Res Ther 2020; 11(1): 466.
[http://dx.doi.org/10.1186/s13287-020-01972-5] [PMID: 33148334]
[11]
Crain DA, Janssen SJ, Edwards TM, et al. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 2008; 90(4): 911-40.
[http://dx.doi.org/10.1016/j.fertnstert.2008.08.067] [PMID: 18929049]
[12]
Salazar CA, Isaacson K, Morris S. A comprehensive review of Asherman’s syndrome: causes, symptoms and treatment options. Curr Opin Obstet Gynecol 2017; 29(4): 249-56.
[http://dx.doi.org/10.1097/GCO.0000000000000378] [PMID: 28582327]
[13]
Bai X. Stem Cell-Based Disease Modeling and Cell Therapy. Multidisciplinary Digital Publishing Institute 2020; p. 2193.
[14]
Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod 2010; 16(11): 818-34.
[http://dx.doi.org/10.1093/molehr/gaq061] [PMID: 20627991]
[15]
Schwab KE, Chan RWS, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril 2005; 84 (Suppl. 2): 1124-30.
[http://dx.doi.org/10.1016/j.fertnstert.2005.02.056] [PMID: 16210003]
[16]
Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 2005; 21: 605-31.
[http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131525] [PMID: 16212509]
[17]
Park H-S, Ashour D, Elsharoud A, et al. Towards cell free therapy of premature ovarian insufficiency: human bone marrow mesenchymal stem cells secretome enhances angiogenesis in human ovarian microvascular endothelial cells HSOA J Stem Cells Res Dev Ther 2019; 5(2)
[18]
Ballini A, Boccaccio A, Saini R, Van Pham P, Tatullo M. Dental-derived stem cells and their secretome and interactions with bioscaffolds/biomaterials in regenerative medicine: From the in vitro research to translational applications. Hindawi 2017.
[19]
Rungsiwiwut R, Virutamasen P, Pruksananonda K. Mesenchymal stem cells for restoring endometrial function: An infertility perspective. Reprod Med Biol 2020; 20(1): 13-9.
[http://dx.doi.org/10.1002/rmb2.12339] [PMID: 33488279]
[20]
Maybin JA, Critchley HO. Menstrual physiology: implications for endometrial pathology and beyond. Hum Reprod Update 2015; 21(6): 748-61.
[http://dx.doi.org/10.1093/humupd/dmv038] [PMID: 26253932]
[21]
Zondervan KT, Becker CM, Missmer SA. Endometriosis. N Engl J Med 2020; 382(13): 1244-56.
[http://dx.doi.org/10.1056/NEJMra1810764] [PMID: 32212520]
[22]
Navarro R, Poder L, Sun D, Jha P. Endometriosis in pregnancy. Abdom Radiol (NY) 2020; 45(6): 1741-53.
[http://dx.doi.org/10.1007/s00261-020-02486-7] [PMID: 32206832]
[23]
Hughes E, Brown J, Collins JJ, Farquhar C, Fedorkow DM, Vanderkerchove P. Ovulation suppression for endometriosis for women with subfertility. Cochrane Database Sys Rev 2007; p. 3.
[http://dx.doi.org/10.1002/14651858.CD000155.pub2]
[24]
Ahmad G, Baker J, Finnerty J, Phillips K, Watson A. Laparoscopic entry techniques. Cochrane Database of systematic review 2019; 1.
[http://dx.doi.org/10.1002/14651858.CD006583.pub5]
[25]
Lee D, Kim SK, Lee JR, Jee BC. Management of endometriosis-related infertility: Considerations and treatment options. Clin Exp Reprod Med 2020; 47(1): 1-11.
[http://dx.doi.org/10.5653/cerm.2019.02971] [PMID: 32088944]
[26]
Benor A, Gay S, DeCherney A. An update on stem cell therapy for Asherman syndrome. J Assist Reprod Genet 2020; 37(7): 1511-29.
[http://dx.doi.org/10.1007/s10815-020-01801-x] [PMID: 32445154]
[27]
Dreisler E, Kjer JJ. Asherman’s syndrome: current perspectives on diagnosis and management. Int J Womens Health 2019; 11: 191-8.
[http://dx.doi.org/10.2147/IJWH.S165474] [PMID: 30936754]
[28]
Di Guardo F, Della Corte L, Vilos GA, et al. Evaluation and treatment of infertile women with Asherman syndrome: an updated review focusing on the role of hysteroscopy. Reprod Biomed Online 2020; 41(1): 55-61.
[http://dx.doi.org/10.1016/j.rbmo.2020.03.021] [PMID: 32444259]
[29]
Esfandyari S, Chugh RM, Park HS, Hobeika E, Ulin M, Al-Hendy A. Mesenchymal stem cells as a bio organ for treatment of female infertility. Cells 2020; 9(10): 2253.
[http://dx.doi.org/10.3390/cells9102253] [PMID: 33050021]
[30]
Tan J, Li P, Wang Q, et al. Autologous menstrual blood-derived stromal cells transplantation for severe Asherman’s syndrome. Hum Reprod 2016; 31(12): 2723-9.
[http://dx.doi.org/10.1093/humrep/dew235] [PMID: 27664218]
[31]
Zhao Y, Luo Q, Zhang X, et al. Clinical efficacy and safety of stem cell-based therapy in treating asherman syndrome: A system review and meta-analysis Stem Cells Int 2020; 2020
[http://dx.doi.org/10.1155/2020/8820538]
[32]
Bahrehbar K, Rezazadeh Valojerdi M, Esfandiari F, Fathi R, Hassani S-N, Baharvand H. Human embryonic stem cell-derived mesenchymal stem cells improved premature ovarian failure. World J Stem Cells 2020; 12(8): 857-78.
[http://dx.doi.org/10.4252/wjsc.v12.i8.857] [PMID: 32952863]
[33]
Ghahremani-Nasab M, Ghanbari E, Jahanbani Y, Mehdizadeh A, Yousefi M. Premature ovarian failure and tissue engineering. J Cell Physiol 2020; 235(5): 4217-26.
[http://dx.doi.org/10.1002/jcp.29376] [PMID: 31663142]
[34]
Jankowska K. Premature ovarian failure. Menopause Rev 2017; 16(2): 51.
[http://dx.doi.org/10.5114/pm.2017.68592]
[35]
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(1): 263.
[http://dx.doi.org/10.1186/s13287-018-1008-9] [PMID: 30286808]
[36]
Rosenfield RL, Ehrmann DA. The Pathogenesis of Polycystic Ovary Syndrome (PCOS): The Hypothesis of PCOS as Functional Ovarian Hyperandrogenism Revisited. Endocr Rev 2016; 37(5): 467-520.
[http://dx.doi.org/10.1210/er.2015-1104] [PMID: 27459230]
[37]
Jin P, Xie Y. Treatment strategies for women with polycystic ovary syndrome. Gynecol Endocrinol 2018; 34(4): 272-7.
[http://dx.doi.org/10.1080/09513590.2017.1395841] [PMID: 29084464]
[38]
Patel S. Polycystic ovary syndrome (PCOS), an inflammatory, systemic, lifestyle endocrinopathy. J Steroid Biochem Mol Biol 2018; 182: 27-36.
[http://dx.doi.org/10.1016/j.jsbmb.2018.04.008] [PMID: 29678491]
[39]
Piparva KG, Buch JG. Deep vein thrombosis in a woman taking oral combined contraceptive pills. J Pharmacol Pharmacother 2011; 2(3): 185-6.
[http://dx.doi.org/10.4103/0976-500X.83284] [PMID: 21897713]
[40]
Yang PK, Hsu CY, Chen MJ, et al. The efficacy of 24-month metformin for improving menses, hormones, and metabolic profiles in polycystic ovary syndrome. J Clin Endocrinol Metab 2018; 103(3): 890-9.
[http://dx.doi.org/10.1210/jc.2017-01739] [PMID: 29325133]
[41]
Howie R, Kay V. Controlled ovarian stimulation for in-vitro fertilization. Br J Hosp Med (Lond) 2018; 79(4): 194-9.
[http://dx.doi.org/10.12968/hmed.2018.79.4.194] [PMID: 29620984]
[42]
Ives CW, Sinkey R, Rajapreyar I, Tita ATN, Oparil S. Preeclampsia-Pathophysiology and Clinical Presentations: JACC State-of-the-Art Review. J Am Coll Cardiol 2020; 76(14): 1690-702.
[http://dx.doi.org/10.1016/j.jacc.2020.08.014] [PMID: 33004135]
[43]
Backes CH, Markham K, Moorehead P, Cordero L, Nankervis CA, Giannone PJ. Maternal preeclampsia and neonatal outcomes. J Pregnancy 2011; 2011: 214365.
[http://dx.doi.org/10.1155/2011/214365] [PMID: 21547086]
[44]
Ghulmiyyah L, Sibai B. Maternal mortality from preeclampsia/eclampsia. Semin Perinatol 2012; 36(1): 56-9.
[http://dx.doi.org/10.1053/j.semperi.2011.09.011] [PMID: 22280867]
[45]
Armaly Z, Jadaon JE, Jabbour A, Abassi ZA. Preeclampsia: Novel Mechanisms and Potential Therapeutic Approaches. Front Physiol 2018; 9: 973.
[http://dx.doi.org/10.3389/fphys.2018.00973] [PMID: 30090069]
[46]
Jim B, Karumanchi SA. Preeclampsia: pathogenesis, prevention, and long-term complications. Semin Nephrol 2017; 37(4): 386-97.
[http://dx.doi.org/10.1016/j.semnephrol.2017.05.011] [PMID: 28711078]
[47]
Wang LL, Yu Y, Guan HB, Qiao C. Effect of human umbilical cord mesenchymal stem cell transplantation in a rat model of preeclampsia. Reprod Sci 2016; 23(8): 1058-70.
[http://dx.doi.org/10.1177/1933719116630417] [PMID: 26887428]
[48]
Stentz NC, Koelper N, Barnhart KT, Sammel MD, Senapati S. Infertility and mortality Am J Obstet Gynecol 2020; 222(3): 251-e1-.e10.
[http://dx.doi.org/10.1016/j.ajog.2019.09.007]
[49]
Wang Z, Wei Q, Wang H, et al. Mesenchymal stem cell therapy using human umbilical cord in a rat model of autoimmune-induced premature ovarian failure. Stem Cells Int 2020; 2020: 3249495.
[http://dx.doi.org/10.1155/2020/3249495] [PMID: 32714395]
[50]
Sanganalmath SK, Bolli R. Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res 2013; 113(6): 810-34.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.300219] [PMID: 23989721]
[51]
Tibbetts MD, Samuel MA, Chang TS, Ho AC. Stem cell therapy for retinal disease. Curr Opin Ophthalmol 2012; 23(3): 226-34.
[http://dx.doi.org/10.1097/ICU.0b013e328352407d] [PMID: 22450217]
[52]
Martínez Morales PL, Revilla. A, Ocaña I, et al. Progress in stem cell therapy for major human neurological disorders. Stem Cell Rev Rep 2013; 9(5): 685-99.
[http://dx.doi.org/10.1007/s12015-013-9443-6] [PMID: 23681704]
[53]
Volarevic V, Bojic S, Nurkovic J, et al. Stem cells as new agents for the treatment of infertility: current and future perspectives and challenges. BioMed Res Int 2014; 2014: 507234.
[http://dx.doi.org/10.1155/2014/507234] [PMID: 24826378]
[54]
Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997; 276(5309): 71-4.
[http://dx.doi.org/10.1126/science.276.5309.71] [PMID: 9082988]
[55]
Chang Z, Zhu H, Zhou X, et al. Mesenchymal Stem Cells in Preclinical Infertility Cytotherapy: A Retrospective Review. Stem Cells Int 2021; 2021: 8882368.
[http://dx.doi.org/10.1155/2021/8882368] [PMID: 34054970]
[56]
Neri S. Genetic stability of mesenchymal stromal cells for regenerative medicine applications: A fundamental biosafety aspect. Int J Mol Sci 2019; 20(10): E2406.
[http://dx.doi.org/10.3390/ijms20102406] [PMID: 31096604]
[57]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[http://dx.doi.org/10.1080/14653240600855905] [PMID: 16923606]
[58]
Khan RS, Newsome PN. A comparison of phenotypic and functional properties of mesenchymal stromal cells and multipotent adult progenitor cells. Front Immunol 2019; 10: 1952.
[http://dx.doi.org/10.3389/fimmu.2019.01952] [PMID: 31555259]
[59]
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(12): 2173-85.
[http://dx.doi.org/10.1002/sctm.17-0129] [PMID: 29076267]
[60]
Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci USA 2002; 99(13): 8932-7.
[http://dx.doi.org/10.1073/pnas.132252399] [PMID: 12084934]
[61]
Chen SL, Fang WW, Ye F, et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004; 94(1): 92-5.
[http://dx.doi.org/10.1016/j.amjcard.2004.03.034] [PMID: 15219514]
[62]
Mun CH, Kang MI, Shin YD, Kim Y, Park YB. The expression of immunomodulation-related cytokines and genes of adipose- and bone marrow-derived human mesenchymal stromal cells from early to late passages. Tissue Eng Regen Med 2018; 15(6): 771-9.
[http://dx.doi.org/10.1007/s13770-018-0147-5] [PMID: 30603595]
[63]
Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol 2016; 2016: 6940283.
[http://dx.doi.org/10.1155/2016/6940283] [PMID: 27516776]
[64]
Prigozhina TB, Khitrin S, Elkin G, Eizik O, Morecki S, Slavin S. Mesenchymal stromal cells lose their immunosuppressive potential after allotransplantation. Exp Hematol 2008; 36(10): 1370-6.
[http://dx.doi.org/10.1016/j.exphem.2008.04.022] [PMID: 18619727]
[65]
Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005; 105(7): 2821-7.
[http://dx.doi.org/10.1182/blood-2004-09-3696] [PMID: 15591115]
[66]
Parsch D, Fellenberg J, Brümmendorf TH, Eschlbeck AM, Richter W. Telomere length and telomerase activity during expansion and differentiation of human mesenchymal stem cells and chondrocytes. J Mol Med (Berl) 2004; 82(1): 49-55.
[http://dx.doi.org/10.1007/s00109-003-0506-z] [PMID: 14647922]
[67]
Zimmermann S, Voss M, Kaiser S, Kapp U, Waller CF, Martens UM. Lack of telomerase activity in human mesenchymal stem cells. Leukemia 2003; 17(6): 1146-9.
[http://dx.doi.org/10.1038/sj.leu.2402962] [PMID: 12764382]
[68]
Zhao YX, Chen SR, Su PP, et al. Using mesenchymal stem cells to treat female infertility: An update on female reproductive diseases. Stem Cells Int 2019; 2019: 9071720.
[http://dx.doi.org/10.1155/2019/9071720] [PMID: 31885630]
[69]
Harrell CR, Fellabaum C, Jovicic N, Djonov V, Arsenijevic N, Volarevic V. Molecular mechanisms responsible for therapeutic potential of mesenchymal stem cell-derived secretome. Cells 2019; 8(5): E467.
[http://dx.doi.org/10.3390/cells8050467] [PMID: 31100966]
[70]
Cho J, Kim TH, Seok J, et al. Vascular remodeling by placenta-derived mesenchymal stem cells restores ovarian function in ovariectomized rat model via the VEGF pathway. Lab Invest 2021; 101(3): 304-17.
[http://dx.doi.org/10.1038/s41374-020-00513-1] [PMID: 33303971]
[71]
Saribas GS, Ozogul C, Tiryaki M, Alpaslan Pinarli F, Hamdemir Kilic S. Effects of uterus derived mesenchymal stem cells and their exosomes on asherman’s syndrome. Acta Histochem 2020; 122(1): 151465.
[http://dx.doi.org/10.1016/j.acthis.2019.151465] [PMID: 31776004]
[72]
Tsuji K, Kitamura S, Wada J. Secretomes from mesenchymal stem cells against acute kidney injury: Possible heterogeneity. Stem Cells Int 2018; 2018: 8693137.
[http://dx.doi.org/10.1155/2018/8693137] [PMID: 30651737]
[73]
Tan JL, Lau SN, Leaw B, et al. Amnion epithelial cell-derived exosomes restrict lung injury and enhance endogenous lung repair. Stem Cells Transl Med 2018; 7(2): 180-96.
[http://dx.doi.org/10.1002/sctm.17-0185] [PMID: 29297621]
[74]
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: 407-18.
[http://dx.doi.org/10.1016/j.omtn.2019.03.008] [PMID: 31022607]
[75]
Yang M, Lin L, Sha C, et al. Bone marrow mesenchymal stem cell-derived exosomal miR-144-5p improves rat ovarian function after chemotherapy-induced ovarian failure by targeting PTEN. Lab Invest 2020; 100(3): 342-52.
[http://dx.doi.org/10.1038/s41374-019-0321-y] [PMID: 31537899]
[76]
Zhao S, Qi W, Zheng J, et al. Exosomes derived from adipose mesenchymal stem cells restore functional endometrium in a rat model of intrauterine adhesions. Reprod Sci 2020; 27(6): 1266-75.
[http://dx.doi.org/10.1007/s43032-019-00112-6] [PMID: 31933162]
[77]
Jahanbani Y, Davaran S, Ghahremani-Nasab M, Aghebati-Maleki L, Yousefi M. Scaffold-based tissue engineering approaches in treating infertility. Life Sci 2020; 240: 117066.
[http://dx.doi.org/10.1016/j.lfs.2019.117066] [PMID: 31738881]
[78]
Hutmacher DW. Scaffold design and fabrication technologies for engineering tissues--state of the art and future perspectives. J Biomater Sci Polym Ed 2001; 12(1): 107-24.
[http://dx.doi.org/10.1163/156856201744489] [PMID: 11334185]
[79]
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]
[80]
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]
[81]
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]
[82]
Sun B, Ma Y, Wang F, Hu L, Sun Y. miR-644-5p carried by bone mesenchymal stem cell-derived exosomes targets regulation of p53 to inhibit ovarian granulosa cell apoptosis. Stem Cell Res Ther 2019; 10(1): 360.
[http://dx.doi.org/10.1186/s13287-019-1442-3] [PMID: 31783913]
[83]
I Cervelló, C Gil-Sanchis, X Santamaría, et al. Human CD133(+)bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome Fertil Steril 2015; 104(6): 1552-60.
[84]
Gao L, Huang Z, Lin H, Tian Y, Li P, Lin S. Bone marrow mesenchymal stem cells (BMSCs) restore functional endometrium in the rat model for severe asherman syndrome. Reprod Sci 2019; 26(3): 436-44.
[http://dx.doi.org/10.1177/1933719118799201] [PMID: 30458678]
[85]
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]
[86]
Terraciano P, Garcez T, Ayres L, et al. Cell therapy for chemically induced ovarian failure in mice. Stem Cells Int 2014; 2014: 720753.
[http://dx.doi.org/10.1155/2014/720753] [PMID: 25548574]
[87]
Su J, Ding L, Cheng J, 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(5): 1075-86.
[http://dx.doi.org/10.1093/humrep/dew041] [PMID: 26965432]
[88]
Kilic S, Yuksel B, Pinarli F, Albayrak A, Boztok B, Delibasi T. Effect of stem cell application on Asherman syndrome, an experimental rat model. J Assist Reprod Genet 2014; 31(8): 975-82.
[http://dx.doi.org/10.1007/s10815-014-0268-2] [PMID: 24974357]
[89]
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]
[90]
Zhong Z, Patel AN, Ichim TE, et al. Feasibility investigation of allogeneic endometrial regenerative cells. J Transl Med 2009; 7: 15.
[http://dx.doi.org/10.1186/1479-5876-7-15] [PMID: 19232091]
[91]
Manshadi MD, Navid S, Hoshino Y, Daneshi E, Noory P, Abbasi M. The effects of human menstrual blood stem cells-derived granulosa cells on ovarian follicle formation in a rat model of premature ovarian failure. Microsc Res Tech 2019; 82(6): 635-42.
[http://dx.doi.org/10.1002/jemt.23120] [PMID: 30582244]
[92]
Mohamed SA, Shalaby S, Brakta S, Elam L, Elsharoud A, Al-Hendy A. Umbilical cord blood mesenchymal stem cells as an infertility treatment for chemotherapy induced premature ovarian insufficiency. Biomedicines 2019; 7(1): E7.
[http://dx.doi.org/10.3390/biomedicines7010007] [PMID: 30669278]
[93]
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(4): 370-82.
[http://dx.doi.org/10.1016/j.tice.2016.05.001] [PMID: 27233913]
[94]
Xie Q, Xiong X, Xiao N, et al. Mesenchymal stem cells alleviate dhea-induced polycystic ovary syndrome (PCOS) by inhibiting inflammation in mice. Stem Cells Int 2019; 2019: 9782373.
[http://dx.doi.org/10.1155/2019/9782373] [PMID: 31611920]
[95]
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]
[96]
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]
[97]
Chu DT, Phuong TNT, Tien NLB, et al. An update on the progress of isolation, culture, storage, and clinical application of human bone marrow mesenchymal stem/stromal cells. Int J Mol Sci 2020; 21(3): E708.
[http://dx.doi.org/10.3390/ijms21030708] [PMID: 31973182]
[98]
Nasef A, Fouillard L, El-Taguri A, Lopez M. Human bone marrow-derived mesenchymal stem cells. Libyan J Med 2007; 2(4): 190-201.
[http://dx.doi.org/10.3402/ljm.v2i4.4729] [PMID: 21503244]
[99]
Besikcioglu HE, GS Sarıbas, C Ozogul, et al. Determination of the effects of bone marrow derived mesenchymal stem cells and ovarian stromal stem cells on follicular maturation in cyclophosphamide induced ovarian failure in rats. Taiwan J Obstet Gynecol 2019; 58(1): 53-9.
[http://dx.doi.org/10.1016/j.tjog.2018.11.010] [PMID: 30638481]
[100]
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(12): 1445-58.
[http://dx.doi.org/10.1016/j.jcyt.2018.09.005] [PMID: 30523787]
[101]
Herraiz S, Romeu M, Buigues A, et al. Autologous stem cell ovarian transplantation to increase reproductive potential in patients who are poor responders. Fertil Steril 2018; 110(3): 496-505.e1.
[http://dx.doi.org/10.1016/j.fertnstert.2018.04.025] [PMID: 29960701]
[102]
Hassanshahi A, Hassanshahi M, Khabbazi S, et al. Adipose-derived stem cells for wound healing. J Cell Physiol 2019; 234(6): 7903-14.
[http://dx.doi.org/10.1002/jcp.27922] [PMID: 30515810]
[103]
Damous LL, Nakamuta JS, Carvalho AE, et al. Does adipose tissue-derived stem cell therapy improve graft quality in freshly grafted ovaries? Reprod Biol Endocrinol 2015; 13: 108.
[http://dx.doi.org/10.1186/s12958-015-0104-2] [PMID: 26394676]
[104]
Zhang C. The roles of different stem cells in premature ovarian failure. Curr Stem Cell Res Ther 2020; 15(6): 473-81.
[http://dx.doi.org/10.2174/1574888X14666190314123006] [PMID: 30868961]
[105]
Lee SY, Shin JE, Kwon H, Choi DH, Kim JH. Effect of autologous adipose-derived stromal vascular fraction transplantation on endometrial regeneration in patients of asherman’s syndrome: A pilot study. Reprod Sci 2020; 27(2): 561-8.
[http://dx.doi.org/10.1007/s43032-019-00055-y] [PMID: 32046396]
[106]
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]
[107]
Chen L, Qu J, Cheng T, Chen X, Xiang C. Menstrual blood-derived stem cells: toward therapeutic mechanisms, novel strategies, and future perspectives in the treatment of diseases. Stem Cell Res Ther 2019; 10(1): 406.
[http://dx.doi.org/10.1186/s13287-019-1503-7] [PMID: 31864423]
[108]
Lv H, Hu Y, Cui Z, Jia H. Human menstrual blood: a renewable and sustainable source of stem cells for regenerative medicine. Stem Cell Res Ther 2018; 9(1): 325.
[http://dx.doi.org/10.1186/s13287-018-1067-y] [PMID: 30463587]
[109]
Abbaszadeh H, Ghorbani F, Derakhshani M, Movassaghpour A, Yousefi M. Human umbilical cord mesenchymal stem cell-derived extracellular vesicles: A novel therapeutic paradigm. J Cell Physiol 2020; 235(2): 706-17.
[http://dx.doi.org/10.1002/jcp.29004] [PMID: 31254289]
[110]
Marino L, Castaldi MA, Rosamilio R, et al. Mesenchymal stem cells from the wharton’s jelly of the human umbilical cord: Biological properties and therapeutic potential. Int J Stem Cells 2019; 12(2): 218-26.
[http://dx.doi.org/10.15283/ijsc18034] [PMID: 31022994]
[111]
Nekanti U, Mohanty L, Venugopal P, Balasubramanian S, Totey S, Ta M. Optimization and scale-up of Wharton’s jelly-derived mesenchymal stem cells for clinical applications. Stem Cell Res (Amst) 2010; 5(3): 244-54.
[http://dx.doi.org/10.1016/j.scr.2010.08.005] [PMID: 20880767]
[112]
Fong CY, Richards M, Manasi N, Biswas A, Bongso A. Comparative growth behaviour and characterization of stem cells from human Wharton’s jelly. Reprod Biomed Online 2007; 15(6): 708-18.
[http://dx.doi.org/10.1016/S1472-6483(10)60539-1] [PMID: 18062871]
[113]
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; 2016: 2517514.
[http://dx.doi.org/10.1155/2016/2517514] [PMID: 27047962]
[114]
Cao Y, Sun H, Zhu H, et al. Allogeneic cell therapy using umbilical cord MSCs on collagen scaffolds for patients with recurrent uterine adhesion: a phase I clinical trial. Stem Cell Res Ther 2018; 9(1): 192.
[http://dx.doi.org/10.1186/s13287-018-0904-3] [PMID: 29996892]
[115]
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]
[116]
Berebichez-Fridman R, Montero-Olvera PR. Sources and clinical applications of mesenchymal stem cells: State-of-the-art review. Sultan Qaboos Univ Med J 2018; 18(3): e264-77.
[http://dx.doi.org/10.18295/squmj.2018.18.03.002] [PMID: 30607265]
[117]
Magatti M, Vertua E, Cargnoni A, Silini A, Parolini O. The immunomodulatory properties of amniotic cells: The two sides of the coin. Cell Transplant 2018; 27(1): 31-44.
[http://dx.doi.org/10.1177/0963689717742819] [PMID: 29562786]
[118]
Muttini A, Barboni B, Valbonetti L, Russo V, Maffulli N. Amniotic epithelial stem cells: Salient features and possible therapeutic role. Sports Med Arthrosc Rev 2018; 26(2): 70-4.
[http://dx.doi.org/10.1097/JSA.0000000000000189] [PMID: 29722767]
[119]
Ding C, Li H, Wang Y, et al. Different therapeutic effects of cells derived from human amniotic membrane on premature ovarian aging depend on distinct cellular biological characteristics. Stem Cell Res Ther 2017; 8(1): 173.
[http://dx.doi.org/10.1186/s13287-017-0613-3] [PMID: 28750654]
[120]
Loukogeorgakis SP, De Coppi P. Concise review: Amniotic fluid stem cells: The known, the unknown, and potential regenerative medicine applications. Stem Cells 2017; 35(7): 1663-73.
[http://dx.doi.org/10.1002/stem.2553] [PMID: 28009066]
[121]
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]
[122]
Azizi R, Aghebati-Maleki L, Nouri M, Marofi F, Negargar S, Yousefi M. Stem cell therapy in Asherman syndrome and thin endometrium: Stem cell- based therapy. Biomed Pharmacother 2018; 102: 333-43.
[http://dx.doi.org/10.1016/j.biopha.2018.03.091] [PMID: 29571018]
[123]
Yang Y, Lei L, Wang S, et al. Transplantation of umbilical cord-derived mesenchymal stem cells on a collagen scaffold improves ovarian function in a premature ovarian failure model of mice. In Vitro Cell Dev Biol Anim 2019; 55(4): 302-11.
[http://dx.doi.org/10.1007/s11626-019-00337-4] [PMID: 30820812]
[124]
Zhao G, Cao Y, Zhu X, et al. Transplantation of collagen scaffold with autologous bone marrow mononuclear cells promotes functional endometrium reconstruction via downregulating ∆Np63 expression in Asherman’s syndrome. Sci China Life Sci 2017; 60(4): 404-16.
[http://dx.doi.org/10.1007/s11427-016-0328-y] [PMID: 27921235]
[125]
Saha S, Roy P, Corbitt C, Kakar SS. Application of stem cell therapy for infertility. Cells 2021; 10(7): 1613.
[http://dx.doi.org/10.3390/cells10071613] [PMID: 34203240]
[126]
Ratajczak MZ, Ratajczak J, Kucia M. Very small embryonic-like stem cells (VSELs). Circ Res 2019; 124(2): 208-10.
[http://dx.doi.org/10.1161/CIRCRESAHA.118.314287] [PMID: 30653438]
[127]
Bhartiya D, Unni S, Parte S, Anand S. Very small embryonic-like stem cells: implications in reproductive biology. BioMed Res Int 2013; 2013: 682326.
[http://dx.doi.org/10.1155/2013/682326] [PMID: 23509758]
[128]
Kucia M, Reca R, Campbell FR, et al. A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006; 20(5): 857-69.
[http://dx.doi.org/10.1038/sj.leu.2404171] [PMID: 16498386]
[129]
Ratajczak MZ, Ratajczak J, Suszynska M, Miller DM, Kucia M, Shin DM. A novel view of the adult stem cell compartment from the perspective of a quiescent population of very small embryonic-like stem cells. Circ Res 2017; 120(1): 166-78.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.309362] [PMID: 28057792]
[130]
Bhartiya D. Stem cells survive oncotherapy & can regenerate non-functional gonads: A paradigm shift for oncofertility. Indian J Med Res 2018; 148 (Suppl.): S38-49.
[PMID: 30964080]
[131]
Virant-Klun I. Functional testing of primitive oocyte-like cells developed in ovarian surface epithelium cell culture from small vsel-like stem cells: Can they be fertilized one day? Stem Cell Rev Rep 2018; 14(5): 715-21.
[http://dx.doi.org/10.1007/s12015-018-9832-y] [PMID: 29876729]
[132]
Sharara FI, Lelea LL, Rahman S, Klebanoff JS, Moawad GN. A narrative review of platelet-rich plasma (PRP) in reproductive medicine. J Assist Reprod Genet 2021; 38(5): 1003-12.
[http://dx.doi.org/10.1007/s10815-021-02146-9] [PMID: 33723748]
[133]
Hajipour H, Farzadi L, Latifi Z, et al. An update on platelet-rich plasma (PRP) therapy in endometrium and ovary related infertilities: clinical and molecular aspects. Syst Biol Reprod Med 2021; 67(3): 177-88.
[http://dx.doi.org/10.1080/19396368.2020.1862357] [PMID: 33632047]
[134]
Bos-Mikich A, de Oliveira R, Frantz N. Platelet-rich plasma therapy and reproductive medicine. J Assist Reprod Genet 2018; 35(5): 753-6.
[http://dx.doi.org/10.1007/s10815-018-1159-8] [PMID: 29564738]
[135]
Sfakianoudis K, Rapani A, Grigoriadis S, et al. Novel approaches in addressing ovarian insufficiency in 2019: Are we there yet? Cell Transplant 2020; 29: 963689720926154.
[http://dx.doi.org/10.1177/0963689720926154] [PMID: 32686983]
[136]
Everts PAM, Knape JTA, Weibrich G, et al. Platelet-rich plasma and platelet gel: a review. J Extra Corpor Technol 2006; 38(2): 174-87.
[PMID: 16921694]
[137]
Zhang S, Li P, Yuan Z, Tan J. Platelet-rich plasma improves therapeutic effects of menstrual blood-derived stromal cells in rat model of intrauterine adhesion. Stem Cell Res Ther 2019; 10(1): 61.
[http://dx.doi.org/10.1186/s13287-019-1155-7] [PMID: 30770774]
[138]
Tomassetti C, D’Hooghe T. Endometriosis and infertility: Insights into the causal link and management strategies. Best Pract Res Clin Obstet Gynaecol 2018; 51: 25-33.
[http://dx.doi.org/10.1016/j.bpobgyn.2018.06.002] [PMID: 30245115]
[139]
Olooto WE, Amballi AA, Banjo TA. A review of Female Infertility; important etiological factors and management. J Microbiol Biotechnol Res 2012; 2(3): 379-85.
[140]
Webber L, Anderson RA, Davies M, Janse F, Vermeulen N. HRT for women with premature ovarian insufficiency: a comprehensive review. Hum Reprod Open 2017; 2017(2): hox007.
[http://dx.doi.org/10.1093/hropen/hox007] [PMID: 30895225]
[141]
Igboeli P, El Andaloussi A, Sheikh U, et al. Intraovarian injection of autologous human mesenchymal stem cells increases estrogen production and reduces menopausal symptoms in women with premature ovarian failure: two case reports and a review of the literature. J Med Case Reports 2020; 14(1): 108.
[http://dx.doi.org/10.1186/s13256-020-02426-5] [PMID: 32680541]
[142]
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]
[143]
Li J, Mao Q, He J, She H, Zhang Z, Yin C. Human umbilical cord mesenchymal stem cells improve the reserve function of perimenopausal ovary via a paracrine mechanism. Stem Cell Res Ther 2017; 8(1): 55.
[http://dx.doi.org/10.1186/s13287-017-0514-5] [PMID: 28279229]
[144]
Hendriks S, Dancet EA, van Pelt AM, Hamer G, Repping S. Artificial gametes: a systematic review of biological progress towards clinical application. Hum Reprod Update 2015; 21(3): 285-96.
[http://dx.doi.org/10.1093/humupd/dmv001] [PMID: 25609401]
[145]
Santamaria X, Cabanillas S, I Cervelló, et al. Autologous cell therapy with CD133+ bone marrow-derived stem cells for refractory Asherman’s syndrome and endometrial atrophy: a pilot cohort study. Hum Reprod 2016; 31(5): 1087-96.
[http://dx.doi.org/10.1093/humrep/dew042] [PMID: 27005892]
[146]
Kokai LE, Marra K, Rubin JP. Adipose stem cells: biology and clinical applications for tissue repair and regeneration. Transl Res 2014; 163(4): 399-408.
[http://dx.doi.org/10.1016/j.trsl.2013.11.009] [PMID: 24361334]
[147]
Ballios BG, Cooke MJ, van der Kooy D, Shoichet MS. A hydrogel-based stem cell delivery system to treat retinal degenerative diseases. Biomaterials 2010; 31(9): 2555-64.
[http://dx.doi.org/10.1016/j.biomaterials.2009.12.004] [PMID: 20056272]

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