Using Mesenchymal Stem Cells to Treat Female Infertility: An Update on Female Reproductive Diseases

Yun-Xia Zhao, Shao-Rong Chen, Ping-Ping Su, Feng-Huang Huang, Yan-Chuan Shi, Qi-Yang Shi, Shu Lin, Yun-Xia Zhao, Shao-Rong Chen, Ping-Ping Su, Feng-Huang Huang, Yan-Chuan Shi, Qi-Yang Shi, Shu Lin

Abstract

Female infertility impacts the quality of life and well-being of affected individuals and couples. Female reproductive diseases, such as primary ovarian insufficiency, polycystic ovary syndrome, endometriosis, fallopian tube obstruction, and Asherman syndrome, can induce infertility. In recent years, translational medicine has developed rapidly, and clinical researchers are focusing on the treatment of female infertility using novel approaches. Owing to the advantages of convenient samples, abundant sources, and avoidable ethical issues, mesenchymal stem cells (MSCs) can be applied widely in the clinic. This paper reviews recent advances in using four types of MSCs, bone marrow stromal cells, adipose-derived stem cells, menstrual blood mesenchymal stem cells, and umbilical cord mesenchymal stem cells. Each of these have been used for the treatment of ovarian and uterine diseases, and provide new approaches for the treatment of female infertility.

Conflict of interest statement

There is no conflict of interest to declare.

Copyright © 2019 Yun-xia Zhao et al.

Figures

Figure 1
Figure 1
Diagram showing some possible causes of female infertility, such as fallopian tube obstruction, premature ovarian failure (POF), endometriosis, polycystic ovary syndrome (PCOS), Asherman syndrome, and polyps.
Figure 2
Figure 2
The derivation of the four types of MSCs and the biologic property of these MSCs. Potential mechanisms have been proposed for ovarian dysfunction and endometrial disorder therapy. Vascular endothelial growth factor (VEGF), hepatocyte growth factor (HGF), leukemia inhibitory factor (LIF), transforming growth factor (TGF), B-cell lymphoma 2 (Bcl-2), and matrix metalloproteinase (MMP).

References

    1. Hull M. G., Glazener C. M., Kelly N. J., et al. Population study of causes, treatment, and outcome of infertility. BMJ. 1985;291(6510):1693–1697. doi: 10.1136/bmj.291.6510.1693.
    1. Chandra A., Martinez G. M., Mosher W. D., Abma J. C., Jones J. Fertility, family planning, and reproductive health of U.S. women; data from the 2002 National Survey of Family Growth. Vital and Health Statistics. 2005;23(25):1–160. doi: 10.1037/e414702008-001.
    1. Deroux A., Dumestre-Perard C., Dunand-Faure C., Bouillet L., Hoffmann P. Female infertility and serum auto-antibodies: a systematic review. Clinical Reviews in Allergy and Immunology. 2017;53(1):78–86. doi: 10.1007/s12016-016-8586-z.
    1. Holmberg L., Iversen O. E., Rudenstam C. M., et al. Increased risk of recurrence after hormone replacement therapy in breast cancer survivors. JNCI: Journal of the National Cancer Institute. 2008;100(7):475–482. doi: 10.1093/jnci/djn058.
    1. Vermeulen R. F. M., Korse C. M., Kenter G. G., Brood-van Zanten M. M. A., van Beurden M. Safety of hormone replacement therapy following risk-reducing salpingo-oophorectomy: systematic review of literature and guidelines. Climacteric. 2019;22(4):352–360. doi: 10.1080/13697137.2019.1582622.
    1. Practice Committee of the American Society for Reproductive Medicine. Multiple gestation associated with infertility therapy: an American Society for Reproductive Medicine Practice Committee opinion. Fertility and Sterility. 2012;97(4):825–834. doi: 10.1016/j.fertnstert.2011.11.048.
    1. Blum B., Benvenisty N. The tumorigenicity of human embryonic stem cells. Advances in Cancer Research. 2008;100(8):133–158. doi: 10.1016/S0065-230X(08)00005-5.
    1. 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):315–317. doi: 10.1080/14653240600855905.
    1. Dezawa M., Ishikawa H., Itokazu Y., et al. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science. 2005;309(5732):314–317. doi: 10.1126/science.1110364.
    1. Salem H. K., Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010;28(3):585–596. doi: 10.1002/stem.269.
    1. Körbling M., Anderlini P. Peripheral blood stem cell versus bone marrow allotransplantation: does the source of hematopoietic stem cells matter? Blood. 2001;98(10):2900–2908. doi: 10.1182/blood.V98.10.2900.
    1. Meng X., Ichim T. E., Zhong J., et al. Endometrial regenerative cells: a novel stem cell population. Journal of Translational Medicine. 2007;5(1):1–10. doi: 10.1186/1479-5876-5-57.
    1. Barry F. P., Murphy J. M. Mesenchymal stem cells: clinical applications and biological characterization. The International Journal of Biochemistry & Cell Biology. 2004;36(4):568–584. doi: 10.1016/j.biocel.2003.11.001.
    1. Lee O. K., Kuo T. K., Chen W.-M., Lee K.-D., Hsieh S.-L., Chen T.-H. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2004;103(5):1669–1675. doi: 10.1182/blood-2003-05-1670.
    1. in’t Anker P. S., Scherjon S. A., der Keur C. K.-v., et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells. 2004;22(7):1338–1345. doi: 10.1634/stemcells.2004-0058.
    1. Krampera M., Galipeau J., Shi Y., Tarte K., Sensebe L., MSC Committee of the International Society for Cellular Therapy (ISCT) Immunological characterization of multipotent mesenchymal stromal cells--The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy. 2013;15(9):1054–1061. doi: 10.1016/j.jcyt.2013.02.010.
    1. Galipeau J., Krampera M., Barrett J., et al. International Society for Cellular Therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy. 2016;18(2):151–159. doi: 10.1016/j.jcyt.2015.11.008.
    1. Naji A., Rouas-Freiss N., Durrbach A., Carosella E. D., Sensébé L., Deschaseaux F. Concise review: combining human leukocyte antigen G and mesenchymal stem cells for immunosuppressant biotherapy. Stem Cells. 2013;31(11):2296–2303. doi: 10.1002/stem.1494.
    1. Squillaro T., Peluso G., Galderisi U. Clinical trials with mesenchymal stem cells: an update. Cell Transplantation. 2016;25(5):829–848. doi: 10.3727/096368915X689622.
    1. Galipeau J., Sensébé L. Mesenchymal stromal cells: clinical challenges and therapeutic opportunities. Cell Stem Cell. 2018;22(6):824–833. doi: 10.1016/j.stem.2018.05.004.
    1. Trounson A., McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell. 2015;17(1):11–22. doi: 10.1016/j.stem.2015.06.007.
    1. Owen M., Friedenstein A. J. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Foundation Symposium. 1988;136:42–60. doi: 10.1002/9780470513637.ch4.
    1. Altaner C., Altanerova V., Cihova M., et al. Characterization of mesenchymal stem cells of “no-options” patients with critical limb ischemia treated by autologous bone marrow mononuclear cells. PLoS One. 2013;8(9, article e73722):9. doi: 10.1371/journal.pone.0073722.
    1. Yun Cheng H. The impact of mesenchymal stem cell source on proliferation, differentiation, immunomodulation and therapeutic efficacy. Journal of Stem Cell Research & Therapy. 2014;04(10) doi: 10.4172/2157-7633.1000237.
    1. Ullah I., Subbarao R. B., Rho G. J. Human mesenchymal stem cells - current trends and future prospective. Bioscience Reports. 2015;35(2):1–18. doi: 10.1042/bsr20150025.
    1. Besikcioglu H. E., Sarıbas G. S., Ozogul C., 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. Taiwanese Journal of Obstetrics & Gynecology. 2019;58(1):53–59. doi: 10.1016/j.tjog.2018.11.010.
    1. 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. Reproductive Sciences. 2019;26(3):436–444. doi: 10.1177/1933719118799201.
    1. Liu Y., Tal R., Pluchino N., Mamillapalli R., Taylor H. S. Systemic administration of bone marrow-derived cells leads to better uterine engraftment than use of uterine-derived cells or local injection. Journal of Cellular and Molecular Medicine. 2018;22(1):67–76. doi: 10.1111/jcmm.13294.
    1. Tepper O. M., Sealove B. A., Murayama T., Asahara T. Newly emerging concepts in blood vessel growth: recent discovery of endothelial progenitor cells and their function in tissue regeneration. Journal of Investigative Medicine. 2003;51(6):353–359. doi: 10.1136/jim-51-06-31.
    1. Wei X., Yang X., Han Z. P., Qu F. F., Shao L., Shi Y. F. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacologica Sinica. 2013;34(6):747–754. doi: 10.1038/aps.2013.50.
    1. Abd-Allah S. H., Shalaby S. M., Pasha H. F., 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. doi: 10.1016/j.jcyt.2012.08.001.
    1. Badawy A., Sobh M. A., Ahdy M., Abdelhafez M. S. Bone marrow mesenchymal stem cell repair of cyclophosphamide-induced ovarian insufficiency in a mouse model. International Journal of Women's Health. 2017;9:441–447. doi: 10.2147/IJWH.S134074.
    1. 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 Research & Therapy. 2017;8(1):p. 187. doi: 10.1186/s13287-017-0641-z.
    1. Mohamed S. A., Shalaby S. M., Abdelaziz M., et al. Human mesenchymal stem cells partially reverse infertility in chemotherapy-induced ovarian failure. Reproductive Sciences. 2018;25(1):51–63. doi: 10.1177/1933719117699705.
    1. Taylor H. S. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. Journal of the American Medical Association. 2004;292(1):81–85. doi: 10.1001/jama.292.1.81.
    1. Panchal S., Patel H., Nagori C. Endometrial regeneration using autologous adult stem cells followed by conception by in vitro fertilization in a patient of severe Asherman’s syndrome. Journal of Human Reproductive Sciences. 2011;4(1):43–48. doi: 10.4103/0974-1208.82360.
    1. Singh N., Mohanty S., Seth T., Shankar M., Dharmendra S., Bhaskaran S. Autologous stem cell transplantation in refractory Asherman’s syndrome: a novel cell based therapy. Journal of Human Reproductive Sciences. 2014;7(2):93–98. doi: 10.4103/0974-1208.138864.
    1. Alawadhi F., Du H., Cakmak H., Taylor H. S. Bone marrow-derived stem cell (BMDSC) transplantation improves fertility in a murine model of Asherman’s syndrome. PLoS One. 2014;9(5):e96662–e96666. doi: 10.1371/journal.pone.0096662.
    1. Wang J., Ju B., Pan C., et al. Application of bone marrow-derived mesenchymal stem cells in the treatment of intrauterine adhesions in rats. Cellular Physiology and Biochemistry. 2016;39(4):1553–1560. doi: 10.1159/000447857.
    1. Santamaria X., Cabanillas S., Cervelló I., et al. Autologous cell therapy with CD133+ bone marrow-derived stem cells for refractory Asherman’s syndrome and endometrial atrophy: a pilot cohort study. Human Reproduction. 2016;31(5):1087–1096. doi: 10.1093/humrep/dew042.
    1. Cervelló I., Gil-Sanchis C., Santamaría X., et al. Human CD133+ bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertility and Sterility. 2015;104(6):1552–1560.e3. doi: 10.1016/j.fertnstert.2015.08.032.
    1. Zhao G., Cao Y., Zhu X., et al. Transplantation of collagen scaffold with autologous bone marrow mononuclear cells promotes functional endometrium reconstruction via downregulating ΔNp63 expression in Asherman’s syndrome. Science China Life Sciences. 2017;60(4):404–416. doi: 10.1007/s11427-016-0328-y.
    1. Lendeckel S., Jödicke A., Christophis P., et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. Journal of Cranio-Maxillofacial Surgery. 2004;32(6):370–373. doi: 10.1016/j.jcms.2004.06.002.
    1. Yang J.-A., Chung H.-M., Won C.-H., Sung J.-H. Potential application of adipose-derived stem cells and their secretory factors to skin: discussion from both clinical and industrial viewpoints. Expert Opinion on Biological Therapy. 2010;10(4):495–503. doi: 10.1517/14712591003610598.
    1. Ra J. C., Jeong E. C., Kang S. K., Lee S. J., Choi K. H. A prospective, nonrandomized, no placebo-controlled, phase I/II clinical trial assessing the safety and efficacy of intramuscular injection of autologous adipose tissue-derived mesenchymal stem cells in patients with severe Buerger’s disease. Cell Medicine. 2017;9(3):87–102. doi: 10.3727/215517916X693069.
    1. Lee R. H., Kim B. C., Choi I. S., et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cellular Physiology and Biochemistry. 2004;14(4–6):311–324. doi: 10.1159/000080341.
    1. Choudhery M. S., Badowski M., Muise A., Pierce J., Harris D. T. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. Journal of Translational Medicine. 2014;12(1):8–14. doi: 10.1186/1479-5876-12-8.
    1. Damous L. L., Nakamuta J. S., Saturi de Carvalho A. E. T., et al. Does adipose tissue-derived stem cell therapy improve graft quality in freshly grafted ovaries? Reproductive Biology and Endocrinology. 2015;13(1, article 104):1–11. doi: 10.1186/s12958-015-0104-2.
    1. Terraciano P., Garcez T., Ayres L., et al. Cell therapy for chemically induced ovarian failure in mice. Stem Cells International. 2014;2014:8. doi: 10.1155/2014/720753.720753
    1. Sun M., Wang S., Li Y., et al. Adipose-derived stem cells improved mouse ovary function after chemotherapy-induced ovary failure. Stem Cell Research & Therapy. 2013;4(4):p. 80. doi: 10.1186/scrt231.
    1. 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. Human Reproduction. 2016;31(5):1075–1086. doi: 10.1093/humrep/dew041.
    1. Kilic S., Yuksel B., Pinarli F., Albayrak A., Boztok B., Delibasi T. Effect of stem cell application on Asherman syndrome, an experimental rat model. Journal of Assisted Reproduction and Genetics. 2014;31(8):975–982. doi: 10.1007/s10815-014-0268-2.
    1. Zhong Z., Patel A. N., Ichim T. E., et al. Feasibility investigation of allogeneic endometrial regenerative cells. Journal of Translational Medicine. 2009;7(1):15–17. doi: 10.1186/1479-5876-7-15.
    1. Wolff E. F., Mutlu L., Massasa E. E., Elsworth J. D., Eugene Redmond D., Jr., Taylor H. S. Endometrial stem cell transplantation in MPTP- exposed primates: an alternative cell source for treatment of Parkinson's disease. Journal of Cellular and Molecular Medicine. 2015;19(1):249–256. doi: 10.1111/jcmm.12433.
    1. Wolff E. F., Gao X. B., Yao K. V., et al. Endometrial stem cell transplantation restores dopamine production in a Parkinson’s disease model. Journal of Cellular and Molecular Medicine. 2011;15(4):747–755. doi: 10.1111/j.1582-4934.2010.01068.x.
    1. Santamaria X., Massasa E. E., Feng Y., Wolff E., Taylor H. S. Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Molecular Therapy. 2011;19(11):2065–2071. doi: 10.1038/mt.2011.173.
    1. Li H.-Y., Chen Y.-J., Chen S.-J., et al. Induction of insulin-producing cells derived from endometrial mesenchymal stem-like cells. The Journal of Pharmacology and Experimental Therapeutics. 2010;335(3):817–829. doi: 10.1124/jpet.110.169284.
    1. 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 and Development. 2014;23(13):1548–1557. doi: 10.1089/scd.2013.0371.
    1. Manshadi M. D., 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. Microscopy Research and Technique. 2019;82(6):635–642. doi: 10.1002/jemt.23120.
    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. Journal of Translational Medicine. 2015;13(1) doi: 10.1186/s12967-015-0516-y.
    1. 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 Research & Therapy. 2017;8(1):11–14. doi: 10.1186/s13287-016-0458-1.
    1. Momose T., Miyaji H., Kato A., et al. Collagen hydrogel scaffold and fibroblast growth factor-2 accelerate periodontal healing of class II furcation defects in dog. The Open Dentistry Journal. 2016;10(1):347–359. doi: 10.2174/1874210601610010347.
    1. Liebermann D. A., Tront J. S., Sha X., Mukherjee K., Mohamed-Hadley A., Hoffman B. Gadd45 stress sensors in malignancy and leukemia. Critical Reviews in Oncogenesis. 2011;16(1–2):129–140. doi: 10.1615/critrevoncog.v16.i1-2.120.
    1. Hyka-Nouspikel N., Desmarais J., Gokhale P. J., et al. Deficient DNA damage response and cell cycle checkpoints lead to accumulation of point mutations in human embryonic stem cells. Stem Cells. 2012;30(9):1901–1910. doi: 10.1002/stem.1177.
    1. Zhao Y., Lou I. C., Conolly R. B. Computational modeling of signaling pathways mediating cell cycle checkpoint control and apoptotic responses to ionizing radiation-induced DNA damage. Dose-Response. 2012;10(2):251–273. doi: 10.2203/dose-response.11-021.Zhao.
    1. Yan Z., Guo F., Yuan Q., et al. Endometrial mesenchymal stem cells isolated from menstrual blood repaired epirubicin-induced damage to human ovarian granulosa cells by inhibiting the expression of Gadd45b in cell cycle pathway. Stem Cell Research & Therapy. 2019;10(1):4–10. doi: 10.1186/s13287-018-1101-0.
    1. Kao A. P., Wang K. H., Chang C. C., et al. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertility and Sterility. 2011;95(4):1308–1315.e1. doi: 10.1016/j.fertnstert.2010.09.064.
    1. Chan R. W. S., Ng E. H. Y., Yeung W. S. B. Identification of cells with colony-forming activity, self-renewal capacity, and multipotency in ovarian endometriosis. The American Journal of Pathology. 2011;178(6):2832–2844. doi: 10.1016/j.ajpath.2011.02.025.
    1. Tan J., Li P., Wang Q., et al. Autologous menstrual blood-derived stromal cells transplantation for severe Asherman’s syndrome. Human Reproduction. 2016;31(12):2723–2729. doi: 10.1093/humrep/dew235.
    1. Domnina A., Novikova P., Obidina J., et al. Human mesenchymal stem cells in spheroids improve fertility in model animals with damaged endometrium. Stem Cell Research & Therapy. 2018;9(1) doi: 10.1186/s13287-018-0801-9.
    1. Paduano F., Marrelli M., Palmieri F., Tatullo M. CD146 expression influences periapical cyst mesenchymal stem cell properties. Stem Cell Reviews and Reports. 2016;12(5):592–603. doi: 10.1007/s12015-016-9674-4.
    1. Zheng S. X., Wang J., Wang X. L., Ali A., Wu L. M., Liu Y. S. Feasibility analysis of treating severe intrauterine adhesions by transplanting menstrual blood-derived stem cells. International Journal of Molecular Medicine. 2018;41(4):2201–2212. doi: 10.3892/ijmm.2018.3415.
    1. Golestaneh N., Kokkinaki M., Pant D., et al. Pluripotent stem cells derived from adult human testes. Stem Cells and Development. 2009;18(8):1115–1126. doi: 10.1089/scd.2008.0347.
    1. Gobbi A., Fishman M. Platelet-rich plasma and bone marrow-derived mesenchymal stem cells in sports medicine. Sports Medicine and Arthroscopy Review. 2016;24(2):69–73. doi: 10.1097/JSA.0000000000000105.
    1. Wei B., Huang C., Zhao M., et al. Effect of mesenchymal stem cells and platelet-rich plasma on the bone healing of ovariectomized rats. Stem Cells International. 2016;2016:11. doi: 10.1155/2016/9458396.9458396
    1. 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 Research & Therapy. 2019;10(1) doi: 10.1186/s13287-019-1155-7.
    1. Mohamed S., 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):p. 7. doi: 10.3390/biomedicines7010007.
    1. Song D., Zhong Y., Qian C., et al. Human Umbilical Cord Mesenchymal Stem Cells Therapy in Cyclophosphamide- Induced Premature Ovarian Failure Rat Model. BioMed Research International. 2016;2016:13. doi: 10.1155/2016/2517514.
    1. Zhu S. F., Hu H. B., Xu H. Y., et al. Human umbilical cord mesenchymal stem cell transplantation restores damaged ovaries. Journal of Cellular and Molecular Medicine. 2015;19(9):2108–2117. doi: 10.1111/jcmm.12571.
    1. Wang S., Yu L., Sun M., et al. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. BioMed Research International. 2013;2013:12. doi: 10.1155/2013/690491.690491
    1. Elfayomy A. K., Almasry S. M., El-Tarhouny S. A., Eldomiaty M. A. 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):370–382. doi: 10.1016/j.tice.2016.05.001.
    1. Jalalie L., Rezaie M. J., Jalili A., et al. Distribution of the CM-Dil-labeled human umbilical cord vein mesenchymal stem cells migrated to the cyclophosphamide-injured ovaries in C57BL/6 mice. Iranian Biomedical Journal. 2019;23(3):200–208.
    1. 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. Science China Life Sciences. 2018;61(12):1554–1565. doi: 10.1007/s11427-017-9272-2.
    1. 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 Cellular & Developmental Biology - Animal. 2019;55(4):302–311. doi: 10.1007/s11626-019-00337-4.
    1. Li J., Mao Q. X., He J. J., She H. Q., Zhang Z., Yin C. Y. Human umbilical cord mesenchymal stem cells improve the reserve function of perimenopausal ovary via a paracrine mechanism. Stem Cell Research & Therapy. 2017;8(1) doi: 10.1186/s13287-017-0514-5.
    1. Shi Q., Gao J. W., Jiang Y., et al. Differentiation of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells into endometrial cells. Stem Cell Research & Therapy. 2017;8(1) doi: 10.1186/s13287-017-0700-5.
    1. Zhang L., Li Y., Guan C. Y., et al. Therapeutic effect of human umbilical cord-derived mesenchymal stem cells on injured rat endometrium during its chronic phase. Stem Cell Research & Therapy. 2018;9(1) doi: 10.1186/s13287-018-0777-5.
    1. Xin L., Lin X., Pan Y., et al. A collagen scaffold loaded with human umbilical cord-derived mesenchymal stem cells facilitates endometrial regeneration and restores fertility. Acta Biomaterialia. 2019;92:160–171. doi: 10.1016/j.actbio.2019.05.012.
    1. Xu L., Ding L., Wang L., et al. Umbilical cord-derived mesenchymal stem cells on scaffolds facilitate collagen degradation via upregulation of MMP-9 in rat uterine scars. Stem Cell Research & Therapy. 2017;8(1) doi: 10.1186/s13287-017-0535-0.
    1. Yang X., Zhang M., Zhang Y., Li W., Yang B. Mesenchymal stem cells derived from Wharton jelly of the human umbilical cord ameliorate damage to human endometrial stromal cells. Fertility and Sterility. 2011;96(4):1029–1036.e4. doi: 10.1016/j.fertnstert.2011.07.005.
    1. Fan D., Wu S., Ye S., Wang W., Guo X., Liu Z. Umbilical cord mesenchyme stem cell local intramuscular injection for treatment of uterine niche. Medicine. 2017;96(44):p. e8480. doi: 10.1097/MD.0000000000008480.
    1. 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 Research & Therapy. 2018;9(1):1–10. doi: 10.1186/s13287-018-0904-3.

Source: PubMed

3
订阅