Stem Cell Reviews and Reports

, Volume 14, Issue 1, pp 1–12 | Cite as

Mesenchymal Stem Cells (MSCs) Therapy for Recovery of Fertility: a Systematic Review

  • Zahra FazeliEmail author
  • Atieh Abedindo
  • Mir Davood Omrani
  • Sayyed Mohammad Hossein Ghaderian


In recent years, the mesenchymal stem cells (MSCs) have provided the new opportunities to treat different disorders including infertility. Different studies have suggested that the MSCs have ability to differentiate into germ-like cells under specific induction conditions as well as transplantation to gonadal tissues. The aim of this systematic review was to evaluate the results obtained from different studies on MSCs therapy for promoting fertility. This search was done in PubMed and Science Direct databases using key words MSCs, infertility, therapy, germ cell, azoospermia, ovarian failure and mesenchymal stem cell. Among the more than 11,400 papers, 53 studies were considered eligible for more evaluations. The obtained results indicated that the most studies were performed on MSCs derived from bone marrow and umbilical cord as compared with the other types of MSCs. Different evaluations on animal models as well as in vitro studies supported from their role in the recovery of spermatogenesis and folliculogenesis. Although the data obtained from this systematic review are promising, but the further studies need to assess the efficiency and safety of transplantation of these cells in fertility recovery.


Stem cell therapy Mesenchymal stem cell Infertility Treatment 


Compliance with Ethical Standards


This research did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Boivin, J., Bunting, L., Collins, J. A., & Nygren, K. G. (2007). International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Human Reproduction, 22(6), 1506–1512.CrossRefPubMedGoogle Scholar
  2. 2.
    Miyamoto, T., Tsujimura, A., Miyagawa, Y., Koh, E., Namiki, M., & Sengoku, K. (2012). Male infertility and its causes in human. Advances in Urology, 2012, 384520.CrossRefPubMedGoogle Scholar
  3. 3.
    Miyamoto, T., Minase, G., Okabe, K., Ueda, H., & Sengoku, K. (2015). Male infertility and its genetic causes. The Journal of Obstetrics and Gynaecology Research, 41(10), 1501–1505.CrossRefPubMedGoogle Scholar
  4. 4.
    Farquhar, C., Rishworth, J. R., Brown, J., Nelen, W. L., & Marjoribanks, J. (2015). Assisted reproductive technology: an overview of cochrane reviews. Cochrane Database of Systematic Reviews, (7):CD010537.Google Scholar
  5. 5.
    Nayernia, K., Lee, J. H., Drusenheimer, N., Nolte, J., Wulf, G., Dressel, R., Gromoll, J., & Engel, W. (2006). Derivation of male germ cells from bone marrow stem cells. Laboratory Investigation, 86(7), 654–663.CrossRefPubMedGoogle Scholar
  6. 6.
    Ghasemzadeh-Hasankolaei, M., Sedighi-Gilani, M. A., & Eslaminejad, M. B. (2014). Induction of ram bone marrow mesenchymal stem cells into germ cell lineage using transforming growth factor-β superfamily growth factors. Reproduction in Domestic Animals, 49(4), 588–598.CrossRefPubMedGoogle Scholar
  7. 7.
    Ghasemzadeh-Hasankolaei, M., Eslaminejad, M. B., Batavani, R., & Sedighi-Gilani, M. (2014). Comparison of the efficacy of three concentrations of retinoic acid for transdifferentiation induction in sheep marrow-derived mesenchymal stem cells into male germ cells. Andrologia, 46(1), 24–35.CrossRefPubMedGoogle Scholar
  8. 8.
    Cakici, C., Buyrukcu, B., Duruksu, G., Haliloglu, A. H., Aksoy, A., Isık, A., Uludag, O., Ustun, H., Subası, C., & Karaoz, E. (2013). Recovery of fertility in azoospermia rats after injection of adipose-tissue-derived mesenchymal stem cells: the sperm generation. Biomed Research International, 2013, 529589.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Tamadon, A., Mehrabani, D., Rahmanifar, F., Jahromi, A. R., Panahi, M., Zare, S., Khodabandeh, Z., Jahromi, I. R., Tanideh, N., Dianatpour, M., & Ramzi, M., Koohi Hoseinabadi O (2015). Induction of spermatogenesis by bone marrow-derived mesenchymal stem cells in busulfan-induced azoospermia in hamster. International Journal of Stem Cells, 8(2), 134–145.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K., & Daley, G. Q. (2004). Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature, 427(6970), 148–154.CrossRefPubMedGoogle Scholar
  11. 11.
    Hua, J., Pan, S., Yang, C., Dong, W., Dou, Z., & Sidhu, K. S. (2009). Derivation of male germ cell-like lineage from human fetal bone marrow stem cells. Reproductive Biomedicine Online, 19(1), 99–105.CrossRefPubMedGoogle Scholar
  12. 12.
    Dyce, P. W., Liu, J., Tayade, C., Kidder, G. M., Betts, D. H., & Li, J. (2011). In vitro and in vivo germ line potential of stem cells derived from newborn mouse skin. PLoS One, 6(5), e20339.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Young, H. E., & Black, A. C. Jr. (2004). Adult stem cells. The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology, 276(1), 75–102.CrossRefPubMedGoogle Scholar
  14. 14.
    Wood, A. (2005). Ethics and embryonic stem cell research. Stem Cell Reviews, 1(4), 317–324.CrossRefPubMedGoogle Scholar
  15. 15.
    Hyun, I. (2010). The bioethics of stem cell research and therapy. The Journal of Clinical Investigation, 120(1), 71–75.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Cyranoski, D. (2013). Stem cells boom in vet clinics. Nature, 496(7444), 148–149.CrossRefPubMedGoogle Scholar
  17. 17.
    Liu, J., Yu, F., Sun, Y., Jiang, B., Zhang, W., Yang, J., Xu, G. T., Liang, A., & Liu, S. (2015). Concise reviews: characteristics and potential applications of human dental tissue-derived mesenchymal stem cells. Stem Cells, 33(3), 627–638.CrossRefPubMedGoogle Scholar
  18. 18.
    Patel, D. M., Shah, J., & Srivastava, A. S. (2013). Therapeutic potential of mesenchymal stem cells in regenerative medicine. Stem Cells International, 2013, 496218.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Fazeli, Z., Omrani, M. D., & Ghaderian, S. M. (2016). CD29/CD184 expression analysis provides a signature for identification of neuronal like cells differentiated from PBMSCs. Neuroscience Letters, 630, 189 93.CrossRefPubMedGoogle Scholar
  20. 20.
    Joyce, N., Annett, G., Wirthlin, L., Olson, S., Bauer, G., & Nolta, J. A. (2010). Mesenchymal stem cells for the treatment of neurodegenerative disease. Regenerative Medicine, 5(6), 933–946.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Martino, G., Franklin, R. J., Baron Van Evercooren A., & Kerr, D. A. (2010). Stem cells in multiple sclerosis (STEMS) consensus group. Stem cell transplantation in multiple sclerosis: current status and future prospects. Nature Reviews Neurology, 6(5), 247–255.Google Scholar
  22. 22.
    Liang, X., Ding, Y., Zhang, Y., Tse, H. F., & Lian, Q. (2014). Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplantation, 23(9), 1045–1059.CrossRefPubMedGoogle Scholar
  23. 23.
    da Silva Meirelles, L., Chagastelles, P. C., & Nardi, N. B. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. Journal of Cell Science, 119(Pt 11), 2204–2213.CrossRefPubMedGoogle Scholar
  24. 24.
    Amarnath, S., Foley, J. E., Farthing, D. E., Gress, R. E., Laurence, A., Eckhaus, M. A., Métais, J. Y., Rose, J. J., Hakim, F. T., Felizardo, T. C., Cheng, A. V., Robey, P. G., Stroncek, D. E., Sabatino, M., Battiwalla, M., Ito, S., Fowler, D. H., & Barrett, A. J. (2015). Bone marrow-derived mesenchymal stromal cells harness purinergenic signaling to tolerize human Th1 cells in vivo. Stem Cells, 33(4), 1200–1212.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Smith, C. L., Chaichana, K. L., Lee, Y. M., Lin, B., Stanko, K. M., O’Donnell, T., Gupta, S., Shah, S. R., Wang, J., Wijesekera, O., Delannoy, M., Levchenko, A., & Quiñones-Hinojosa, A. (2015). Pre-exposure of human adipose mesenchymal stem cells to soluble factors enhances their homing to brain cancer. Stem Cells Translational Medicine, 4(3), 239–251.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bourzac, C. A., Koenig, J. B., Link, K. A., Nykamp, S. G., & Koch, T. G. (2014). Evaluation of ultrasmall superparamagnetic iron oxide contrast agent labeling of equine cord blood and bone marrow mesenchymal stromal cells. American Journal of Veterinary Research, 75(11), 1010–1017.CrossRefPubMedGoogle Scholar
  27. 27.
    Shi, W., Nie, D., Jin, G., Chen, W., Xia, L., Wu, X., Su, X., Xu, X., Ni, L., Zhang, X., Zhang, X., & Chen, J. (2012). BDNF blended chitosan scaffolds for human umbilical cord MSC transplants in traumatic brain injury therapy. Biomaterials, 33(11), 3119–3126.CrossRefPubMedGoogle Scholar
  28. 28.
    Krstić, J., Obradović, H., Jauković, A., Okić-Đorđević, I., Trivanović, D., Kukolj, T., Mojsilović, S., Ilić, V., Santibañez, J. F., & Bugarski, D. (2015). Urokinase type plasminogen activator mediates interleukin-17-induced peripheral blood mesenchymal stem cell motility and transendothelial migration. Biochimica et Biophysica Acta, 1853(2), 431–444.CrossRefPubMedGoogle Scholar
  29. 29.
    Zhou, K., Xia, M., Tang, B., Yang, D., Liu, N., Tang, D., Xie, H., Wang, X., Zhu, H., Liu, C., & Zuo, C. (2016). Isolation and comparison of mesenchymal stem cell like cells derived from human gastric cancer tissues and corresponding ovarian metastases. Molecular Medicine Reports, 13(2), 1788–1794.CrossRefPubMedGoogle Scholar
  30. 30.
    Chikhovskaya, J. V., van Daalen, S. K., Korver, C. M., Repping, S., & van Pelt, A. M. (2014). Mesenchymal origin of multipotent human testis-derived stem cells in human testicular cell cultures. Molecular Human Reproduction, 20(2), 155–167.CrossRefPubMedGoogle Scholar
  31. 31.
    Lai, D., Wang, F., Yao, X., Zhang, Q., Wu, X., & Xiang, C. (2015). 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, 13, 155.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Fazeli, Z., Rajabibazl, M., Salami, S., Vazifeh Shiran, N., Ghaderian, S. M. H., & Omrani, M. D. (2016). Gene expression profile of adherent cells derived from human peripheral blood: evidence of mesenchymal stem cells. Journal of Sciences, Islamic Republic of Iran, 27(2), 105–112.Google Scholar
  33. 33.
    Chikhovskaya, J. V., Jonker, M. J., Meissner, A., Breit, T. M., Repping, S., & van Pelt, A. M. (2012). Human testis-derived embryonic stem cell-like cells are not pluripotent, but possess potential of mesenchymal progenitors. Human Reproduction, 27(1), 210–221.CrossRefPubMedGoogle Scholar
  34. 34.
    Sriraman, K., Bhartiya, D., Anand, S., & Bhutda, S. (2015). Mouse ovarian very small embryonic-like stem cells resist chemotherapy and retain ability to initiate oocyte-specific differentiation. Reproductive Sciences, 22(7), 884–903.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kurkure, P., Prasad, M., Dhamankar, V., & Bakshi, G. (2015). Very small embryonic-like stem cells (VSELs) detected in azoospermic testicular biopsies of adult survivors of childhood cancer. Reproductive Biology and Endocrinology, 13, 122.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Dezawa, M. (2016). Muse cells provide the pluripotency of mesenchymal stem cells: direct contribution of muse cells to tissue regeneration. Cell Transplantation, 25(5), 849–861.CrossRefPubMedGoogle Scholar
  37. 37.
    Fang, J., Wei, Y., Lv, C., Peng, S., Zhao, S., & Hua, J. (2017). CD61 promotes the differentiation of canine ADMSCs into PGC-like cells through modulation of TGF-β signaling. Science Reports, 7, 43851.CrossRefGoogle Scholar
  38. 38.
    Shlush, E., Maghen, L., Swanson, S., Kenigsberg, S., Moskovtsev, S., Barretto, T., Gauthier-Fisher, A., & Librach, C. L. (2017). In vitro generation of sertoli-like and haploid spermatid-like cells from human umbilical cord perivascular cells. Stem Cell Research & Therapy, 8(1), 37.CrossRefGoogle Scholar
  39. 39.
    Abd Allah, S. H., Pasha, H. F., Abdelrahman, A. A., & Mazen, N. F. (2017). Molecular effect of human umbilical cord blood CD34-positive and CD34-negative stem cells and their conjugate in azoospermic mice. Molecular and Cellular Biochemistry, 428(1–2), 179–191.CrossRefPubMedGoogle Scholar
  40. 40.
    Asgari, H. R., Akbari, M., Yazdekhasti, H., Rajabi, Z., Navid, S., Aliakbari, F., Abbasi, N., Aval, F. S., Shams, A., & Abbasi, M. (2017). Comparison of human amniotic, chorionic, and umbilical cord multipotent mesenchymal stem cells regarding their capacity for differentiation toward female germ cells. Cellular Reprogramming, 19(1), 44–53.CrossRefPubMedGoogle Scholar
  41. 41.
    Maghen, L., Shlush, E., Gat, I., Filice, M., Barretto, T., Jarvi, K., Lo, K., Gauthier-Fisher, A. S., & Librach, C. L. (2016). Human umbilical perivascular cells: a novel source of MSCs to support testicular niche regeneration. Reproduction.Google Scholar
  42. 42.
    Afsartala, Z., Rezvanfar, M. A., Hodjat, M., Tanha, S., Assadollahi, V., Bijangi, K., Abdollahi, M., & Ghasemzadeh-Hasankolaei, M. (2016). Amniotic membrane mesenchymal stem cells can differentiate into germ cells in vitro. In Vitro Cellular and Developmental Biology - Animal, 52(10), 1060–1071.CrossRefPubMedGoogle Scholar
  43. 43.
    Ghasemzadeh-Hasankolaei, M., Batavani, R., Eslaminejad, M. B., & Sayahpour, F. (2016). Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. International Journal of Stem Cells, 9(2), 250–263.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Ghasemzadeh-Hasankolaei, M., Eslaminejad, M. B., & Sedighi-Gilani, M. (2016). Derivation of male germ cells from ram bone marrow mesenchymal stem cells by three different methods and evaluation of their fate after transplantation into the testis. In Vitro Cellular and Developmental Biology - Animal, 52(1), 49–61.CrossRefPubMedGoogle Scholar
  45. 45.
    Nejad, N. A., Amidi, F., Hoseini, M. A., Nia, K. N., Habibi, M., Kajbafzadeh, A. M., Mazaheri, Z., & Yamini, N. (2015). Male germ-like cell differentiation potential of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells in co-culture with human placenta cells in presence of BMP4 and retinoic acid. Iranian Journal of Basic Medical Sciences, 18(4), 325–333.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Hassan, A. I., & Alam, S. S. (2014). Evaluation of mesenchymal stem cells in treatment of infertility in male rats. Stem Cell Research & Therapy, 5(6), 131.CrossRefGoogle Scholar
  47. 47.
    Yang, R. F., Liu, T. H., Zhao, K., & Xiong, C. L. (2014). Enhancement of mouse germ cell-associated genes expression by injection of human umbilical cord mesenchymal stem cells into the testis of chemical-induced azoospermic mice. Asian Journal of Andrology, 16(5), 698–704.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hua, J., Yu, H., Dong, W., Yang, C., Gao, Z., Lei, A., Sun, Y., Pan, S., Wu, Y., & Dou, Z. (2009). Characterization of mesenchymal stem cells (MSCs) from human fetal lung: potential differentiation of germ cells. Tissue and Cell, 41(6), 448–455.CrossRefPubMedGoogle Scholar
  49. 49.
    Hsiao, C. H., Ji, A. T., Chang, C. C., Cheng, C. J., Lee, L. M., & Ho, J. H. (2015). Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury. Stem Cell Research & Therapy, 6, 113.CrossRefGoogle Scholar
  50. 50.
    Song, D., Zhong, Y., Qian, C., Zou, Q., Ou, J., Shi, Y., Gao, L., Wang, G., Liu, Z., Li, H., Ding, H., Wu, H., Wang, F., Wang, J., & Li, H. (2016). Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. Biomed Research International, 2016, 2517514.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Amidi, F., Ataie Nejad, N., Agha Hoseini, M., Nayernia, K., Mazaheri, Z., Yamini, N., & Saeednia, S. (2015). In vitro differentiation process of human Wharton’s jelly mesenchymal stem cells to male germ cells in the presence of gonadal and non-gonadal conditioned media with retinoic acid. In Vitro Cellular and Developmental Biology - Animal, 51(10), 1093–1101.CrossRefPubMedGoogle Scholar
  52. 52.
    Chen, H., Tang, Q. L., Wu, X. Y., Xie, L. C., Lin, L. M., Ho, G. Y., & Ma, L. (2015). Differentiation of human umbilical cord mesenchymal stem cells into germ-like cells in mouse seminiferous tubules. Molecular Medicine Reports, 12(1), 819–828.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Asgari, H. R., Akbari, M., Abbasi, M., Ai, J., Korouji, M., Aliakbari, F., Babatunde, K. A., Aval, F. S., & Joghataei, M. T. (2015). Human Wharton’s jelly-derived mesenchymal stem cells express oocyte developmental genes during co-culture with placental cells. Iranian Jouranl of Basic Medical Sciences, 18(1), 22–29.Google Scholar
  54. 54.
    Xie, L., Lin, L., Tang, Q., Li, W., Huang, T., Huo, X., Liu, X., Jiang, J., He, G., & Ma, L. (2015). Sertoli cell-mediated differentiation of male germ cell-like cells from human umbilical cord Wharton’s jelly-derived mesenchymal stem cells in an in vitro co-culture system. European Journal of Medical Research, 20, 9.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Zhang, D., Liu, X., Peng, J., He, D., Lin, T., Zhu, J., Li, X., Zhang, Y., & Wei, G. (2014). Potential spermatogenesis recovery with bone marrow mesenchymal stem cells in an azoospermic rat model. International Journal of Molecular Sciences, 15(8), 13151–13165.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Hosseinzadeh Shirzeily, M., Pasbakhsh, P., Amidi, F., Mehrannia, K., & Sobhani, A. (2013). Comparison of differentiation potential of male mouse adipose tissue and bone marrow derived-mesenchymal stem cells into germ cells. Iranian Journal of Reproductive Medicine, 11(12), 965–976.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Kaviani, M., Ezzatabadipour, M., Nematollahi-Mahani, S. N., Salehinejad, P., Mohammadi, M., Kalantar, S. M., & Motamedi, B. (2014). Evaluation of gametogenic potential of vitrified human umbilical cord Wharton’s jelly-derived mesenchymal cells. Cytotherapy, 16(2), 203–312.CrossRefPubMedGoogle Scholar
  58. 58.
    Sabbaghi, M. A., Bahrami, A. R., Feizzade, B., Kalantar, S. M., Matin, M. M., Kalantari, M., Aflatoonian, A., & Saeinasab, M. (2012). Trial evaluation of bone marrow derived mesenchymal stem cells (MSCs) transplantation in revival of spermatogenesis in testicular torsion. Middle East Fertility Society Journal, 17(4), 243–249.CrossRefGoogle Scholar
  59. 59.
    Abd-Allah, S. H., Shalaby, S. M., Pasha, H. F., El-Shal, A. S., Raafat, N., Shabrawy, S. M., Awad, H. A., Amer, M. G., Gharib, M. A., El Gendy, E. A., Raslan, A. A., & El-Kelawy, H. M. (2013). Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy, 15(1), 64–75.CrossRefPubMedGoogle Scholar
  60. 60.
    Wang, F., Zhang, S.H.-S.H., Liu, W.-S.H., & Hua, J.-L. (2013). Transplantation of goat bone marrow mesenchymal stem cells (gMSCs) help restore spermatogenesis in endogenous germ cells-depleted mouse models. Journal of Integrative Agriculture, 12(3), 483–494.CrossRefGoogle Scholar
  61. 61.
    Hou, L., Dong, Q., Wu, Y. J., Sun, Y. X., Guo, Y. Y., & Huo, Y. H. (2016). Gonadotropins facilitate potential differentiation of human bone marrow mesenchymal stem cells into Leydig cells in vitro. The Kaohsiung Journal of Medical Sciences, 32(1), 1–9.CrossRefPubMedGoogle Scholar
  62. 62.
    Jouni, F. J., Abdolmaleki, P., Behmanesh, M., & Movahedin, M. (2014). An in vitro study of the impact of 4mT static magnetic field to modify the differentiation rate of rat bone marrow stem cells into primordial germ cells. Differentiation, 87(5), 230–237.CrossRefPubMedGoogle Scholar
  63. 63.
    Mokarizadeh, A., Rezvanfar, M. A., Dorostkar, K., & Abdollahi, M. (2013). Mesenchymal stem cell derived microvesicles: trophic shuttles for enhancement of sperm quality parameters. Reproductive Toxicology, 42, 78–84.CrossRefPubMedGoogle Scholar
  64. 64.
    Fu, X., He, Y., Xie, C., & Liu, W. (2008). Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage. Cytotherapy, 10(4), 353–363.CrossRefPubMedGoogle Scholar
  65. 65.
    Elfayomy, A. K., Almasry, S. M., El-Tarhouny, S. A., & Eldomiaty, M. A. (2016). 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 and Cell, 48(4), 370–382.CrossRefPubMedGoogle Scholar
  66. 66.
    Mehrabani, D., Hassanshahi, M. A., Tamadon, A., Zare, S., Keshavarz, S., Rahmanifar, F., Dianatpour, M., Khodabandeh, Z., Jahromi, I., Tanideh, N., Ramzi, M., Aqababa, H., & Kuhi-Hoseinabadi, O. (2015). Adipose tissue-derived mesenchymal stem cells repair germinal cells of seminiferous tubules of busulfan-induced azoospermic rats. Journal of Human Reproductive Sciences, 8(2), 103–110.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Aghamir, S. M., Salavati, A., Yousefie, R., Tootian, Z., Ghazaleh, N., Jamali, M., & Azimi, P. (2014). Does bone marrow-derived mesenchymal stem cell transfusion prevent antisperm antibody production after traumatic testis rupture? Urology, 84(1), 82–86.CrossRefPubMedGoogle Scholar
  68. 68.
    Cui, G., Qi, Z., Guo, X., Qin, J., Gui, Y., & Cai, Z. (2009). Rat bone marrow derived mesenchymal progenitor cells support mouse ES cell growth and germ-like cell differentiation. Cell Biology International, 33(3), 434–441.CrossRefPubMedGoogle Scholar
  69. 69.
    Anand, S., Bhartiya, D., Sriraman, K., & Mallick, A. (2016). Underlying mechanisms that restore spermatogenesis on transplanting healthy niche cells in busulphan treated mouse testis. Stem Cell Reviews, 12(6), 682–697.CrossRefPubMedGoogle Scholar
  70. 70.
    Wang, Z., Wang, Y., Yang, T., Li, J., & Yang, X. (2017). Study of the reparative effects of menstrual-derived stem cells on premature ovarian failure in mice. Stem Cell Research & Therapy, 8(1), 11.CrossRefGoogle Scholar
  71. 71.
    Li, P. Z., Yan, G. Y., Han, L., Pang, J., Zhong, B. S., Zhang, G. M., Wang, F., & Zhang, Y. L. (2017). Overexpression of STRA8, BOULE, and DAZL genes promotes goat bone marrow-derived mesenchymal stem cells in vitro transdifferentiation toward putative male germ cells. Reproductive Sciences, 24(2), 300–312.CrossRefPubMedGoogle Scholar
  72. 72.
    Wang, S., Yu, L., Sun, M., Mu, S., Wang, C., Wang, D., & Yao, Y. (2013). The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. Biomed Research International, 2013, 690491.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Gan, L., Duan, H., Xu, Q., Tang, Y. Q., Li, J. J., Sun, F. Q., & Wang, S. (2017). Human amniotic mesenchymal stromal cell transplantation improves endometrial regeneration in rodent models of intrauterine adhesions. Cytotherapy, 19(5), 603–616.CrossRefPubMedGoogle Scholar
  74. 74.
    Rahmanifar, F., Tamadon, A., Mehrabani, D., Zare, S., Abasi, S., Keshavarz, S., Dianatpour, M., Khodabandeh, Z., Jahromi, I. R., & Koohi-Hoseinabadi, O. (2016). Histomorphometric evaluation of treatment of rat azoosper-mic seminiferous tubules by allotransplantation of bone marrow-derived mesenchymal stem cells. Iranian Journal of Basic Medical Sciences, 19(6), 653–661.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Liu, T., Huang, Y., Guo, L., Cheng, W., & Zou, G. (2012). 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. International Journal of Medical Sciences, 9(7), 592–602.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Kilic, S., Pinarli, F., Ozogul, C., Tasdemir, N., Naz Sarac, G., & Delibasi, T. (2014). Protection from cyclophosphamide-induced ovarian damage with bone marrow-derived mesenchymal stem cells during puberty. Gynecological Endocrinology, 30(2), 135–140.CrossRefPubMedGoogle Scholar
  77. 77.
    Li, N., Pan, S., Zhu, H., Mu, H., Liu, W., & Hua, J. (2014). BMP4 promotes SSEA-1(+) hUC-MSC differentiation into male germ-like cells in vitro. Cell Proliferation, 47(4), 299–309.CrossRefPubMedGoogle Scholar
  78. 78.
    Li, B., Liu, W., Zhuang, M., Li, N., Wu, S., Pan, S., & Hua, J. (2016). Overexpression of CD61 promotes hUC-MSC differentiation into male germ-like cells. Cell Proliferation, 49(1), 36–47.CrossRefPubMedGoogle Scholar
  79. 79.
    Fouad, H., Sabry, D., Elsetohy, K., & Fathy, N. (2016). Therapeutic efficacy of amniotic membrane stem cells and adipose tissue stem cells in rats with chemically induced ovarian failure. Journal of Advanced Research, 7(2), 233–241.CrossRefPubMedGoogle Scholar
  80. 80.
    Mohamed, S. A., Shalaby, S. M., Abdelaziz, M., Brakta, S., Hill, W. D., Ismail, N., & Al-Hendy, A. (2017). Human mesenchymal stem cells partially reverse infertility in chemotherapy-induced ovarian failure. Reproductive Sciences 1933719117699705.Google Scholar
  81. 81.
    Liu, J., Zhang, H., Zhang, Y., Li, N., Wen, Y., Cao, F., Ai, H., & Xue, X. (2014). Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Molecules and Cells, 37(12), 865–872.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Lai, D., Wang, F., Dong, Z., & Zhang, Q. (2014). Skin-derived mesenchymal stem cells help restore function to ovaries in a premature ovarian failure mouse model. PLoS One, 9(5), e98749.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Liu, T., Huang, Y., Zhang, J., Qin, W., Chi, H., Chen, J., Yu, Z., & Chen, C. (2014). Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells and Development, 23(13), 1548–1557.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Wei, Y., Fang, J., Cai, S., Lv, C., Zhang, S., & Hua, J. (2016). Primordial germ cell-like cells derived from canine adipose mesenchymal stem cells. Cell Proliferation, 49(4), 503–511.CrossRefPubMedGoogle Scholar
  85. 85.
    Vahdati, A., Fathi, A., Hajihoseini, M., Aliborzi, G., & Hosseini, E. (2017). The regenerative effect of bone marrow-derived stem cells in spermatogenesis of infertile hamster. World Journal of Plastic Surgery, 6(1), 18–25.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Yan, G., Fan, Y., Li, P., Zhang, Y., & Wang, F. (2015). Ectopic expression of DAZL gene in goat bone marrow-derived mesenchymal stem cells enhances the trans-differentiation to putative germ cells compared to the exogenous treatment of retinoic acid or bone morphogenetic protein 4 signalling molecules. Cell Biology International, 39(1), 74–83.CrossRefPubMedGoogle Scholar
  87. 87.
    Rothschild, G., Sottas, C. M., Kissel, H., Agosti, V., Manova, K., Hardy, M. P., & Besmer, P. (2003). A role for kit receptor signaling in Leydig cell steroidogenesis. Biology of Reproduction, 69(3), 925–932.CrossRefPubMedGoogle Scholar
  88. 88.
    Silvestris, E., D’Oronzo, S., Cafforio, P., D’Amato, G., & Loverro, G. (2015). Perspective in infertility: the ovarian stem cells. Journal of Ovarian Research, 8, 55.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Bukovsky, A., Virant-Klun, I., Svetlikova, M., & Willson, I. (2006). Ovarian germ cells. Methods in Enzymology, 419, 208–258.CrossRefPubMedGoogle Scholar
  90. 90.
    Goossens, E., & Tournaye, H. (2006). Testicular stem cells. Seminars in Reproductive Medicine, 24(5), 370–378.CrossRefPubMedGoogle Scholar
  91. 91.
    Schlatt, S., Ehmcke, J., & Jahnukainen, K. (2009). Testicular stem cells for fertility preservation: preclinical studies on male germ cell transplantation and testicular grafting. Pediatric Blood and Cancer, 53(2), 274–280.CrossRefPubMedGoogle Scholar
  92. 92.
    Ge, W., Chen, C., De Felici, M., & Shen, W. (2015). In vitro differentiation of germ cells from stem cells: a comparison between primordial germ cells and in vitro derived primordial germ cell-like cells. Cell Death & Disease, 6, e1906.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Zahra Fazeli
    • 1
    Email author
  • Atieh Abedindo
    • 1
  • Mir Davood Omrani
    • 1
    • 2
  • Sayyed Mohammad Hossein Ghaderian
    • 1
    • 2
  1. 1.Department of Medical Genetics, Faculty of MedicineShahid Beheshti University of Medical SciencesTehranIran
  2. 2.Urogenital Stem Cell Research CenterShahid Beheshti University of Medical SciencesTehranIran

Personalised recommendations