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Stem Cell Reviews and Reports

, Volume 13, Issue 6, pp 741–756 | Cite as

Eminent Sources of Adult Mesenchymal Stem Cells and Their Therapeutic Imminence

  • Dannie Macrin
  • Joel P. Joseph
  • Aruthra Arumugam Pillai
  • Arikketh Devi
Article

Abstract

In the recent times, stem cell biology has garnered the attention of the scientific fraternity and the general public alike due to the immense therapeutic potential that it holds in the field of regenerative medicine. A breakthrough in this direction came with the isolation of stem cells from human embryo and their differentiation into cell types of all three germ layers. However, the isolation of mesenchymal stem cells from adult tissues proved to be advantageous over embryonic stem cells due to the ethical and immunological naivety. Mesenchymal Stem Cells (MSCs) isolated from the bone marrow were found to differentiate into multiple cell lineages with the help of appropriate differentiation factors. Furthermore, other sources of stem cells including adipose tissue, dental pulp, and breast milk have been identified. Newer sources of stem cells have been emerging recently and their clinical applications are also being studied. In this review, we examine the eminent sources of Mesenchymal Stem Cells (MSCs), their immunophenotypes, and therapeutic imminence.

Keywords

Mesenchymal stem cells Therapeutic potential Cell lineages Differentiation factors Immunophenotype 

Notes

Acknowledgements

The authors acknowledge the assistance of Jismi Elsa Abraham in drawing the figure that depicts the eminent sources of stem cells and their differentiation potential.

Compliance with Ethical Standards

Conflict of Interest

The authors have no conflict of interest to declare.

References

  1. 1.
    Hipp, J., & Atala, A. (2008). Sources of stem cells for regenerative medicine. (February):3–11.Google Scholar
  2. 2.
    Martin, G. R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proceedings of the National Academy of Sciences of the United States of America, 78(12), 7634–7638.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Evans, M. J., & Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature, 292(5819), 154–156.PubMedCrossRefGoogle Scholar
  4. 4.
    Thomson, J. A., Itskovitz-eldor, J., Shapiro, S. S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282(1998), 1145–1148.PubMedCrossRefGoogle Scholar
  5. 5.
    Yabut, O., & Bernstein, H. S. (2011). Human embryonic stem cells in regenerative medicine. In Tissue engineering in regenerative medicine, p. 17–38.Google Scholar
  6. 6.
    Niclis, J. C., Trounson, A. O., Dottori, M., et al. (2009). Human embryonic stem cell models of Huntington disease. Reproductive Biomedicine Online, 19(1), 106–113.PubMedCrossRefGoogle Scholar
  7. 7.
    Verlinsky, Y., Strelchenko, N., Kukharenko, V., et al. (2005). Human embryonic stem cell lines with genetic disorders. Reproductive Biomedicine Online, 10(1), 105–110.PubMedCrossRefGoogle Scholar
  8. 8.
    Rugg-Gunn, P. J., Ferguson-Smith, A. C., & Pedersen, R. A. (2005). Human embryonic stem cells as a model for studying epigenetic regulation during early development. Cell Cycle, 4(10), 1323–1326.PubMedCrossRefGoogle Scholar
  9. 9.
    Swijnenburg, R. J., Tanaka, M., Vogel, H., et al. (2005). Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation, 112, 166–173.Google Scholar
  10. 10.
    Quartu, M., Serra, M., Boi, M., et al. (2008). Polysialylated-neural cell adhesion molecule (PSA-NCAM) in the human trigeminal ganglion and brainstem at prenatal and adult ages. BMC Neuroscience, 9(1), 108.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Jaiswal, R. K., Jaiswal, N., Bruder, S. P., Mbalaviele, G., Marshak, D. R., & Pittenger, M. F. (2000). Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase *. The Journal of Biological Chemistry, 275(13), 9645–9652.PubMedCrossRefGoogle Scholar
  12. 12.
    Yen, B. L., Huang, H., Chien, C., et al. (2005). Isolation of multipotent cells from human term. Placenta, 161, 3–9.Google Scholar
  13. 13.
    Civin, C. I. (2002). Commitment to biomedical research: clearing unnecessary impediments to progress. Stem Cells, 20, 482–484.PubMedCrossRefGoogle Scholar
  14. 14.
    Kurtzberg, J., Laughlin, M., Graham, M. L., et al. (1996). Placental blood as a source of hematopoietic stem cells for transplantation into unrelated recipients. The New England Journal of Medicine, 335(3), 157–166.PubMedCrossRefGoogle Scholar
  15. 15.
    Lee, O. K., Kuo, T. K., Chen, W., Lee, K., Hsieh, S., & Chen, T. (2015). Isolation of multipotent mesenchymal stem cells from umbilical cord blood. 103(5), 1669–1676.Google Scholar
  16. 16.
    Bieback, K., Kern, S., Klutter, H., & Eichler, H. (2004). Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells, 22, 625–634.PubMedCrossRefGoogle Scholar
  17. 17.
    Swamynathan, P., Venugopal, P., Kannan, S., et al. (2014) Are serum-free and xeno-free culture conditions ideal for large scale clinical grade expansion of Wharton’ s jelly derived mesenchymal stem cells? A comparative study.Google Scholar
  18. 18.
    Lu, L., Zhao, Q., Wang, X., et al. (2006). Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica, 91, 1017–1026.PubMedGoogle Scholar
  19. 19.
    Tsai, M., Hwang, S., Tsai, Y., Cheng, F., & Lee, J. (2006). Clonal amniotic fluid-derived stem cells express characteristics of both mesenchymal and neural stem cells 1. 551(August 2005), 545–551.Google Scholar
  20. 20.
    Yu, X., Wang, N., Qiang, R., et al. (2014). Human amniotic fluid stem cells possess the potential to differentiate into primordial follicle oocytes in vitro 1 running title: oocyte-like cells from hAFSCs. Society Study Reproduction.Google Scholar
  21. 21.
    Banas, A., Teratani, T., Yamamoto, Y., et al. (2007). Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. 219–228.Google Scholar
  22. 22.
    Nakagami, H., Morishita, R., Maeda, K., Kikuchi, Y., & Ogihara, T. (2006). Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. Journal of Atherosclerosis and Thrombosis, 13(2), 77–81.PubMedCrossRefGoogle Scholar
  23. 23.
    Fraser, J. K., Wulur, I., Alfonso, Z., & Hedrick, M. H. (2006). Fat tissue: an underappreciated source of stem cells for biotechnology. Trends in Biotechnology, 24(4), 150–154.PubMedCrossRefGoogle Scholar
  24. 24.
    Zuk, P. A., Zhu, M., Ashjian, P., et al. (2002). Human adipose tissue is a source of multipotent stem cells. 13, 4279–4295.Google Scholar
  25. 25.
    Telles, P. D., Aparecida, M., Moreira, D. A., Sakai, V. T., & Nör, J. E. (2011). Pulp tissue from primary teeth: new source of stem cells. 19(3), 189–194.Google Scholar
  26. 26.
    Arthur, A., Rychkov, G., Shi, S., Koblar, S. A., & Gronthos, S. (2008). Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells, 26, 1787–1795.PubMedCrossRefGoogle Scholar
  27. 27.
    Kerkis, I., & Caplan, A. I. (2012). Stem cells in dental pulp of deciduous teeth. Tissue Engineering, 18(2).Google Scholar
  28. 28.
    Hosseini, S. M., Talaei-khozani, T., & Sani, M., Owrangi, B. (2014). Differentiation of human breast-milk stem cells to neural stem cells and neurons. 2014.Google Scholar
  29. 29.
    Hassiotou, F., Beltran, A., Chetwynd, E., Stuebe, A. M., Twigger, A. J., Metzger, P., Trengove, N., Lai, C. T., Filgueira, L., Blancafort, P., & Hartmann, P. E. (2012). Breastmilk is a novel source of stem cells with multilineage differentiation potential. Stem Cells, 30, 2164–2174.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Fan, Y., Chong, Y. S., Choolani, M. A., Cregan, M. D., & Chan, J. K. Y. (2010). Unravelling the mystery of stem / progenitor cells in human breast milk. PLoS One, 5(12).Google Scholar
  31. 31.
    Ogata, Y., Mabuchi, Y., Yoshida, M., Suto, E. G., & Suzuki, N. (2015). Purified human synovium mesenchymal stem cells as a good resource for cartilage regeneration. PLoS One, 5–9.Google Scholar
  32. 32.
    Baksh, D., Song, L., & Tuan, R. S. (2004). Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. 8(3), 301–316.Google Scholar
  33. 33.
    Yu, J., He, H., Tang, C., et al. (2010). Differentiation potential of STRO-1 + dental pulp stem cells changes during cell passaging. BMC Cell Biology.Google Scholar
  34. 34.
    Kang, Y., Kim, S., Bishop, J., Khademhosseini, A., & Yang, Y. (2012). The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and b -TCP scaffold. Biomaterials, 33(29), 6998–7007. doi: 10.1016/j.biomaterials.2012.06.061.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Brar, G. S., Sher, R., & Toor, S. (2012). Dental stem cells: dentinogenic, osteogenic, and neurogenic differentiation and its clinical cell based therapies. Indian Journal of Dental Research, 23(3), 393–397.PubMedCrossRefGoogle Scholar
  36. 36.
    Roya, M., & Ai, J. (2015). Differentiation of human endometrial stem cells into germ cell – like cell in fibrin scaffold. Journal of Medical Hypotheses Ideas, 9(2), 90–93. doi: 10.1016/j.jmhi.2015.09.001.CrossRefGoogle Scholar
  37. 37.
    Ilancheran, S., Moodley, Y., & Manuelpillai, U. (2009). Human fetal membranes: a source of stem cells for tissue regeneration and repair? AS. Placenta, 30(1), 2–10. doi: 10.1016/j.placenta.2008.09.009.PubMedCrossRefGoogle Scholar
  38. 38.
    Jackson, K. A., Majka, S. M., Wang, H., et al. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. The Journal of Clinical Investigation, 107(11), 1355–1356.CrossRefGoogle Scholar
  39. 39.
    Wang, G., Bunnell, B. A., Painter, R. G., et al. (2005). Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis. 102(1).Google Scholar
  40. 40.
    Kale, S., Karihaloo, A., Clark, P. R., Kashgarian, M., Krause, D. S., & Cantley, L. G. (2003). Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. 112(1).Google Scholar
  41. 41.
    Orlic, D., Kajstura, J., Chimenti, S., et al. (2001). Bone marrow cells regenerate infarcted myocardium. 410(April), 701–705.Google Scholar
  42. 42.
    Kao, S., Shyu, J., Wang, H., et al. (2015). Comparisons of differentiation potential in human mesenchymal stem cells from Wharton’ s jelly, bone marrow, and pancreatic tissues. Stem Cells International, 2015, 1–10.CrossRefGoogle Scholar
  43. 43.
    Xie, X., Wang, Y., Zhao, C., et al. (2012). Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration. Biomaterials, 33(29), 7008–7018. doi: 10.1016/j.biomaterials.2012.06.058.PubMedCrossRefGoogle Scholar
  44. 44.
    Baksh, D., Yao, R., & Tuan, R. S. (2007). Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells, 25, 1384–1392.PubMedCrossRefGoogle Scholar
  45. 45.
    Champlin, R. E., Schmitz, N., Horowitz, M. M., et al. (2000). Blood stem cells compared with bone marrow as a source of hematopoietic cells for allogeneic transplantation, 95(12), 3702–3709.Google Scholar
  46. 46.
    Bianco, P., Riminucci, M., Gronthos, S., & Robey, P. G. (2001). Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells, 19, 180–192.PubMedCrossRefGoogle Scholar
  47. 47.
    Wagner, W., Feldmann, R. E., Seckinger, A., et al. (2006). The heterogeneity of human mesenchymal stem cell preparations evidence from simultaneous analysis of proteomes and transcriptomes. 34, 536–548.Google Scholar
  48. 48.
    Liu, Q., Cheng, G., Wang, Z., Zhan, S., Xiong, B., & Zhao, X. (2015). Bone marrow-derived mesenchymal stem cells differentiate into nerve-like cells in vitro after transfection with brain-derived neurotrophic factor gene. In Vitro Cellular and Developmental Biology - Animal, 51(3), 319–327.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Dueñas, F., Becerra, V., Cortes, Y., et al. (2014). Hepatogenic and neurogenic differentiation of bone marrow mesenchymal stem cells from abattoir-derived bovine fetuses. BMC Veterinary Research, 10(1), 154.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Lagasse, E., Connors, H., Al-Dhalimy, M., et al. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Natural Medicines, 6(11), 1229–1234.CrossRefGoogle Scholar
  51. 51.
    Riew, K. D., Wright, N. M., Cheng, S., Avioli, LV, & Lou, J. (1998). Induction of bone formation using a recombinant adenoviral vector carrying the human BMP-2 gene in a rabbit spinal fusion model. Calcified Tissue International, 63(4), 357–360.PubMedCrossRefGoogle Scholar
  52. 52.
    Gazit, D., Turgeman, G., Kelley, P., et al. Engineered pluripotent mesenchymal cells integrate and differentiate in regenerating bone: a novel cell-mediated gene therapy. The Journal of Gene Medicine, 1(2), 121–133.Google Scholar
  53. 53.
    Awad, H. A., Wickham, M. Q., Leddy, H. A., Gimble, J. M., & Guilak, F. (2004). Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. 25, 3211–3222.Google Scholar
  54. 54.
    Fraser, J. K., Schreiber, R., Strem, B., et al. (2006). Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nature Clinical Practice. Cardiovascular Medicine, 3 Suppl 1, S33–S37.PubMedCrossRefGoogle Scholar
  55. 55.
    Choi, Y. S., Dusting, G. J., Stubbs, S., et al. (2010). Differentiation of human adipose-derived stem cells into beating cardiomyocytes - Choi – 2010. Journal of Cellular and Molecular Medicine - Wiley Online Library.Google Scholar
  56. 56.
    Jang, S., Cho, H., Cho, Y., Park, J., & Jeong, H. (2010). Functional neural differentiation of human adipose tissue-derived stem cells using bFGF and forskolin. BMC Cell Biology, 10, 25.CrossRefGoogle Scholar
  57. 57.
    Gimble, J. M., Katz, A. J., & Bunnell, B. A. (2007). Adipose-derived stem cells for regenerative medicine.Google Scholar
  58. 58.
    Rodbell, M., & Jones, A. (1966). Metabolism of isolated fat cells II the similar effects of phospholipase C (Clostridium perfringens α toxin) and of insulin on glucose and amino acid metabolism. The Journal of Biological Chemistry, 241, 130–139.PubMedGoogle Scholar
  59. 59.
    Rodbell, M., & Jones, A. B. (1996). Metabolism of isolated fat cells III the similar inhibitory action of phospholipase C (Clostridium perfringens α toxin) and of insulin on lipolysis stimulated by lipolytic hormones and theophylline. The Journal of Biological Chemistry, 241(1), 140–142.Google Scholar
  60. 60.
    Rodbell, M., & Jones, A. (1966). Metabolism of isolated fat cells IV regulation of release of protein by lipolytic hormones and insulin. The Journal of Biological Chemistry, 241, 3909–3917.PubMedGoogle Scholar
  61. 61.
    Sun, N., Panetta, N. J., Gupta, D. M., et al. (2009). Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells.Google Scholar
  62. 62.
    Schäffler, A., & Büchler, C. (2007). Concise review: adipose tissue-derived stromal cells–basic and clinical implications for novel cell-based therapies. Stem Cells, 25(4), 818–827.PubMedCrossRefGoogle Scholar
  63. 63.
    Knipperberg, M., Helder, M. N., Doulabi, B. Z., Semeins, C. M., Wuisman PIJ., & Klein-Nulend, J. (2005). Adipose tissue-derived mesenchymal stem cells acquire osteogenic stimulation. Tissue Engineering, 11(11), 1780–1788.CrossRefGoogle Scholar
  64. 64.
    Charrière, G., Cousin, B., Arnaud, E., et al. (2003). Preadipocyte conversion to macrophage: evidence of plasticity. The Journal of Biological Chemistry, 278(11), 9850–9855.PubMedCrossRefGoogle Scholar
  65. 65.
    Urbich, C., & Dimmeler, S. (2004). Endothelial progenitor cells: characterization and role in vascular biology. Circulation Research, 95(4), 343–353.PubMedCrossRefGoogle Scholar
  66. 66.
    Erices, A., Conget, P., & Minguell, J. J. (2000). Mesenchymal progenitor cells in human umbilical cord blood. British Journal of Haematology, 109(1), 235–242.PubMedCrossRefGoogle Scholar
  67. 67.
    Sarugaser, R., Lickorish, D., Baksh, D., Hosseini, M. M., & Davies, J. E. (2005). Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells, 23(2), 220–229.PubMedCrossRefGoogle Scholar
  68. 68.
    Wang, H.-S., Hung, S.-C., Peng, S.-T., et al. (2004). Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord. Stem Cells, 22(7), 1330–1337.PubMedCrossRefGoogle Scholar
  69. 69.
    Ding, D. C., Chang, Y. H., Shyu, W. C., & Lin, S. Z. (2015). Human umbilical cord mesenchymal stem cells: a new era for stem cell therapy. Cell Transplantation, 24(3), 339–347.PubMedCrossRefGoogle Scholar
  70. 70.
    Chen, Y. (2015). Human umbilical cord mesenchymal stem cells: a new therapeutic option for tooth regeneration. Stem Cells International, 24(3), 339–347.Google Scholar
  71. 71.
    Kim, S.-W., Han, H., Chae, G.-T., et al. (2006). Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger’s disease and ischemic limb disease animal model. Stem Cells, 24(6), 1620–1626.PubMedCrossRefGoogle Scholar
  72. 72.
    Weiss, M. L., Medicetty, S., Bledsoe, A. R., et al. (2006). Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells, 24(3), 781–792.PubMedCrossRefGoogle Scholar
  73. 73.
    Chen, F. (2016). Stem cell-delivery therapeutics for periodontal tissue regeneration.Google Scholar
  74. 74.
    Gronthos, S., Mankani, M., Brahim, J., Robey, P. G., & Shi, S. (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. 97(25).Google Scholar
  75. 75.
    Miura, M., Gronthos, S., Zhao, M., et al. (2003). SHED: stem cells from human exfoliated deciduous teeth. 100(10), 5807–5812.Google Scholar
  76. 76.
    Kerkis, I., Dozortsev, D. (2007). Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. 900, 105–116.Google Scholar
  77. 77.
    Spath, L., Rotilio, V., Alessandrini, M., et al. (2010). Explant-derived human dental pulp stem cells enhance differentiation and proliferation potentials. Journal of Cellular and Molecular Medicine, 14(6 B), 1635–1644.PubMedGoogle Scholar
  78. 78.
    Hilkens, P., Gervois, P., Fanton, Y., et al. (2013). Effect of isolation methodology on stem cell properties and multilineage differentiation potential of human dental pulp stem cells. Cell and Tissue Research, 353(1), 65–78.PubMedCrossRefGoogle Scholar
  79. 79.
    Wang, J., Liu, X., Jin, X., et al. (2010). The odontogenic differentiation of human dental pulp stem cells on nanofibrous poly(l-lactic acid) scaffolds in vitro and in vivo. Acta Biomaterialia , 6(10), 3856–3863. doi: 10.1016/j.actbio.2010.04.009.PubMedCrossRefGoogle Scholar
  80. 80.
    d’Aquino, R., Graziano, A., Sampaolesi, M., et al. (2007). Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death and Differentiation, 14, 1162–1171.PubMedCrossRefGoogle Scholar
  81. 81.
    Karaöz, E., Nur, B., Gülçin, A., et al. (2010). Isolation and in vitro characterisation of dental pulp stem cells from natal teeth. 95–112.Google Scholar
  82. 82.
    Almushayt, A., Narayanan, K., Zaki, A. E., & George, A. (2006). Dentin matrix protein 1 induces cytodifferentiation of dental pulp stem cells into odontoblasts. 611–620.Google Scholar
  83. 83.
    Huang, G. T.-J., Yamaza, T., Shea, L. D., et al. (2010). Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model. Tissue Engineering Part A, 16(2), 605–615.PubMedCrossRefGoogle Scholar
  84. 84.
    Yamada, Y., Ito, K., Nakamura, S., Ueda, M., & Nagasaka, T. (2011). Promising cell-based therapy for bone regeneration using stem cells from deciduous teeth, dental pulp, and bone marrow. Cell Transplantation, 20(7), 1003–1013.PubMedCrossRefGoogle Scholar
  85. 85.
    D’Aquino, R., De Rosa, A., Lanza, V., et al. (2009). Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. European Cells & Materials, 18, 75–83.CrossRefGoogle Scholar
  86. 86.
    Seo, B., Miura, M., Gronthos, S., et al. (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. 149–155.Google Scholar
  87. 87.
    Abumaree, M., Al Jumah, M., Pace, R. A., & Kalionis, B. (2012). Immunosuppressive properties of mesenchymal stem cells. Stem Cell Reviews and Reports, 8, 375–392.PubMedCrossRefGoogle Scholar
  88. 88.
    Chan, R. W. S (2004). Clonogenicity of human endometrial epithelial and stromal cells. Biology of Reproduction, 70, 1738–1750.PubMedCrossRefGoogle Scholar
  89. 89.
    Gargett, C. E., & Masuda, H. (2010). Adult stem cells in the endometrium. 16(11), 818–834.Google Scholar
  90. 90.
    Meng, X., Ichim, T. E., Zhong, J., et al. (2007). Endometrial regenerative cells: a novel stem cell population. 10, 1–10.Google Scholar
  91. 91.
    Matthai, C., Horvat, R., Noe, M., et al. (2006). Oct-4 expression in human endometrium. Molecular Human Reproduction, 12(1), 7–10.PubMedCrossRefGoogle Scholar
  92. 92.
    Park, J. H., Daheron, L., Kantarci, S., Lee, B. S., & Teixeira, J. M. (2015). Human endometrial cells express elevated levels of pluripotent factors and are more amenable to reprogramming into induced pluripotent stem cells. Endocrinology, 152, 1080–1089.CrossRefGoogle Scholar
  93. 93.
    Gargett, C. E., Schwab, K. E., Zillwood, R. M., Nguyen, H. P. T., & Wu, D. (2009). Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biology of Reproduction, 1145, 1136–1145.CrossRefGoogle Scholar
  94. 94.
    Yang, X., Wang, W., & Li, X. (2014). In vitro hepatic differentiation of human endometrial stromal stem cells. In Vitro Cellular & Developmental Biology, 50, 162–170.CrossRefGoogle Scholar
  95. 95.
    Asmani, M. N., Ai, J., Amoabediny, G., & Noroozi, A. (2013). Three-dimensional culture of differentiated endometrial stromal cells to oligodendrocyte progenitor cells (OPCs) in fi brin hydrogel. Cell Biology International, 37, 1340–1349.PubMedCrossRefGoogle Scholar
  96. 96.
    Navaei-nigjeh, M., Amoabedini, G., Noroozi, A., et al. (2013). Enhancing neuronal growth from human endometrial stem cells derived neuron-like cells in three-dimensional fibrin gel for nerve tissue engineering. Journal of Biomedical Materials Research. Part A, 102A(8), 2533–2543.Google Scholar
  97. 97.
    Niknamasl, A., Ostad, S. N., Soleimani, M., et al. (2014). A new approach for pancreatic tissue engineering: human endometrial stem cells encapsulated in fibrin gel can differentiate to pancreatic islet beta-cell. Cell Biology International, 9999, 1–9.Google Scholar
  98. 98.
    Shoae-hassani, A., Sharif, S., & Seifalian, A. M. (2013). Endometrial stem cell differentiation into smooth muscle cell†¯: a novel approach for bladder tissue engineering in women. BJU International, 112, 854–863.PubMedCrossRefGoogle Scholar
  99. 99.
    Sekine, W., Haraguchi, Y., Shimizu, T., Yamato, M., Umezawa, A., & Okano, T. (2013). Chondrocyte differentiation of human endometrial gland-derived MSCs in layered cell sheets. The Scientific World Journal, 2013, 1–7.CrossRefGoogle Scholar
  100. 100.
    Ai, J., Azizi, E., Shamsian, A., Eslami, A., Khoshzaban, A., & Ebrahimi-barough, S. (2014). BMP-2 can promote the osteogenic differentiation of human endometrial stem cells. Asian Biomed, 8(1), 21–29.CrossRefGoogle Scholar
  101. 101.
    Wang, J., Chen, S., Zhang, C., et al. (2012). Human endometrial stromal stem cells differentiate into megakaryocytes with the ability to produce functional platelets. PLoS One, 7(8), 1–9.CrossRefGoogle Scholar
  102. 102.
    Ai, J., Shahverdi, A. R., Barough, S. E., & Kouchesfehani, H. M. (2012). Derivation of adipocytes from human Endometrial Stem Cells (EnSCs). Journal of Reproduction and Infertility, 13(1), 151–157.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Mobarakeh, Z. T., Ai, J., Yazdani, F., Mahdi, S., Sorkhabadi, R., & Ghanbari, Z. (2012). Human endometrial stem cells as a new source for programming to neural cells. Cell Biology International Reports, 19(1), 7–14.CrossRefGoogle Scholar
  104. 104.
    Mobarakeh, Z. T., Ai, J., Yazdani, F., Mahdi, S., Sorkhabadi, R., & Ghanbari, Z. (2012). Human endometrial stem cells as a new source for programming to neural cells. Cell Biology International, 19(1), 7–14.CrossRefGoogle Scholar
  105. 105.
    Tavakol, S., Aligholi, H., Gorji, A., et al. (2014). Thermogel nanofiber induces human endometrial-derived stromal cells to neural differentiation: in vitro and in vivo studies in rat. Society Biomaterials, 1–8.Google Scholar
  106. 106.
    Ai, J., & Mehrabani, D. (2010). Are endometrial stem cells novel tools against ischemic heart failure in women? A hypothesis. Iranian Red Crescent Medical Journal, 12(1), 73–75.Google Scholar
  107. 107.
    Toma, J. G., Akhavan, M., Fernandes, K. J., et al. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biology, 3(9), 778–784.PubMedCrossRefGoogle Scholar
  108. 108.
    Dyce, P. W., Zhu, H., Craig, J., & Li, J. (2004). Stem cells with multilineage potential derived from porcine skin. Biochemical and Biophysical Research Communications, 316(3), 651–658.PubMedCrossRefGoogle Scholar
  109. 109.
    Lysy, P. A., Smets, F., Sibille, C., Najimi, M., & Sokal, E. M. (2007). Human skin fibroblasts: from mesodermal to hepatocyte-like differentiation. Hepatology, 46(5), 1574–1585.PubMedCrossRefGoogle Scholar
  110. 110.
    Chen, F. G., Zhang, W. J., Bi, D., et al. (2007). Clonal analysis of nestin vimentin+ multipotent fibroblasts isolated from human dermis. Journal of Cell Science, 120(16), 2875–2883.PubMedCrossRefGoogle Scholar
  111. 111.
    Joannides, A., Gaughwin, P., Schwiening, C., & Majed, H. (2004). Efficient generation of neural precursors from adult human skin: astrocytes p. 364, 172–178.Google Scholar
  112. 112.
    Jahoda, C. A. B., Whitehouse, C. J., Reynolds, A. J., & Hole, N. (2003). Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Experimental Dermatology, 12(6), 849–859.PubMedCrossRefGoogle Scholar
  113. 113.
    Gingras, M., & Champigny, M., Berthod, F. (2007). Differentiation of human adult skin-derived neuronal precursors into mature neurons. Journal of Cellular Physiology, 210(1), 498–506.PubMedCrossRefGoogle Scholar
  114. 114.
    Shi, C., Zhu, Y., Su, Y., & Cheng, T. (2006). Stem cells and their applications in skin-cell therapy. Trends in Biotechnology, 24(1), 48–52.PubMedCrossRefGoogle Scholar
  115. 115.
    Prusa, A., Marton, E., Rosner, M., Bernaschek, G., & Hengstschla, M. (2003). Oct-4-expressing cells in human amniotic fluid: a new source for stem cell research? 18(7), 1489–1493.Google Scholar
  116. 116.
    Tsai, M.-S. (2004). Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Human Reproduction, 19(6), 1450–1456.PubMedCrossRefGoogle Scholar
  117. 117.
    Tsai, M.-S. (2006). Clonal amniotic fluid-derived stem cells express characteristics of both mesenchymal and neural stem cells. Biology of Reproduction, 74(3), 545–551.PubMedCrossRefGoogle Scholar
  118. 118.
    Hauser, P. V., De Fazio, R., Bruno, S., et al. (2011). Stem cells derived from human amniotic fluid contribute to acute kidney injury recovery. The American Journal of Pathology, 177(4), 2011–2021.CrossRefGoogle Scholar
  119. 119.
    De Coppi, P., Bartsch, G., Siddiqui, M. M., et al. (2007). Isolation of amniotic stem cell lines with potential for therapy. Nature Biotechnology, 25(1), 100–106.PubMedCrossRefGoogle Scholar
  120. 120.
    Soker, S., Atala, A., & Guldberg, R. E. (2007). Chondrogenic differentiation of amniotic fluid-derived stem cells. Journal of Molecular Histology, 38, 405–413.PubMedCrossRefGoogle Scholar
  121. 121.
    Perin, L., Giuliani, S., Jin, D., et al. (2007). Renal differentiation of amniotic fluid stem cells. Cell Proliferation, 40, 936–948.PubMedCrossRefGoogle Scholar
  122. 122.
    Carraro, G., Perin, L., & Sedrakyan, S. (2008). Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells, 2902–2911.Google Scholar
  123. 123.
    Yu, X., Wang, N., Qiang, R., et al. (2014). Human amniotic fluid stem cells possess the potential to differentiate into primordial follicle oocytes in vitro. Biology of Reproduction, 90(4), 73.PubMedCrossRefGoogle Scholar
  124. 124.
    Jun, E., Zhang, Q., Yoon, B., et al. (2014). Hypoxic conditioned medium from human amniotic fluid-derived mesenchymal stem cells accelerates skin wound healing through TGF-β/SMAD2 and PI3K/Akt pathways. International Journal of Molecular Sciences, 15(1), 605–628.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Cells, A. S. Results hAFSC phenotype and karyotype before injection in vivo detection of hAFSC by bioluminescence evaluation of the glycerol induced muscle damage and ATN using Period Acid Schiff Staining (PAS) and tunel staining.Google Scholar
  126. 126.
    Murphy, S. V., & Atala, A. (2013). Amniotic fluid stem cells. Perinatal Stem Cells, 1–16.Google Scholar
  127. 127.
    In’t Anker, P. S., Scherjon, S. A., Kleijburg-van der Keur, C., et al. (2004). Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells, 22(7), 1338–1345.CrossRefGoogle Scholar
  128. 128.
    Fukuchi, Y., Nakajima, H., Sugiyama, D., Hirose, I., Kitamura, T., & Tsuji, K. (2004). Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells, 22(5), 649–658.PubMedCrossRefGoogle Scholar
  129. 129.
    Yen, B. L., Chien, C.-C., Chen, Y.-C., et al. (2008). Placenta-derived multipotent cells differentiate into neuronal and glial cells in vitro. doi: 10.1089/ten.a20060352.
  130. 130.
    Chang, C.-M., Kao, C.-L., Chang, Y.-L., et al. (2007). Placenta-derived multipotent stem cells induced to differentiate into insulin-positive cells. Biochemical and Biophysical Research Communications, 357(2), 414–420.PubMedCrossRefGoogle Scholar
  131. 131.
    Chien, C.-C., Yen, B. L., Lee, F.-K., et al. (2006). In vitro differentiation of human placenta-derived multipotent cells into hepatocyte-like cells. Stem Cells, 24(7), 1759–1768.PubMedCrossRefGoogle Scholar
  132. 132.
    Haranova, D., Tothova, T., Sarissky, M., & Rosocha, J. (2011). Isolation and characterization of synovial mesenchymal stem. Folia Biologica, 57, 119–124.Google Scholar
  133. 133.
    De Sousa, E., Casado, P., Neto, V., Duarte, M. E., & Aguiar, D. (2014). Synovial fluid and synovial membrane mesenchymal stem cells: latest discoveries and therapeutic perspectives. Stem Cell Research & Therapy, 5(5), 112.CrossRefGoogle Scholar
  134. 134.
    Tatu, R. F., Anusca, D.-N., & Groza, S. S. (2014). Morphological and functional characterization of femoral head drilling-derived mesenchymal stem cells. Romanian Journal of Morphology and Embryology, 55(4), 1415–1422.PubMedGoogle Scholar
  135. 135.
    Chen, J., Mou, X., Du, X., Xiang, C. (2015). Comparative analysis of biological characteristics of adut mesenchymal stem cells with different tissue origins. Asian Pacific Journal of Tropical Medicine, 8(9), 739–746. doi: 10.1016/j.apjtm.2015.07.022.PubMedCrossRefGoogle Scholar
  136. 136.
    Yen, B. L., Huang, H., Chien, C., et al. (2005). Isolation of multipotent cells from human term placenta. Stem Cells, 23, 3–9.PubMedCrossRefGoogle Scholar
  137. 137.
    Stanko, P., Kaiserova, K., Altanerova, V., Altaner, C. (2013). Comparison of human mesenchymal stem cells derived from dental pulp, bone marrow, adipose tissue, and umbilical cord tissue by gene expression. Biomedical Papers of the Medical Faculty of the University Palacky, Olomouc, Czech Republic, 157(XX), 1–5.Google Scholar
  138. 138.
    Heo, J. S., Choi, Y., Kim, H., & Kim, H. O. K. (2016). Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. International Journal of Molecular Medicine, 37, 115–125.PubMedCrossRefGoogle Scholar
  139. 139.
    Liu, T. M., Martina, M., Hutmacher, D. W., Hui, J. H. P., Lee, E. H., & Lim, B. (2007). Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells, 25, 750–760.PubMedCrossRefGoogle Scholar
  140. 140.
    Bonaventura, G., Chamayou, S., Liprino, A., et al. (2015). Different tissue-derived stem cells: a comparison of neural differentiation capability. PLoS One, 1–26.Google Scholar
  141. 141.
    Le Blanc, K., Frassoni, F., Ball, L., et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet, 371, 1579–1586.PubMedCrossRefGoogle Scholar
  142. 142.
    Fibbe, W. E. (2003). Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation to the editor: in B-cell chronic lymphocytic leukemias, 7q21 translocations lead to overexpression of the. Blood, 102(4), 1548–1549.PubMedCrossRefGoogle Scholar
  143. 143.
    Uccelli, A., Pistoia, V., & Moretta, L. (2007). Mesenchymal stem cells: a new strategy for immunosuppression? Trends in Immunology, 28(5), 219-26.PubMedCrossRefGoogle Scholar
  144. 144.
    Taylor, C. J., Bolton, E. M., & Bradley, J. A. (2011). Immunological considerations for embryonic and induced pluripotent stem cell banking. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 366(1575), 2312–2322.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Orleans, N. (2008). Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells, 26(1), 99–107.CrossRefGoogle Scholar
  146. 146.
    Zhao, Q., Ren, H., & Han, Z. (2015) Science direct mesenchymal stem cells: immunomodulatory capability and clinical potential in immune diseases. Journal of Cellular Immunotherapy. doi: 10.1016/j.jocit.2014.12.001.Google Scholar
  147. 147.
    Racz, G. Z., Kadar, K., Foldes, A., Kallo, K., Perczel-Kovach, K., Keremi, B., & Nagy, A., Varga, G. (2014). Immunomodulatory and potential therapeutic role of mesenchymal stem cells in periodontitis. Journal of Physiology and Pharmacology, 65(3), 327–339.PubMedGoogle Scholar
  148. 148.
    Deuse, T., Stubbendorff, M., Tang-Quan, K., et al. (2011). Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplantation, 20, 655–667.PubMedCrossRefGoogle Scholar
  149. 149.
    Le Blanc, K., Tammik, C., Rosendahl, K., Zetterberg, E., & Ringde, O. (2003). HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Experimental Hematology, 31, 890–896.PubMedCrossRefGoogle Scholar
  150. 150.
    Chan, J. L., Tang, K. C., Patel, A. P., et al. (2006). Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-γ. Blood, 107(12), 4817–4824.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Schurgers, E., Kelchtermans, H., Mitera, T., Geboes, L., & Matthys, P. (2010). Discrepancy between the in vitro and in vivo effects of murine mesenchymal stem cells on T-cell proliferation and collagen-induced arthritis. Arthritis Research and Therapy, 12, R31. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2875665&tool=pmcentrez&rendertype=abstract.
  152. 152.
    Tse, W. T., Pendleton, J. D., Beyer, W. M., Egalka, M. C., & Guinan, E. C. (2003). Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation, 75(5), 389–397.PubMedCrossRefGoogle Scholar
  153. 153.
    Chen, L., He, D. M., & Zhang, Y. (2009). The differentiation of human placenta-derived mesenchymal stem cells into dopaminergic cells in vitro. Cellular and Molecular Biology Letters, 14(August 2008):528–36. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19412574.
  154. 154.
    Chang, C.-J., Yen, M.-L., Chen, Y.-C., et al. (2006). Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells, 24, 2466–2477.PubMedCrossRefGoogle Scholar
  155. 155.
    Jones, B. J., Brooke, G., Atkinson, K., & McTaggart, S. J. (2007). Immunosuppression by placental indoleamine 2,3-dioxygenase: a role for mesenchymal stem cells. Placenta, 28, 1174–1181.PubMedCrossRefGoogle Scholar
  156. 156.
    Constantin, G., Marconi, S., Rossi, B., et al. (2009). Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells, 27, 2624–2635.PubMedCrossRefGoogle Scholar
  157. 157.
    Tomic, S., Djokic, J., Vasilijic, S., Vucevic, D., & Todorovic, V. (2010). Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells and Development, 20(4), 695–708.CrossRefGoogle Scholar
  158. 158.
    Peron, J. P. S., Jazedje, T., Brandão, W. N., et al. (2012). Human endometrial-derived mesenchymal stem cells suppress inflammation in the central nervous system of EAE mice. Stem Cell Reviews and Reports, 8(3), 940–952.PubMedCrossRefGoogle Scholar
  159. 159.
    Pisati, F., Belicchi, M., Acerbi, F., et al. (2007). Effect of human skin-derived stem cells on vessel architecture, tumor growth, and tumor invasion in brain tumor animal models. Cancer Research, 67(7), 3054–3064.PubMedCrossRefGoogle Scholar
  160. 160.
    Zheng, Z. H., Li, X. Y., Ding, J., Jia, J. F., & Zhu, P. (2008). Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Rheumatology, 47, 22–30.PubMedCrossRefGoogle Scholar
  161. 161.
    Zappia, E., Casazza, S., Pedemonte, E., et al. (2008). Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. 106(5), 1755–1761.Google Scholar
  162. 162.
    Liang, J., Zhang, H., Hua, B., et al. (2010). Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Annals of the Rheumatic Diseases, 69, 1423–1429. Available from: http://0-ard.bmj.com.wam.leeds.ac.uk/content/69/8/1423.full.
  163. 163.
    Sun, L., Akiyama, K., Zhang, H., et al. (2009). Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells, 27, 1421–1432.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Jorgensen, C. (2010). Mesenchymal stem cells immunosuppressive properties: is it specifi c to bone marrow-derived cells? Stem Cell Research & Therapy, 1(15), 1–2.Google Scholar
  165. 165.
    Krampera, M., Cosmi, L., Angeli, R., et al. (2006). Role for Interferon gamma in the Immunomodulatory activity of human. Stem Cells, 24, 386–398.PubMedCrossRefGoogle Scholar
  166. 166.
    Liu, R., Li, X., Zhang, Z., et al. (2015). Allogeneic mesenchymal stem cells inhibited T follicular helper cell generation in rheumatoid arthritis. Scientific Reports, 5(12777), 1–11. doi: 10.1038/srep12777.Google Scholar
  167. 167.
    Sonoda, S., Yamaza, H., Ma, L., & Tanaka, Y., Tomoda, E. (2016). Interferon-gamma improves impaired dentinogenic and immunosuppressive functions of irreversible pulpitis-derived human dental pulp stem cells. Science Reports, 6(19286), 1–12. doi: 10.1038/srep19286.Google Scholar
  168. 168.
    DelaRosa, O., Lombardo, E., Beraza, A., et al. (2009). 2, 3-dioxygenase expression in the modulation of lymphocyte. Tissue Engineering, 15(10), 2795–2806.PubMedCrossRefGoogle Scholar
  169. 169.
    Hwang, J. H., Shim, S. S., Seok, O. S., et al. (2009). Comparison of cytokine expression in mesenchymal stem cells from human placenta, cord blood, and bone marrow. Journal of Korean Medical Science, 24, 547–554.PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Peister, A., Mellad, J. A., Larson, B. L., Hall, B. M., Gibson, L. F., & Prockop, D. J. (2015). Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood, 103(5), 1662–1669.CrossRefGoogle Scholar
  171. 171.
    Joannides, A., Gaughwin, P., Schwiening, C., & Majed, H. (2004). Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet, 364(9429), 172–178.PubMedCrossRefGoogle Scholar
  172. 172.
    Kim, B.-O., Tian, H., Prasongsukarn, K., et al. (2005). Cell transplantation improves ventricular function after a myocardial infarction: a preclinical study of human unrestricted somatic stem cells in a porcine model. Circulation, 112(9 Suppl), 96–104.Google Scholar
  173. 173.
    Augello, A., Tasso, R., Negrini, S. M., Cancedda, R., & Pennesi, G. (2007). Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis and Rheumatism, 56(4), 1175–1186.PubMedCrossRefGoogle Scholar
  174. 174.
    Gerdoni, E., Gallo, B., Casazza, S., et al. (2007). Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Annals of Neurology, 61(3), 219–227.PubMedCrossRefGoogle Scholar
  175. 175.
    Zhao, Y., Xu, A., Xu, Q., et al. (2014). Bone marrow mesenchymal stem cell transplantation for treatment of emphysemic rats. International Journal of Clinical and Experimental Medicine, 7(4), 968.PubMedPubMedCentralGoogle Scholar
  176. 176.
    Roddy, G. W., Oh, J. Y., Lee, R. H., et al. (2011). Action at a distance: systemically administered adult stem/progenitor cells (MSCs) reduce inflammatory damage to the cornea without engraftment and primarily by secretion of TNF-α stimulated gene/protein 6. Stem Cells, 29(10), 1572–1579.PubMedCrossRefGoogle Scholar
  177. 177.
    Gu, Z., Akiyama, K., Ma, X., et al. (2010). Transplantation of umbilical cord mesenchymal stem cells alleviates lupus nephritis in MRL/lpr mice. Lupus, 19(13), 1502–1514.PubMedCrossRefGoogle Scholar
  178. 178.
    Liu, Y., Mu, R., Wang, S., et al. (2010). Therapeutic potential of human umbilical cord mesenchymal stem cells in the treatment of rheumatoid arthritis. Arthritis Research & Therapy, 12(6), R210.CrossRefGoogle Scholar
  179. 179.
    Zucconi, E., Vieira, N. M., Bueno, C. R., et al. (2011). Preclinical studies with umbilical cord mesenchymal stromal cells in different animal models for muscular dystrophy. Journal of Biomedicine & Biotechnology, 2011, 715251.CrossRefGoogle Scholar
  180. 180.
    Koh, S.-H., Kim, K. S., Choi, M. R., et al. (2008). Implantation of human umbilical cord-derived mesenchymal stem cells as a neuroprotective therapy for ischemic stroke in rats. Brain Research, 1229, 233–248.PubMedCrossRefGoogle Scholar
  181. 181.
    Lee, H. J., Lee, J. K., Lee, H., et al. (2010). The therapeutic potential of human umbilical cord blood-derived mesenchymal stem cells in Alzheimer’s disease. Neuroscience Letters, 481(1), 30–35.PubMedCrossRefGoogle Scholar
  182. 182.
    Takehara, Y., Yabuuchi, A., Ezoe, K., et al. (2013). The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Laboratory Investigation, 93(2), 181–193.PubMedCrossRefGoogle Scholar
  183. 183.
    Zhou, B., Yuan, J., Zhou, Y., et al. (2011). Administering human adipose-derived mesenchymal stem cells to prevent and treat experimental arthritis. Clinical Immunology, 141(3), 328–337.PubMedCrossRefGoogle Scholar
  184. 184.
    González, M. A., Gonzalez-Rey, E., Rico, L., et al. (2009). Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology, 136(3), 978–989.PubMedCrossRefGoogle Scholar
  185. 185.
    Lin, G., Wang, G., Banie, L., et al. (2010). Treatment of stress urinary incontinence with adipose tissue-derived stem cells. Cytotherapy, 12(1), 88–95.PubMedPubMedCentralCrossRefGoogle Scholar
  186. 186.
    Gomes, J. A., Monteiro, B. G., Melo, G. B., et al. (2008). Pre-clinical investigation of the efficacy of immature dental pulp stem cells transplantation for ocular surface reconstruction. Investigative Ophthalmology and Visual Science, 49(13), 5730–5730.Google Scholar
  187. 187.
    Gandia, C., Armiñan, A., García-Verdugo, J. M., et al. (2008). Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction. Stem Cells, 26(3), 638–645.PubMedCrossRefGoogle Scholar
  188. 188.
    Sonoyama, W., Liu, Y., Fang, D., et al. (2006). Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One, 1(1), e79.PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Sakai, K., Yamamoto, A., Matsubara, K., et al. (2011). Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. The Journal of Clinical Investigation, 122(1), 429–440.Google Scholar
  190. 190.
    Fisher-Shoval, Y., Barhum, Y., Sadan, O., et al. (2012). Transplantation of placenta-derived mesenchymal stem cells in the EAE mouse model of MS. Journal of Molecular Neuroscience: MN, 48(1), 176–184.PubMedCrossRefGoogle Scholar
  191. 191.
    Jung, J., Choi, J. H., Lee, Y., et al. (2013). Human placenta-derived mesenchymal stem cells promote hepatic regeneration in CCl4 -injured rat liver model via increased autophagic mechanism. Stem Cells, 31(8), 1584–1596.PubMedCrossRefGoogle Scholar
  192. 192.
    Park, S., Koh, S.-E., Maeng, S., et al. (2011). Neural progenitors generated from the mesenchymal stem cells of first-trimester human placenta matured in the hypoxic-ischemic rat brain and mediated restoration of locomotor activity. Placenta, 32(3), 269–276.PubMedCrossRefGoogle Scholar
  193. 193.
    Prather, W. R., Toren, A., Meiron, M., Ofir, R., Tschope, C., & Horwitz, E. M. (2009). The role of placental-derived adherent stromal cell (PLX-PAD) in the treatment of critical limb ischemia. Cytotherapy, 11(4), 427–434.PubMedCrossRefGoogle Scholar
  194. 194.
    Baulier, E., Favreau, F., Le Corf, A., et al. (2014). Amniotic fluid-derived mesenchymal stem cells prevent fibrosis and preserve renal function in a preclinical porcine model of kidney transplantation. Stem Cells Translational Medicine, 3(7), 809–820.PubMedPubMedCentralCrossRefGoogle Scholar
  195. 195.
    Turner, C. G., Klein, J. D., Steigman, S. A., et al. (2011). Preclinical regulatory validation of an engineered diaphragmatic tendon made with amniotic mesenchymal stem cells. Journal of Pediatric Surgery, 46(1), 57–61.PubMedCrossRefGoogle Scholar
  196. 196.
    Zagoura, D. S., Roubelakis, M. G., Bitsika, V., et al. (2012). Therapeutic potential of a distinct population of human amniotic fluid mesenchymal stem cells and their secreted molecules in mice with acute hepatic failure. Gut, 61(6), 894–906.PubMedCrossRefGoogle Scholar
  197. 197.
    Perin, L., Sedrakyan, S., Giuliani, S., et al. (2010). Protective effect of human amniotic fluid stem cells in an immunodeficient mouse model of acute tubular necrosis. PLoS One, 5(2), e9357.PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Chang, Y.-J., Ho, T.-Y., Wu, M.-L., Hwang, S.-M., Chiou, T.-W., & Tsai, M.-S. (2013). Amniotic fluid stem cells with low γ-interferon response showed behavioral improvement in Parkinsonism rat model. PLoS One, 8(9), e76118.PubMedPubMedCentralCrossRefGoogle Scholar
  199. 199.
    Li, H.-Y., Chen, Y.-J., Chen, S.-J., et al. (2010). Induction of insulin-producing cells derived from endometrial mesenchymal stem-like cells. The Journal of Pharmacology and Experimental Therapeutics, 335(3), 817–829.PubMedCrossRefGoogle Scholar
  200. 200.
    Edwards, S. L., Ulrich, D., White, J. F., et al. (2015). Temporal changes in the biomechanical properties of endometrial mesenchymal stem cell seeded scaffolds in a rat model. Acta Biomaterialia, 13, 286–294.PubMedCrossRefGoogle Scholar
  201. 201.
    Lai, D., Wang, F., Yao, X., et al. (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(1), 155.PubMedPubMedCentralCrossRefGoogle Scholar
  202. 202.
    Zhao, Z., Liao, L., Cao, Y., Jiang, X., & Zhao, R. (2005). Pre-clinical studies establishment and properties of fetal dermis-derived mesenchymal stem cell lines: plasticity in vitro and hematopoietic protection in vivo. Bone Marrow Transplantation, 36, 355–365.PubMedCrossRefGoogle Scholar
  203. 203.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    Koizumi, K., Ebina, K., Hart, D. A., et al. (2016). Synovial mesenchymal stem cells from osteo- or rheumatoid arthritis joints exhibit good potential for cartilage repair using a scaffold-free tissue engineering approach. Osteoarthritis and Cartilage, 24(8), 1413–1422.PubMedCrossRefGoogle Scholar
  205. 205.
    Ozeki, N., Muneta, T., Koga, H., et al. (2016). Not single but periodic injections of synovial mesenchymal stem cells maintain viable cells in knees and inhibit osteoarthritis progression in rats. Osteoarthritis and Cartilage, 24(6), 1061–1070.PubMedCrossRefGoogle Scholar
  206. 206.
    Li, H., Qian, J., Chen, J., Zhong, K., & Chen, S. (2016). Osteochondral repair with synovial membrane-derived mesenchymal stem cells. Molecular Medicine Reports, 13(3), 2071–2077.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Nakagawa, Y., Muneta, T., Kondo, S., et al. (2015). Synovial mesenchymal stem cells promote healing after meniscal repair in microminipigs. Osteoarthritis and Cartilage/OARS, Osteoarthritis Research Society, 23(6), 1007–1017.CrossRefGoogle Scholar
  208. 208.
    Solari, M. G., Srinivasan, S., Boumaza, I., et al. (2009). Marginal mass islet transplantation with autologous mesenchymal stem cells promotes long-term islet allograft survival and sustained normoglycemia. Journal of Autoimmunity, 32(2), 116–124.PubMedCrossRefGoogle Scholar
  209. 209.
    Calió, M. L., Marinho, D. S., Ko, G. M., et al. (2014). Transplantation of bone marrow mesenchymal stem cells decreases oxidative stress, apoptosis, and hippocampal damage in brain of a spontaneous stroke model. Free Radical Biology and Medicine, 70, 141–154.PubMedCrossRefGoogle Scholar
  210. 210.
    Zhou, K., Zhang, H., Jin, O., et al. (2008). Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cellular & Molecular Immunology, 5(6), 417–424.CrossRefGoogle Scholar
  211. 211.
    Cai, M., Shen, R., Song, L., et al. (2016). Bone Marrow Mesenchymal Stem Cells (BM-MSCs) improve heart function in swine myocardial infarction model through paracrine effects. Scientific Reports, 6, 28250.PubMedPubMedCentralCrossRefGoogle Scholar
  212. 212.
    Pelizzo, G., Avanzini, M. A., Icaro Cornaglia, A., et al. (2015). Mesenchymal stromal cells for cutaneous wound healing in a rabbit model: pre-clinical study applicable in the pediatric surgical setting. Journal of Translational Medicine, 13(1), 219.PubMedPubMedCentralCrossRefGoogle Scholar
  213. 213.
    Yokoya, S., Mochizuki, Y., Natsu, K., Omae, H., Nagata, Y., & Ochi, M. (2012). Rotator cuff regeneration using a bioabsorbable material with bone marrow-derived mesenchymal stem cells in a rabbit model. The American Journal of Sports Medicine, 40(6), 1259–1268.PubMedCrossRefGoogle Scholar
  214. 214.
    Ahmed, S. K., Soliman, A. A., Omar, S. M. M., & Mohammed, W. R. (2015). Bone marrow mesenchymal stem cell transplantation in a rabbit corneal alkali burn model (A histological and immune histo-chemical study). International Journal of Stem Cells, 8(1), 69.PubMedPubMedCentralCrossRefGoogle Scholar
  215. 215.
    El-Menoufy, H., Aly, L. A. A., Aziz, M. T. A., et al. (2009). The role of bone marrow-derived mesenchymal stem cells in treating formocresol induced oral ulcers in dogs. Journal of Oral Pathology & Medicine, 39(4), 281–289.Google Scholar
  216. 216.
    Penha, E. M., Meira, C. S., Guimarães, E. T., et al. (2014). Use of autologous mesenchymal stem cells derived from bone marrow for the treatment of naturally injured spinal cord in dogs. Stem Cells International, 2014, 437521.PubMedPubMedCentralCrossRefGoogle Scholar
  217. 217.
    Berman, D. M., Willman, M. A., Han, D., et al. (2010). Mesenchymal stem cells enhance allogeneic islet engraftment in nonhuman primates. Diabetes, 59(10), 2558–2568.PubMedPubMedCentralCrossRefGoogle Scholar
  218. 218.
    Devine, S. M., Bartholomew, A. M., Mahmud, N., et al. (2001). Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Experimental Hematology, 29(2), 244–255.PubMedCrossRefGoogle Scholar
  219. 219.
    Steinberg, G. K., Kondziolka, D., Wechsler, L. R., et al. (2016). Clinical outcomes of transplanted modified bone marrow–derived mesenchymal stem cells in stroke. Stroke; a Journal of Cerebral Circulation, 47(7), 1817–1824.CrossRefGoogle Scholar
  220. 220.
    Lee, P., Kim, J., Bang, O., Ahn, Y., Joo, I., & Huh, K. (2008). Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clinical Pharmacology and Therapeutics, 83(5), 723–730.PubMedCrossRefGoogle Scholar
  221. 221.
    Ding, D.-C., Shyu, W.-C., Chiang, M.-F., et al. (2007). Enhancement of neuroplasticity through upregulation of β1-integrin in human umbilical cord-derived stromal cell implanted stroke model. Neurobiology of Diseases, 27(3), 339–353.CrossRefGoogle Scholar
  222. 222.
    Kim, E. S., Ahn, S. Y., Im, G. H., et al. (2012). Human umbilical cord blood–derived mesenchymal stem cell transplantation attenuates severe brain injury by permanent middle cerebral artery occlusion in newborn rats. Pediatric Research, 72(3), 277–284.PubMedCrossRefGoogle Scholar
  223. 223.
    Guan, Y.-M., Zhu, Y., Liu, X.-C., et al. (2014). Effect of human umbilical cord blood mesenchymal stem cell transplantation on neuronal metabolites in ischemic rabbits. BMC Neuroscience, 15(1), 41.PubMedPubMedCentralCrossRefGoogle Scholar
  224. 224.
    Ha, C.-W., Kim, J.-A., Rhim, J., et al. (2016). Articular cartilage repair by transplanting various concentrations of human umbilical cord blood-derived mesenchymal stem cells and hyaluronic acid hydrogel composites in a rabbit model. Osteoarthritis and Cartilage, 24, S164–S165.CrossRefGoogle Scholar
  225. 225.
    Wang, Y., Han, Z.-B., Ma, J., et al. (2012). A toxicity study of multiple-administration human umbilical cord mesenchymal stem cells in cynomolgus monkeys. Stem Cells and Development, 21(9), 1401–1408.PubMedCrossRefGoogle Scholar
  226. 226.
    Miao, X., Wu, X., & Shi, W. (2015). Umbilical cord mesenchymal stem cells in neurological disorders: a clinical study. Indian Journal of Biochemistry and Biophysics, 52(2), 140–146.PubMedGoogle Scholar
  227. 227.
    Lu, Z., Zhao, H., Xu, J., Zhang, Z. (2013). Human umbilical cord mesenchymal stem cells in the treatment of secondary progressive multiple sclerosis. Stem Cell Research & Therapy, 6, 2157–7633.Google Scholar
  228. 228.
    Haller, M. J., Wasserfall, C. H., Hulme, M. A., et al. (2011). Autologous umbilical cord blood transfusion in young children with type 1 diabetes fails to preserve C-peptide. Diabetes Care, 34(12), 2567–2569.PubMedPubMedCentralCrossRefGoogle Scholar
  229. 229.
    Wang, D., Li, J., Zhang, Y., et al. (2014). Umbilical cord mesenchymal stem cell transplantation in active and refractory systemic lupus erythematosus: a multicenter clinical study. Arthritis Research & Therapy, 16(2), R79.CrossRefGoogle Scholar
  230. 230.
    Leu, S., Lin, Y.-C., Yuen, C.-M., et al. (2010). Adipose-derived mesenchymal stem cells markedly attenuate brain infarct size and improve neurological function in rats. Journal of Translational Medicine, 8, 63.PubMedPubMedCentralCrossRefGoogle Scholar
  231. 231.
    Eirin, A., Zhu, X.-Y., Krier, J. D., et al. (2012). Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells, 30(5), 1030–1041.PubMedPubMedCentralCrossRefGoogle Scholar
  232. 232.
    Wilson, S. M., Goldwasser, M. S., Clark, S. G., et al. (2012). Adipose-derived mesenchymal stem cells enhance healing of mandibular defects in the ramus of swine. Journal of Oral and Maxillofacial Surgery, 70(3), e193–e203.PubMedCrossRefGoogle Scholar
  233. 233.
    Desando, G., Cavallo, C., Sartoni, F., et al. (2013). Intra-articular delivery of adipose derived stromal cells attenuates osteoarthritis progression in an experimental rabbit model. Arthritis Research & Therapy, 15(1), R22.CrossRefGoogle Scholar
  234. 234.
    Vilar, J. M., Batista, M., Morales, M., et al. (2014). Assessment of the effect of intraarticular injection of autologous adipose-derived mesenchymal stem cells in osteoarthritic dogs using a double blinded force platform analysis. BMC Veterinary Research, 10(1), 143.PubMedPubMedCentralCrossRefGoogle Scholar
  235. 235.
    Panfilov, I. A., De Jong, R., Takashima, S., & Duckers, H. J. (2013). Clinical study using adipose-derived mesenchymal-like stem cells in acute myocardial infarction and heart failure. p 207–212.Google Scholar
  236. 236.
    Koh, Y.-G., Jo, S.-B., Kwon, O.-R., et al. (2013). Mesenchymal stem cell injections improve symptoms of knee osteoarthritis. Arthroscopy: The Journal of Arthroscopic and Related Surgery, 29(4), 748–755.PubMedCrossRefGoogle Scholar
  237. 237.
    Pak, J., Chang, J.-J., Lee, J. H., & Lee, S. H. (2013). Safety reporting on implantation of autologous adipose tissue-derived stem cells with platelet-rich plasma into human articular joints. BMC Musculoskeletal Disorders, 14, 337.PubMedPubMedCentralCrossRefGoogle Scholar
  238. 238.
    Leong, W. K., Henshall, T. L., Arthur, A., et al. (2012). Human adult dental pulp stem cells enhance poststroke functional recovery through non-neural replacement mechanisms. Stem Cells Translational Medicine, 1(3), 177–187.PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Shi, S., Bartold, P., Miura, M., Seo, B., Robey, P., & Gronthos, S. (2005). The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthodontics and Craniofacial Research, 8(3), 191–199.PubMedCrossRefGoogle Scholar
  240. 240.
    Khorsand, A., Baghaban Eslaminejad, M., Arabsolghar, M., et al. Autologous dental pulp stem cells in regeneration of defect created in canine periodontal tissue.Google Scholar
  241. 241.
    Kerkis, I., Ambrosio, C. E., Kerkis, A., et al. (2008). Early transplantation of human immature dental pulp stem cells from baby teeth to golden retriever muscular dystrophy (GRMD) dogs: local or systemic? Journal of Translational Medicine, 6(1), 35.PubMedPubMedCentralCrossRefGoogle Scholar
  242. 242.
    Ulrich, D., Edwards, S. L., Su, K., et al. (2014). Human endometrial mesenchymal stem cells modulate the tissue response and mechanical behavior of polyamide mesh implants for pelvic organ prolapse repair. Tissue Engineering Part A, 20(3–4), 785–798.PubMedGoogle Scholar
  243. 243.
    Wolff, E. F., Mutlu, L., Massasa, E. E., Elsworth, J. D., Eugene Redmond, D., & Taylor, H. S. (2015). Endometrial stem cell transplantation in MPTP- exposed primates: an alternative cell source for treatment of Parkinson’s disease. Journal of Cellular and Molecular Medicine, 19(1), 249–256.PubMedCrossRefGoogle Scholar
  244. 244.
    Monteiro Carvalho Mori da Cunha, M. G., Zia, S., Oliveira Arcolino, F., et al. (2015). Amniotic fluid derived stem cells with a renal progenitor phenotype inhibit interstitial fibrosis in renal ischemia and reperfusion injury in rats. PLoS One, 10(8), e0136145.PubMedPubMedCentralCrossRefGoogle Scholar
  245. 245.
    Perin, L., Sedrakyan, S., Giuliani, S., et al. Protective effect of human amniotic fluid stem cells in an immunodefficient mouse model of acute tubular necrosis.Google Scholar
  246. 246.
    Klein, J. D., Turner, C. G. B., Ahmed, A., et al. (2010). Chest wall repair with engineered fetal bone grafts: an efficacy analysis in an autologous leporine model. Journal of Pediatric Surgery, 45(6), 1354–1360.PubMedCrossRefGoogle Scholar
  247. 247.
    Tan, L., Dai, T., Liu, D., et al. (2016). Contribution of dermal-derived mesenchymal cells during liver repair in two different experimental models. Scientific Reports, 6, 25314.PubMedPubMedCentralCrossRefGoogle Scholar
  248. 248.
    Ma, D., Kua, J. E. H, Lim, W. K., et al. (2015). In vitro characterization of human hair follicle dermal sheath mesenchymal stromal cells and their potential in enhancing diabetic wound healing. Cytotherapy, 17(8), 1036–1051.PubMedCrossRefGoogle Scholar
  249. 249.
    Mak, J., Jablonski, C. L., Leonard, C. A., et al. (2016). Intra-articular injection of synovial mesenchymal stem cells improves cartilage repair in a mouse injury model. Scientific Reports, 6, 23076.PubMedPubMedCentralCrossRefGoogle Scholar
  250. 250.
    Lee, J.-C., Min, H. J., Park, H. J., et al. (2013). Synovial membrane–derived mesenchymal stem cells supported by platelet-rich plasma can repair osteochondral defects in a rabbit model. Arthroscopy: The Journal of Arthroscopic and Related Surgery, 29(6), 1034–1046.PubMedCrossRefGoogle Scholar
  251. 251.
    Horie, M., Driscoll, M. D., Sampson, H. W., et al. (2012). Implantation of allogenic synovial stem cells promotes meniscal regeneration in a rabbit meniscal defect model. The Journal of Bone and Joint Surgery. American Volume, 94(8), 701–712.PubMedPubMedCentralCrossRefGoogle Scholar
  252. 252.
    Kondo, S., Muneta, T., Nakagawa, Y., et al. (2016). Transplantation of autologous synovial mesenchymal stem cells promotes meniscus regeneration in aged primates. Journal of Orthopaedic Research.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Dannie Macrin
    • 1
  • Joel P. Joseph
    • 1
  • Aruthra Arumugam Pillai
    • 1
  • Arikketh Devi
    • 1
  1. 1.Department of Genetic EngineeringSRM UniversityKattankulathurIndia

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