Biomolecules & Therapeutics

  • 제27권1호
  • /
  • Pages.25-33
  • /
  • 2019
  • /
  • 1976-9148(pISSN)
  • /
  • 2005-4483(eISSN)
한국응용약물학회 (The Korean Society of Applied Pharmacology)
권호 표지
DOI QR코드

DOI QR Code

Roles of Mesenchymal Stem Cells in Tissue Regeneration and Immunomodulation

  • Ayala-Cuellar, Ana Patricia (Laboratory of Biochemistry and Immunology, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Kang, Ji-Houn (Laboratory of Internal Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Jeung, Eui-Bae (Laboratory of Biochemistry and Molecular Biology, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Choi, Kyung-Chul (Laboratory of Biochemistry and Immunology, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University)
  • 투고 : 2017.12.27
  • 심사 : 2018.04.16
  • 발행 : 2019.01.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Mesenchymal stem cells are classified as multipotent stem cells, due to their capability to transdifferentiate into various lineages that develop from mesoderm. Their popular appeal as cell-based therapy was initially based on the idea of their ability to restore tissue because of their differentiation potential in vitro; however, the lack of evidence of their differentiation to target cells in vivo led researchers to focus on their secreted trophic factors and their role as potential powerhouses on regulation of factors under different immunological environments and recover homeostasis. To date there are more than 800 clinical trials on humans related to MSCs as therapy, not to mention that in animals is actively being applied as therapeutic resource, though it has not been officially approved as one. But just as how results from clinical trials are important, so is to reveal the biological mechanisms involved on how these cells exert their healing properties to further enhance the application of MSCs on potential patients. In this review, we describe characteristics of MSCs, evaluate their benefits as tissue regenerative therapy and combination therapy, as well as their immunological properties, activation of MSCs that dictate their secreted factors, interactions with other immune cells, such as T cells and possible mechanisms and pathways involved in these interactions.

키워드

참고문헌

  1. Abouelkheir, M., Eltantawy, D. A., Saad, M.-A., Abdelrahman, K. M., Sobh, M.-A., Lotfy, A. and Sobh, M. A. (2016) Mesenchymal stem cells versus their conditioned medium in the treatment of cisplatin-induced acute kidney injury: evaluation of efficacy and cellular side effects. Int. J. Clin. Exp. Med. 9, 23222-23234.
  2. Alcayaga-Miranda, F., Cuenca, J., Luz-Crawford, P., Aguila-Diaz, C., Fernandez, A., Figueroa, F. E. and Khoury, M. (2015) Characterization of menstrual stem cells: angiogenic effect, migration and hematopoietic stem cell support in comparison with bone marrow mesenchymal stem cells. Stem Cell Res. Ther. 6, 32. https://doi.org/10.1186/s13287-015-0013-5
  3. Arutyunyan, I., Elchaninov, A., Makarov, A. and Fatkhudinov, T. (2016) Umbilical Cord as Prospective Source for Mesenchymal Stem Cell-Based Therapy. Stem Cells Int. 2016, 6901286.
  4. Bahamondes, F., Flores, E., Cattaneo, G., Bruna, F. and Conget, P. (2017) Omental adipose tissue is a more suitable source of canine Mesenchymal stem cells. BMC Vet. Res. 13, 166. https://doi.org/10.1186/s12917-017-1053-0
  5. Bai, C., Gao, Y., Li, Q., Feng, Y., Yu, Y., Meng, G., Zhang, M. and Guan, W. (2015) Differentiation of chicken umbilical cord mesenchymal stem cells into beta-like pancreatic islet cells. Artif. Cells Nanomed. Biotechnol. 43, 106-111. https://doi.org/10.3109/21691401.2013.864662
  6. Bartholomew, A., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K., Patil, S., Hardy, W., Devine, S., Ucker, D., Deans, R., Moseley, A. and Hoffman, R. (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30, 42-48. https://doi.org/10.1016/S0301-472X(01)00769-X
  7. Bonab, M. M., Alimoghaddam, K., Talebian, F., Ghaffari, S. H., Ghavamzadeh, A. and Nikbin, B. (2006) Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 7, 14. https://doi.org/10.1186/1471-2121-7-14
  8. Boomsma, R. A. and Geenen, D. L. (2012) Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS ONE 7, e35685. https://doi.org/10.1371/journal.pone.0035685
  9. Brown, S. G., Harman, R. J. and Black, L. L. (2012) Adipose-derived stem cell therapy for severe muscle tears in working German shepherds: two case reports. Stem Cell Discovery 2, 41-44. https://doi.org/10.4236/scd.2012.22007
  10. Burr, S. P., Dazzi, F. and Garden, O. A. (2013) Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance? Immunol. Cell Biol. 91, 12-18. https://doi.org/10.1038/icb.2012.60
  11. Byeon, J. S., Lee, J., Kim, D. H., Lee, G.-B., Kim, H.-R., Gu, N.-Y., Cho, I.-S. and Cha, S.-H. (2016) Canine mesenchymal stem cells immunomodulate atopic dermatitis through the induction of regulatory T cells in an ex vivo experimental study. J. Prev. Vet. Med. 40, 12-21. https://doi.org/10.13041/jpvm.2016.40.1.12
  12. Caplan, A. I. (1991) Mesenchymal stem cells. J. Orthop. Res. 9, 641-650. https://doi.org/10.1002/jor.1100090504
  13. Carrade Holt, D. D., Wood, J. A., Granick, J. L., Walker, N. J., Clark, K. C. and Borjesson, D. L. (2014) Equine mesenchymal stem cells inhibit T cell proliferation through different mechanisms depending on tissue source. Stem Cells Dev. 23, 1258-1265. https://doi.org/10.1089/scd.2013.0537
  14. Case, J. B., Palmer, R., Valdes-Martinez, A., Egger, E. L. and Haussler, K. K. (2013) Gastrocnemius tendon strain in a dog treated with autologous mesenchymal stem cells and a custom orthosis. Vet. Surg. 42, 355-360. https://doi.org/10.1111/j.1532-950X.2013.12007.x
  15. Chen, L. B., Jiang, X. B. and Yang, L. (2004) Differentiation of rat marrow mesenchymal stem cells into pancreatic islet beta-cells. World J. Gastroenterol. 10, 3016-3020. https://doi.org/10.3748/wjg.v10.i20.3016
  16. Cyranoski, D. (2013) Stem cells boom in vet clinics. Nature 496, 148-149. https://doi.org/10.1038/496148a
  17. de Mattos Carvalho, A., Alves, A. L. G., de Oliveira, P. G. G., Cisneros Alvarez, L. E., Amorim, R. L., Hussni, C. A. and Deffune, E. (2011) Use of adipose tissue-derived mesenchymal stem cells for experimental tendinitis therapy in equines. J. Equine Vet. Sci. 31, 26-34. https://doi.org/10.1016/j.jevs.2010.11.014
  18. Domergue, S., Bony, C., Maumus, M., Toupet, K., Frouin, E., Rigau, V., Vozenin, M. C., Magalon, G., Jorgensen, C. and Noel, D. (2016) Comparison between stromal vascular fraction and adipose mesenchymal stem cells in remodeling hypertrophic scars. PLoS ONE 11, e0156161. https://doi.org/10.1371/journal.pone.0156161
  19. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D. and Horwitz, E. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317. https://doi.org/10.1080/14653240600855905
  20. Engela, A. U., Baan, C. C., Dor, F. J., Weimar, W. and Hoogduijn, M. J. (2012) On the interactions between mesenchymal stem cells and regulatory T cells for immunomodulation in transplantation. Front. Immunol. 3, 126. https://doi.org/10.3389/fimmu.2012.00126
  21. Engela, A. U., Baan, C. C., Peeters, A. M., Weimar, W. and Hoogduijn, M. J. (2013) Interaction between adipose tissue-derived mesenchymal stem cells and regulatory T-cells. Cell Transplant. 22, 41-54. https://doi.org/10.3727/096368912X636984
  22. English, K. and Mahon, B. P. (2011) Allogeneic mesenchymal stem cells: agents of immune modulation. J. Cell. Biochem. 112, 1963-1968. https://doi.org/10.1002/jcb.23119
  23. Fallarino, F., Grohmann, U., Vacca, C., Bianchi, R., Orabona, C., Spreca, A., Fioretti, M. C. and Puccetti, P. (2002) T cell apoptosis by tryptophan catabolism. Cell Death Differ. 9, 1069-1077. https://doi.org/10.1038/sj.cdd.4401073
  24. Fei, X., Jiang, S., Zhang, S., Li, Y., Ge, J., He, B., Goldstein, S. and Ruiz, G. (2013) Isolation, culture, and identification of amniotic fluid-derived mesenchymal stem cells. Cell Biochem. Biophys. 67, 689-694. https://doi.org/10.1007/s12013-013-9558-z
  25. Friedenstein, A. J., Chailakhjan, R. K. and Lalykina, K. S. (1970) The development of fibroblast colonies in monolayer cultures of guineapig bone marrow and spleen cells. Cell Tissue Kinet. 3, 393-403.
  26. Gaafar, T., Attia, W., Mahmoud, S., Sabry, D., Aziz, O. A., Rasheed, D. and Hamza, H. (2017) Cardioprotective effects of wharton jelly derived mesenchymal stem cell transplantation in a rodent model of myocardial injury. Int. J. Stem Cells 10, 48-59. https://doi.org/10.15283/ijsc16063
  27. Ganguly, P., El-Jawhari, J. J., Giannoudis, P. V., Burska, A. N., Ponchel, F. and Jones, E. A. (2017) Age-related changes in bone marrow mesenchymal stromal cells: a potential impact on osteoporosis and osteoarthritis development. Cell Transplant. 26, 1520-1529. https://doi.org/10.1177/0963689717721201
  28. Gibson, M., Brown, S. G. and Brown, N. O. (2017) Semitendinosus myopathy and treatment with adipose-derived stem cells in working German shepherd police dogs. Can. Vet. J. 58, 241-246.
  29. Glennie, S., Soeiro, I., Dyson, P. J., Lam, E. W. and Dazzi, F. (2005) Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105, 2821-2827. https://doi.org/10.1182/blood-2004-09-3696
  30. Guercio, A., Di Marco, P., Casella, S., Cannella, V., Russotto, L., Purpari, G., Di Bella, S. and Piccione, G. (2012) Production of canine mesenchymal stem cells from adipose tissue and their application in dogs with chronic osteoarthritis of the humeroradial joints. Cell Biol. Int. 36, 189-194. https://doi.org/10.1042/CBI20110304
  31. Hakki, S. S., Turac, G., Bozkurt, S. B., Kayis, S. A., Hakki, E. E., Sahin, E., Subasi, C. and Karaoz, E. (2017) Comparison of different sources of mesenchymal stem cells: palatal versus lipoaspirated adipose tissue. Cells Tissues Organs 204, 228-240. https://doi.org/10.1159/000478998
  32. Han, S. M., Kim, H. T., Kim, K. W., Jeon, K. O., Seo, K. W., Choi, E. W. and Youn, H. Y. (2015) CTLA4 overexpressing adipose tissuederived mesenchymal stem cell therapy in a dog with steroid-refractory pemphigus foliaceus. BMC Vet. Res. 11, 49. https://doi.org/10.1186/s12917-015-0371-3
  33. Jacobs, S. A., Roobrouck, V. D., Verfaillie, C. M. and Van Gool, S. W. (2013) Immunological characteristics of human mesenchymal stem cells and multipotent adult progenitor cells. Immunol. Cell Biol. 91, 32-39. https://doi.org/10.1038/icb.2012.64
  34. Kaewsuwan, S., Song, S. Y., Kim, J. H. and Sung, J. H. (2012) Mimicking the functional niche of adipose-derived stem cells for regenerative medicine. Expert Opin. Biol. Ther. 12, 1575-1588. https://doi.org/10.1517/14712598.2012.721763
  35. Kalinski, P. (2012) Regulation of immune responses by prostaglandin E2. J. Immunol. 188, 21-28. https://doi.org/10.4049/jimmunol.1101029
  36. Kang, J. W., Kang, K. S., Koo, H. C., Park, J. R., Choi, E. W. and Park, Y. H. (2008) Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Dev. 17, 681-693. https://doi.org/10.1089/scd.2007.0153
  37. Kim, C. H., Lee, J. H., Won, J. H. and Cho, M. K. (2011) Mesenchymal stem cells improve wound healing in vivo via early activation of matrix metalloproteinase-9 and vascular endothelial growth factor. J. Korean Med. Sci. 26, 726-733. https://doi.org/10.3346/jkms.2011.26.6.726
  38. Kim, H. S., Kim, K. H., Kim, S. H., Kim, Y. S., Koo, K. T., Kim, T. I., Seol, Y. J., Ku, Y., Rhyu, I. C., Chung, C. P. and Lee, Y. M. (2010) Immunomodulatory effect of canine periodontal ligament stem cells on allogenic and xenogenic peripheral blood mononuclear cells. J. Periodontal. Implant. Sci. 40, 265-270. https://doi.org/10.5051/jpis.2010.40.6.265
  39. Kim, H. W., Song, W. J., Li, Q., Han, S. M., Jeon, K. O., Park, S. C., Ryu, M. O., Chae, H. K., Kyeong, K. and Youn, H. Y. (2016) Canine adipose tissue-derived mesenchymal stem cells ameliorate severe acute pancreatitis by regulating T cells in rats. J. Vet. Sci. 17, 539-548. https://doi.org/10.4142/jvs.2016.17.4.539
  40. Kisiel, A. H., McDuffee, L. A., Masaoud, E., Bailey, T. R., Esparza Gonzalez, B. P. and Nino-Fong, R. (2012) Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Am. J. Vet. Res. 73, 1305-1317. https://doi.org/10.2460/ajvr.73.8.1305
  41. Koch, T. G., Heerkens, T., Thomsen, P. D. and Betts, D. H. (2007) Isolation of mesenchymal stem cells from equine umbilical cord blood. BMC Biotechnol. 7, 26. https://doi.org/10.1186/1472-6750-7-26
  42. Kondo, M., Yamaoka, K., Sakata, K., Sonomoto, K., Lin, L., Nakano, K. and Tanaka, Y. (2015) Contribution of the Interleukin-6/STAT-3 signaling pathway to chondrogenic differentiation of human mesenchymal stem cells. Arthritis Rheumatol. 67, 1250-1260. https://doi.org/10.1002/art.39036
  43. Kopen, G. C., Prockop, D. J. and Phinney, D. G. (1999) Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U.S.A. 96, 10711-10716. https://doi.org/10.1073/pnas.96.19.10711
  44. Krampera, M., Galipeau, J., Shi, Y., Tarte, K. and Sensebe, L. (2013) Immunological characterization of multipotent mesenchymal stromal cells--The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy 15, 1054-1061. https://doi.org/10.1016/j.jcyt.2013.02.010
  45. Lawson, J., Elliott, J., Wheeler-Jones, C., Syme, H. and Jepson, R. (2015) Renal fibrosis in feline chronic kidney disease: known mediators and mechanisms of injury. Vet. J. 203, 18-26. https://doi.org/10.1016/j.tvjl.2014.10.009
  46. Le Blanc, K., Tammik, L., Sundberg, B., Haynesworth, S. E. and Ringden, O. (2003) Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57, 11-20. https://doi.org/10.1046/j.1365-3083.2003.01176.x
  47. Lee, J. Y., Uzuka, Y., Tanabe, S. and Sarashina, T. (2004) Prevalence of thyroglobulin autoantibodies detected by enzyme-linked immunosorbent assay of canine serum in hypothyroid, obese and healthy dogs in Japan. Res. Vet. Sci. 76, 129-132. https://doi.org/10.1016/j.rvsc.2003.10.002
  48. Lee, W. S., Suzuki, Y., Graves, S. S., Iwata, M., Venkataraman, G. M., Mielcarek, M., Peterson, L. J., Ikehara, S., Torok-Storb, B. and Storb, R. (2011) Canine bone marrow-derived mesenchymal stromal cells suppress alloreactive lymphocyte proliferation in vitro but fail to enhance engraftment in canine bone marrow transplantation. Biol. Blood Marrow Transplant. 17, 465-475. https://doi.org/10.1016/j.bbmt.2010.04.016
  49. Lei, J., Wang, Z., Hui, D., Yu, W., Zhou, D., Xia, W., Chen, C., Zhang, Q., Wang, Z., Zhang, Q. and Xiang, A. P. (2011) Ligation of TLR2 and TLR4 on murine bone marrow-derived mesenchymal stem cells triggers differential effects on their immunosuppressive activity. Cell. Immunol. 271, 147-156. https://doi.org/10.1016/j.cellimm.2011.06.014
  50. Lim, J. Y., Im, K. I., Lee, E. S., Kim, N., Nam, Y. S., Jeon, Y. W. and Cho, S. G. (2016) Enhanced immunoregulation of mesenchymal stem cells by IL-10-producing type 1 regulatory T cells in collagen-induced arthritis. Sci. Rep. 6, 26851. https://doi.org/10.1038/srep26851
  51. Liu, Y. L., Liu, W. H., Sun, J., Hou, T. J., Liu, Y. M., Liu, H. R., Luo, Y. H., Zhao, N. N., Tang, Y. and Deng, F. M. (2014) Mesenchymal stem cell-mediated suppression of hypertrophic scarring is p53 dependent in a rabbit ear model. Stem Cell Res. Ther. 5, 136. https://doi.org/10.1186/scrt526
  52. Lo, B. and Parham, L. (2009) Ethical issues in stem cell research. Endocr. Rev. 30, 204-213. https://doi.org/10.1210/er.2008-0031
  53. Ma, S., Chen, X., Wang, L., Wei, Y., Ni, Y., Chu, Y., Liu, Y., Zhu, H., Zheng, R. and Zhang, Y. (2017) Repairing effects of ICAM-1-expressing mesenchymal stem cells in mice with autoimmune thyroiditis. Exp. Ther. Med. 13, 1295-1302. https://doi.org/10.3892/etm.2017.4131
  54. Mahla, R. S. (2016) Stem cells applications in regenerative medicine and disease therapeutics. Int. J. Cell Biol. 2016, 6940283. https://doi.org/10.1155/2016/6940283
  55. Matsui, F., Babitz, S. A., Rhee, A., Hile, K. L., Zhang, H. and Meldrum, K. K. (2017) Mesenchymal stem cells protect against obstruction-induced renal fibrosis by decreasing STAT3 activation and STAT3-dependent MMP-9 production. Am. J. Physiol. Renal Physiol. 312, F25-F32. https://doi.org/10.1152/ajprenal.00311.2016
  56. Matsui, F. and Meldrum, K. K. (2012) The role of the Janus kinase family/signal transducer and activator of transcription signaling pathway in fibrotic renal disease. J. Surg. Res. 178, 339-345. https://doi.org/10.1016/j.jss.2012.06.050
  57. Mrozik, K. M., Zilm, P. S., Bagley, C. J., Hack, S., Hoffmann, P., Gronthos, S. and Bartold, P. M. (2010) Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: analysis of differentially expressed proteins. Stem Cells De. 19, 1485-1499. https://doi.org/10.1089/scd.2009.0446
  58. Najimi, M., Berardis, S., El-Kehdy, H., Rosseels, V., Evraerts, J., Lombard, C., El Taghdouini, A., Henriet, P., van Grunsven, L. and Sokal, E. M. (2017) Human liver mesenchymal stem/progenitor cells inhibit hepatic stellate cell activation: in vitro and in vivo evaluation. Stem Cell Res. Ther. 8, 131. https://doi.org/10.1186/s13287-017-0575-5
  59. Nordgren, T. M., Bailey, K. L., Heires, A. J., Katafiasz, D. and Romberger, D. J. (2018) Effects of agricultural organic dusts on human lung-resident mesenchymal stem (stromal) cell function. Toxicol. Sci. 162, 635-644. https://doi.org/10.1093/toxsci/kfx286
  60. Otabe, K., Muneta, T., Kawashima, N., Suda, H., Tsuji, K. and Sekiya, I. (2012) Comparison of gingiva, dental pulp, and periodontal ligament cells from the standpoint of mesenchymal stem cell properties. Cell Med. 4, 13-21. https://doi.org/10.3727/215517912X653319
  61. Plumas, J., Chaperot, L., Richard, M. J., Molens, J. P., Bensa, J. C. and Favrot, M. C. (2005) Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 19, 1597-1604. https://doi.org/10.1038/sj.leu.2403871
  62. Raabe, O., Shell, K., Goessl, A., Crispens, C., Delhasse, Y., Eva, A., Scheiner-Bobis, G., Wenisch, S. and Arnhold, S. (2013) Effect of extracorporeal shock wave on proliferation and differentiation of equine adipose tissue-derived mesenchymal stem cells in vitro. Am. J. Stem Cells. 8, 2, 62-73.
  63. Rawlings, J. S., Rosler, K. M. and Harrison, D. A. (2004) The JAK/STAT signaling pathway. J Cell Sci. 117, 1281-1283. https://doi.org/10.1242/jcs.00963
  64. Reiter, J., Drummond, S., Sammour, I., Huang, J., Florea, V., Dornas, P., Hare, J. M., Rodrigues, C. O. and Young, K. C. (2017) Stromal derived factor-1 mediates the lung regenerative effects of mesenchymal stem cells in a rodent model of bronchopulmonary dysplasia. Respir. Res. 18, 137. https://doi.org/10.1186/s12931-017-0620-z
  65. Ren, H., Sang, Y., Zhang, F., Liu, Z., Qi, N. and Chen, Y. (2016) Comparative analysis of human mesenchymal stem cells from umbilical cord, dental pulp, and menstrual blood as sources for cell therapy. Stem Cells Int. 2016, 3516574.
  66. Rhee, K. J., Lee, J. I. and Eom, Y. W. (2015) Mesenchymal Stem Cell-Mediated Effects of Tumor Support or Suppression. Int. J. Mol. Sci. 16, 30015-30033. https://doi.org/10.3390/ijms161226215
  67. Ryan, J. M., Barry, F., Murphy, J. M. and Mahon, B. P. (2007) Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin. Exp. Immunol. 149, 353-363. https://doi.org/10.1111/j.1365-2249.2007.03422.x
  68. Sato, K., Ozaki, K., Oh, I., Meguro, A., Hatanaka, K., Nagai, T., Muroi, K. and Ozawa, K. (2007) Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109, 228-234. https://doi.org/10.1182/blood-2006-02-002246
  69. Schlosser, S., Dennler, C., Schweizer, R., Eberli, D., Stein, J. V., Enzmann, V., Giovanoli, P., Erni, D. and Plock, J. A. (2012) Paracrine effects of mesenchymal stem cells enhance vascular regeneration in ischemic murine skin. Microvasc. Res. 83, 267-275. https://doi.org/10.1016/j.mvr.2012.02.011
  70. Schuh, E. M., Friedman, M. S., Carrade, D. D., Li, J., Heeke, D., Oyserman, S. M., Galuppo, L. D., Lara, D. J., Walker, N. J., Ferraro, G. L., Owens, S. D. and Borjesson, D. L. (2009) Identification of variables that optimize isolation and culture of multipotent mesenchymal stem cells from equine umbilical-cord blood. Am. J. Vet. Res. 70, 1526-1535. https://doi.org/10.2460/ajvr.70.12.1526
  71. Shabbir, A., Zisa, D., Lin, H., Mastri, M., Roloff, G., Suzuki, G. and Lee, T. (2010) Activation of host tissue trophic factors through JAK-STAT3 signaling: a mechanism of mesenchymal stem cell-mediated cardiac repair. Am. J. Physiol. Heart Circ. Physiol. 299, H1428-H1438. https://doi.org/10.1152/ajpheart.00488.2010
  72. Sharma, R. R., Pollock, K., Hubel, A. and McKenna, D. (2014) Mesenchymal stem or stromal cells: a review of clinical applications and manufacturing practices. Transfusion 54, 1418-1437. https://doi.org/10.1111/trf.12421
  73. Singer, N. G. and Caplan, A. I. (2011) Mesenchymal stem cells: mechanisms of inflammation. Annu. Rev. Pathol. 6, 457-478. https://doi.org/10.1146/annurev-pathol-011110-130230
  74. Sousa, M. G., Paulino-Junior, D., Pascon, J. P., Pereira-Neto, G. B., Carareto, R., Champion, T. and Camacho, A. A. (2011) Cardiac function in dogs with chronic Chagas cardiomyopathy undergoing autologous stem cell transplantation into the coronary arteries. Can. Vet. J. 52, 869-874.
  75. Squillaro, T., Peluso, G. and Galderisi, U. (2016) Clinical trials with mesenchymal stem cells: an update. Cell Transplant. 25, 829-848. https://doi.org/10.3727/096368915X689622
  76. Strioga, M., Viswanathan, S., Darinskas, A., Slaby, O. and Michalek, J. (2012) Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev. 21, 2724-2752. https://doi.org/10.1089/scd.2011.0722
  77. Teixeira, F. G., Panchalingam, K. M., Anjo, S. I., Manadas, B., Pereira, R., Sousa, N., Salgado, A. J. and Behie, L. A. (2015) Do hypoxia/normoxia culturing conditions change the neuroregulatory profile of Wharton Jelly mesenchymal stem cell secretome? Stem Cell Res. Ther. 6, 133. https://doi.org/10.1186/s13287-015-0124-z
  78. Tidd, N., Michelsen, J., Hilbert, B. and Quinn, J. C. (2017) Minicircle mediated gene delivery to canine and equine mesenchymal stem cells. Int. J. Mol. Sci. 18, E819. https://doi.org/10.3390/ijms18040819
  79. Ulrich, D., Muralitharan, R. and Gargett, C. E. (2013) Toward the use of endometrial and menstrual blood mesenchymal stem cells for cell-based therapies. Expert Opin. Biol. Ther. 13, 1387-1400. https://doi.org/10.1517/14712598.2013.826187
  80. Ullah, I., Subbarao, R. B. and Rho, G. J. (2015) Human mesenchymal stem cells - current trends and future prospective. Biosci. Rep. 35, e00191. https://doi.org/10.1042/BSR20150025
  81. Vidal, M. A., Robinson, S. O., Lopez, M. J., Paulsen, D. B., Borkhsenious, O., Johnson, J. R., Moore, R. M. and Gimble, J. M. (2008) Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet. Surg. 37, 713-724. https://doi.org/10.1111/j.1532-950X.2008.00462.x
  82. Volk, S. W. and Theoret, C. (2013) Translating stem cell therapies: the role of companion animals in regenerative medicine. Wound Repair Regen. 21, 382-394. https://doi.org/10.1111/wrr.12044
  83. Wipff, P. J. and Hinz, B. (2008) Integrins and the activation of latent transforming growth factor beta1 - an intimate relationship. Eur. J. Cell Biol. 87, 601-615. https://doi.org/10.1016/j.ejcb.2008.01.012
  84. Xiong, H., Bai, C., Wu, S., Gao, Y., Lu, T., Hu, Q., Guan, W. and Ma, Y. (2014) Biological characterization of mesenchymal stem cells from bovine umbilical cord. Animal Cells and Systems 18, 59-67. https://doi.org/10.1080/19768354.2014.880370
  85. Zhu, W. and Liang, M. (2015) Periodontal ligament stem cells: current status, concerns, and future prospects. Stem Cells Int. 2015, 972313. https://doi.org/10.1155/2015/972313

피인용 문헌

  1. Two-Cell Spheroid Angiogenesis Assay System Using Both Endothelial Colony Forming Cells and Mesenchymal Stem Cells vol.26, pp.5, 2019, https://doi.org/10.4062/biomolther.2018.134
  2. Case Report: Exploratory treatment with multiple intravenous infusion of the autologous adipose tissue-derived mesenchymal stem cells for the treatment of Diamond-Blackfan anemia patient vol.8, 2019, https://doi.org/10.12688/f1000research.20391.1
  3. Amyloid-like peptide nanofibrils as scaffolds for tissue engineering: Progress and challenges (Review) vol.14, pp.4, 2019, https://doi.org/10.1116/1.5098332
  4. In vitro differentiation of conjunctiva mesenchymal stem cells into insulin producing cells on natural and synthetic electrospun scaffolds vol.62, 2019, https://doi.org/10.1016/j.biologicals.2019.10.004
  5. Mesenchymal stem cells therapy in companion animals: useful for immune-mediated diseases? vol.15, 2019, https://doi.org/10.1186/s12917-019-2087-2
  6. The Exposure to Osteoarthritic Synovial Fluid Enhances the Immunomodulatory Profile of Adipose Mesenchymal Stem Cell Secretome vol.2020, 2019, https://doi.org/10.1155/2020/4058760
  7. Human Mesenchymal Stem Cells for Spinal Cord Injury vol.15, 2019, https://doi.org/10.2174/1574888x15666200316164051
  8. Immunomodulation of MSCs and MSC-Derived Extracellular Vesicles in Osteoarthritis vol.8, 2019, https://doi.org/10.3389/fbioe.2020.575057
  9. Pre-conditioning of Equine Bone Marrow-Derived Mesenchymal Stromal Cells Increases Their Immunomodulatory Capacity vol.7, 2019, https://doi.org/10.3389/fvets.2020.00318
  10. Mesenchymal Stromal Cell Immunology for Efficient and Safe Treatment of Osteoarthritis vol.8, 2019, https://doi.org/10.3389/fcell.2020.567813
  11. Mesenchymal stem cell-derived extracellular vesicles as a new therapeutic strategy for ocular diseases vol.12, pp.3, 2020, https://doi.org/10.4252/wjsc.v12.i3.178
  12. Melatonin and Mesenchymal Stem Cells as a Key for Functional Integrity for Liver Cancer Treatment vol.21, pp.12, 2019, https://doi.org/10.3390/ijms21124521
  13. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy vol.77, pp.14, 2020, https://doi.org/10.1007/s00018-020-03454-6
  14. Transcriptomic Analysis of Human Mesenchymal Stem Cell Therapy in Incontinent Rat Injured Urethra vol.26, pp.13, 2019, https://doi.org/10.1089/ten.tea.2020.0033
  15. Defining a Regulatory Strategy for ATMP/Aerosol Delivery Device Combinations in the Treatment of Respiratory Disease vol.12, pp.10, 2019, https://doi.org/10.3390/pharmaceutics12100922
  16. Medicinal signaling cells: A potential antimicrobial drug store vol.235, pp.11, 2019, https://doi.org/10.1002/jcp.29728
  17. Cryopreservation of Mesenchymal Stem Cells Using Medical Grade Ice Nucleation Inducer vol.21, pp.22, 2019, https://doi.org/10.3390/ijms21228579
  18. Molecular Mechanisms Responsible for Mesenchymal Stem Cell-Based Treatment of Viral Diseases vol.10, pp.4, 2021, https://doi.org/10.3390/pathogens10040409
  19. Transcriptional Profile of Cytokines, Regulatory Mediators and TLR in Mesenchymal Stromal Cells after Inflammatory Signaling and Cell-Passaging vol.22, pp.14, 2021, https://doi.org/10.3390/ijms22147309
  20. Myeloid-Derived Suppressor Cells and Mesenchymal Stem/Stromal Cells in Myeloid Malignancies vol.10, pp.13, 2019, https://doi.org/10.3390/jcm10132788
  21. Toward a Better Regeneration through Implant‐Mediated Immunomodulation: Harnessing the Immune Responses vol.8, pp.16, 2019, https://doi.org/10.1002/advs.202100446
  22. What Molecular Recognition Systems Do Mesenchymal Stem Cells/Medicinal Signaling Cells (MSC) Use to Facilitate Cell-Cell and Cell Matrix Interactions? A Review of Evidence and Options vol.22, pp.16, 2019, https://doi.org/10.3390/ijms22168637
  23. Mesenchymal Stromal Cells: Potential Option for COVID-19 Treatment vol.13, pp.9, 2019, https://doi.org/10.3390/pharmaceutics13091481
  24. Influence of extracellular nanovesicles derived from adipose‑derived stem cells on nucleus pulposus cell from patients with intervertebral disc degeneration vol.22, pp.6, 2021, https://doi.org/10.3892/etm.2021.10866
  25. Mesenchymal stem cell therapies for Alzheimer’s disease: preclinical studies vol.36, pp.7, 2019, https://doi.org/10.1007/s11011-021-00777-6
  26. Immunomodulation and Regenerative Capacity of MSCs for Long-COVID vol.22, pp.22, 2019, https://doi.org/10.3390/ijms222212421
  27. Fibronectin-coating enhances attachment and proliferation of mesenchymal stem cells on a polyurethane meniscal scaffold vol.18, 2019, https://doi.org/10.1016/j.reth.2021.11.001
  28. Basement membrane proteins modulate cell migration on bovine pericardium extracellular matrix scaffold vol.11, pp.1, 2019, https://doi.org/10.1038/s41598-021-84161-5