Therapeutic and Safety Promise of Mesenchymal Stem Cells for Liver Failure: From Preclinical Experiment to Clinical Application


Cite item

Full Text

Abstract

:Liver failure (LF) is serious liver damage caused by multiple factors, resulting in severe impairment or decompensation of liver synthesis, detoxification, metabolism, and biotransformation. The general prognosis of LF is poor with high mortality in non-transplant patients. The clinical treatments for LF are mainly internal medicine comprehensive care, artificial liver support system, and liver transplantation. However, none of the above treatment strategies can solve the problems of all liver failure patients and has its own limitations. Mesenchymal stem cells (MSCs) are a kind of stem cells with multidirectional differentiation potential and paracrine function, which play an important role in immune regulation and tissue regeneration. In recent years, MSCs have shown multiple advantages in the treatment of LF in pre-clinical experiments and clinical trials. In this work, we reviewed the biological characteristics of MSCs, the possible molecular mechanisms of MSCs in the treatment of liver failure, animal experiments, and clinical application, and also discussed the existing problems of MSCs in the treatment of liver failure.

About the authors

Qiong Xie

National Engineering Research Center of Cell Products,, AmCellGene Engineering Co., Ltd,

Email: info@benthamscience.net

Jundong Gu

National Engineering Research Center of Cell Products, AmCellGene Engineering Co., Ltd,

Author for correspondence.
Email: info@benthamscience.net

References

  1. Navarro, V.J.; Senior, J.R. Drug-related hepatotoxicity. N. Engl. J. Med., 2006, 354(7), 731-739. doi: 10.1056/NEJMra052270 PMID: 16481640
  2. Wang, L.; Geng, J. Acute hepatitis E virus infection in patients with acute liver failure in China: Not quite an uncommon cause. Hepatology, 2017, 65(5), 1769-1770. doi: 10.1002/hep.28939 PMID: 27862123
  3. Li, M.; Wang, Z.Q.; Zhang, L.; Zheng, H.; Liu, D.W.; Zhou, M.G. Burden of cirrhosis and other chronic liver diseases caused by specific etiologies in china, 1990-2016: Findings from the global burden of disease study 2016. Biomed. Environ. Sci., 2020, 33(1), 1-10. doi: 10.3967/bes2020.001 PMID: 32029053
  4. Wang, F.S.; Fan, J.G.; Zhang, Z.; Gao, B.; Wang, H.Y. The global burden of liver disease: The major impact of China. Hepatology, 2014, 60(6), 2099-2108. doi: 10.1002/hep.27406 PMID: 25164003
  5. Naghavi, M.; Abajobir, A.A.; Abbafati, C. Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet, 2017, 390(10100), 1151-1210. doi: 10.1016/S0140-6736(17)32152-9 PMID: 28919116
  6. Allen, A.M.; Kim, W.R.; Moriarty, J.P.; Shah, N.D.; Larson, J.J.; Kamath, P.S. Time trends in the health care burden and mortality of acute on chronic liver failure in the United States. Hepatology, 2016, 64(6), 2165-2172. doi: 10.1002/hep.28812 PMID: 27696493
  7. Xue, R.; Meng, Q. The management of glucocorticoid therapy in liver failure. Front. Immunol., 2019, 10, 2490. doi: 10.3389/fimmu.2019.02490 PMID: 31749799
  8. Trovato, F.M.; Rabinowich, L.; McPhail, M.J.W. Update on the management of acute liver failure. Curr. Opin. Crit. Care, 2019, 25(2), 157-164. doi: 10.1097/MCC.0000000000000583 PMID: 30694840
  9. Escorsell, À.; Castellote, J.; Sánchez-Delgado, J.; Charco, R.; Crespo, G.; Fernández, J. Management of acute liver failure. Clinical guideline from the catalan society of digestology. Gastroenterol. Hepatol., 2019, 42(1), 51-64. doi: 10.1016/j.gastrohep.2018.07.013 PMID: 30309739
  10. Rela, M.; Kaliamoorthy, I.; Reddy, M.S. Current status of auxiliary partial orthotopic liver transplantation for acute liver failure. Liver Transpl., 2016, 22(9), 1265-1274. doi: 10.1002/lt.24509 PMID: 27357489
  11. Szydlak, R. Mesenchymal stem cells’ homing and cardiac tissue repair. Acta Biochim. Pol., 2019, 66(4), 483-489. doi: 10.18388/abp.2019_2890 PMID: 31834688
  12. Jo, H.; Brito, S.; Kwak, B.M.; Park, S.; Lee, M.G.; Bin, B.H. Applications of mesenchymal stem cells in skin regeneration and rejuvenation. Int. J. Mol. Sci., 2021, 22(5), 2410. doi: 10.3390/ijms22052410 PMID: 33673711
  13. Asgari Taei, A.; Nasoohi, S.; Hassanzadeh, G.; Kadivar, M.; Dargahi, L.; Farahmandfar, M. Enhancement of angiogenesis and neurogenesis by intracerebroventricular injection of secretome from human embryonic stem cell-derived mesenchymal stem cells in ischemic stroke model. Biomed. Pharmacother., 2021, 140, 111709. doi: 10.1016/j.biopha.2021.111709 PMID: 34020250
  14. Gao, L.; Peng, Y.; Xu, W. Progress in stem cell therapy for spinal cord injury. Stem Cells Int., 2020, 2020, 1-16. doi: 10.1155/2020/2853650 PMID: 33204276
  15. Friedenstein, A.J.; Chailakhjan, R.K.; Lalykina, K.S. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Prolif., 1970, 3(4), 393-403. doi: 10.1111/j.1365-2184.1970.tb00347.x PMID: 5523063
  16. Dominici, M.; Le Blanc, K.; Mueller, I. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4), 315-317. doi: 10.1080/14653240600855905 PMID: 16923606
  17. Wang, S.; Qu, X.; Zhao, R.C. Clinical applications of mesenchymal stem cells. J. Hematol. Oncol., 2012, 5(1), 19. doi: 10.1186/1756-8722-5-19 PMID: 22546280
  18. Zhao, K.; Liu, Q. The clinical application of mesenchymal stromal cells in hematopoietic stem cell transplantation. J. Hematol. Oncol., 2016, 9(1), 46. doi: 10.1186/s13045-016-0276-z PMID: 27193054
  19. Najar, M.; Raicevic, G.; Boufker, H.I. Mesenchymal stromal cells use PGE2 to modulate activation and proliferation of lymphocyte subsets: Combined comparison of adipose tissue, Wharton’s Jelly and bone marrow sources. Cell. Immunol., 2010, 264(2), 171-179. doi: 10.1016/j.cellimm.2010.06.006 PMID: 20619400
  20. Montesinos, J.J.; Flores-Figueroa, E.; Castillo-Medina, S. Human mesenchymal stromal cells from adult and neonatal sources: Comparative analysis of their morphology, immunophenotype, differentiation patterns and neural protein expression. Cytotherapy, 2009, 11(2), 163-176. doi: 10.1080/14653240802582075 PMID: 19152152
  21. Montesinos, J.J.; Mora-García, M.L.; Mayani, H. In vitro evidence of the presence of mesenchymal stromal cells in cervical cancer and their role in protecting cancer cells from cytotoxic T cell activity. Stem Cells Dev., 2013, 22(18), 2508-2519. doi: 10.1089/scd.2013.0084 PMID: 23656504
  22. Lu, L.L.; Liu, Y.J.; Yang, S.G. Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica, 2006, 91(8), 1017-1026. PMID: 16870554
  23. McGuirk, J.; Smith, J.; Divine, C.; Zuniga, M.; Weiss, M. Wharton’s jelly-derived mesenchymal stromal cells as a promising cellular therapeutic strategy for the management of graft-versus-host disease. Pharmaceuticals, 2015, 8(2), 196-220. doi: 10.3390/ph8020196 PMID: 25894816
  24. Uzieliene, I.; Urbonaite, G.; Tachtamisevaite, Z.; Mobasheri, A.; Bernotiene, E. The Potential of menstrual blood-derived mesenchymal stem cells for cartilage repair and regeneration: Novel aspects. Stem Cells Int., 2018, 2018, 1-10. doi: 10.1155/2018/5748126 PMID: 30627174
  25. Staniowski, T.; Zawadzka-Knefel, A.; Skośkiewicz-Malinowska, K. Therapeutic potential of dental pulp stem cells according to different transplant types. Molecules, 2021, 26(24), 7423. doi: 10.3390/molecules26247423 PMID: 34946506
  26. Chen, JY Characteristics of menstrual-blood-derived endometrial stem cells and their role in liver injury models., 2014.
  27. Deuse, T.; Stubbendorff, M.; Tang-Quan, K. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant., 2011, 20(5), 655-667. doi: 10.3727/096368910X536473 PMID: 21054940
  28. Pelosi, E.; Castelli, G.; Testa, U. Human umbilical cord is a unique and safe source of various types of stem cells suitable for treatment of hematological diseases and for regenerative medicine. Blood Cells Mol. Dis., 2012, 49(1), 20-28. doi: 10.1016/j.bcmd.2012.02.007 PMID: 22446302
  29. Kita, K.; Gauglitz, G.G.; Phan, T.T.; Herndon, D.N.; Jeschke, M.G. Isolation and characterization of mesenchymal stem cells from the sub-amniotic human umbilical cord lining membrane. Stem Cells Dev., 2010, 19(4), 491-502. doi: 10.1089/scd.2009.0192 PMID: 19635009
  30. Tipnis, S.; Viswanathan, C.; Majumdar, A.S. Immunosuppressive properties of human umbilical cord-derived mesenchymal stem cells: Role of B7-H1 and IDO. Immunol. Cell Biol., 2010, 88(8), 795-806. doi: 10.1038/icb.2010.47 PMID: 20386557
  31. Chatterjee, D.; Marquardt, N.; Tufa, D.M. Human umbilical cord-derived mesenchymal stem cells utilize activin-a to suppress interferon-Î3 production by natural killer cells. Front. Immunol., 2014, 5, 662. doi: 10.3389/fimmu.2014.00662 PMID: 25584044
  32. Weiss, M.L.; Anderson, C.; Medicetty, S. Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells, 2008, 26(11), 2865-2874. doi: 10.1634/stemcells.2007-1028 PMID: 18703664
  33. Volarevic, V.; Gazdic, M.; Simovic Markovic, B.; Jovicic, N.; Djonov, V.; Arsenijevic, N. Mesenchymal stem cell-derived factors: Immuno-modulatory effects and therapeutic potential. Biofactors, 2017, 43(5), 633-644. doi: 10.1002/biof.1374 PMID: 28718997
  34. Aqmasheh, S. Shamsasanjan, Akbarzadehlaleh P, Pashoutan Sarvar D, Timari H. Effects of mesenchymal stem cell derivatives on hematopoiesis and hematopoietic stem cells. Adv. Pharm. Bull., 2017, 7(2), 165-177. doi: 10.15171/apb.2017.021 PMID: 28761818
  35. Liang, L.; Li, Z.; Ma, T. Transplantation of human placenta-derived mesenchymal stem cells alleviates critical limb ischemia in diabetic nude rats. Cell Transplant., 2017, 26(1), 45-61. doi: 10.3727/096368916X692726 PMID: 27501782
  36. Meuleman, N.; Tondreau, T.; Ahmad, I. Infusion of mesenchymal stromal cells can aid hematopoietic recovery following allogeneic hematopoietic stem cell myeloablative transplant: A pilot study. Stem Cells Dev., 2009, 18(9), 1247-1252. doi: 10.1089/scd.2009.0029 PMID: 19309241
  37. Eggenhofer, E.; Benseler, V.; Kroemer, A. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front. Immunol., 2012, 3, 297. doi: 10.3389/fimmu.2012.00297 PMID: 23056000
  38. Zachar, L.; Bačenková, D.; Rosocha, J. Activation, homing, and role of the mesenchymal stem cells in the inflammatory environment. J. Inflamm. Res., 2016, 9, 231-240. doi: 10.2147/JIR.S121994 PMID: 28008279
  39. Ullah, M.; Liu, D.D.; Thakor, A.S. Mesenchymal stromal cell homing: Mechanisms and strategies for improvement. iScience, 2019, 15, 421-438. doi: 10.1016/j.isci.2019.05.004 PMID: 31121468
  40. Zhou, R.; Li, Z.; He, C. Human umbilical cord mesenchymal stem cells and derived hepatocyte-like cells exhibit similar therapeutic effects on an acute liver failure mouse model. PLoS One, 2014, 9(8), e104392. doi: 10.1371/journal.pone.0104392 PMID: 25101638
  41. Zhao, Q.J.; Ren, H.Y.; Chi, Y. Umbilical cord mesenchymal stem cell for chronic experimental liver injury. Chinese J Cell Stem Cell, 2014, 4(4), 6. doi: 10.3877/cma.j.issn.2095-1221.2014.04.005
  42. Liu, Z.; Meng, F.; Li, C. Human umbilical cord mesenchymal stromal cells rescue mice from acetaminophen-induced acute liver failure. Cytotherapy, 2014, 16(9), 1207-1219. doi: 10.1016/j.jcyt.2014.05.018 PMID: 25108650
  43. Stock, P.; Brückner, S.; Ebensing, S.; Hempel, M.; Dollinger, M.M.; Christ, B. The generation of hepatocytes from mesenchymal stem cells and engraftment into murine liver. Nat. Protoc., 2010, 5(4), 617-627. doi: 10.1038/nprot.2010.7 PMID: 20224562
  44. Gu, W.; Gu, J. Homing mechanism of umbilical cord mesenchymal stem cells. Chinese J Tissue Eng Res, 2013, 6, 6. doi: 10.3969/j.issn.2095-4344.2013.06.031
  45. Yu, Y.; Yoo, S.M.; Park, H.H. Preconditioning with interleukin-1 beta and interferon-gamma enhances the efficacy of human umbilical cord blood-derived mesenchymal stem cells-based therapy via enhancing prostaglandin E2 secretion and indoleamine 2,3-dioxygenase activity in dextran sulfate sodium-induced colitis. J. Tissue Eng. Regen. Med., 2019, 13(10), 1792-1804. doi: 10.1002/term.2930 PMID: 31293088
  46. Singer, N.G.; Caplan, A.I. Mesenchymal stem cells: Mechanisms of inflammation. Annu. Rev. Pathol., 2011, 6(1), 457-478. doi: 10.1146/annurev-pathol-011110-130230 PMID: 21073342
  47. Xu, W.; He, H.; Pan, S. Combination treatments of plasma exchange and umbilical cord-derived mesenchymal stem cell transplantation for patients with hepatitis b virus-related acute-on-chronic liver failure: A clinical trial in China. Stem Cells Int., 2019, 2019, 1-10. doi: 10.1155/2019/4130757 PMID: 30863450
  48. Zhang, Z.; Lin, H.; Shi, M. Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients. J. Gastroenterol. Hepatol., 2012, 27(Suppl. 2), 112-120. doi: 10.1111/j.1440-1746.2011.07024.x PMID: 22320928
  49. Wynn, T.; Barron, L. Macrophages: Master regulators of inflammation and fibrosis. Semin. Liver Dis., 2010, 30(3), 245-257. doi: 10.1055/s-0030-1255354 PMID: 20665377
  50. Kudlik, G.; Hegyi, B.; Czibula, Á.; Monostori, É.; Buday, L.; Uher, F. Mesenchymal stem cells promote macrophage polarization toward M2b-like cells. Exp. Cell Res., 2016, 348(1), 36-45. doi: 10.1016/j.yexcr.2016.08.022 PMID: 27578361
  51. Li, Y.W.; Zhang, C.; Sheng, Q.J.; Bai, H.; Ding, Y.; Dou, X.G. Mesenchymal stem cells rescue acute hepatic failure by polarizing M2 macrophages. World J. Gastroenterol., 2017, 23(45), 7978-7988. doi: 10.3748/wjg.v23.i45.7978 PMID: 29259373
  52. Guo, Z.; Su, W.; Zhou, R. Exosomal MATN3 of urine-derived stem cells ameliorates intervertebral disc degeneration by antisenescence effects and promotes npc proliferation and ecm synthesis by activating TGF-β. Oxid. Med. Cell. Longev., 2021, 2021, 1-18. doi: 10.1155/2021/5542241 PMID: 34136064
  53. Soliman, H.; Theret, M.; Scott, W. Multipotent stromal cells: One name, multiple identities. Cell Stem Cell, 2021, 28(10), 1690-1707. doi: 10.1016/j.stem.2021.09.001 PMID: 34624231
  54. Lee, C.; Kim, M.; Han, J.; Yoon, M.; Jung, Y. Mesenchymal stem cells influence activation of hepatic stellate cells, and constitute a promising therapy for liver fibrosis. Biomedicines, 2021, 9(11), 1598. doi: 10.3390/biomedicines9111598 PMID: 34829827
  55. Tan, Y.; Huang, Y.; Mei, R. HucMSC-derived exosomes delivered BECN1 induces ferroptosis of hepatic stellate cells via regulating the xCT/GPX4 axis. Cell Death Dis., 2022, 13(4), 319. doi: 10.1038/s41419-022-04764-2 PMID: 35395830
  56. Wang, J.; Bian, C.; Liao, L. Inhibition of hepatic stellate cells proliferation by mesenchymal stem cells and the possible mechanisms. Hepatol. Res., 2009, 39(12), 1219-1228. doi: 10.1111/j.1872-034X.2009.00564.x PMID: 19788697
  57. Yu, F.; Ji, S.; Su, L. Adipose-derived mesenchymal stem cells inhibit activation of hepatic stellate cells in vitro and ameliorate rat liver fibrosis in vivo. J. Formos. Med. Assoc., 2015, 114(2), 130-138. doi: 10.1016/j.jfma.2012.12.002 PMID: 25678175
  58. Chen, S. Xu, Lin N, Pan W, Hu K, Xu R. Activation of Notch1 signaling by marrow-derived mesenchymal stem cells through cell–cell contact inhibits proliferation of hepatic stellate cells. Life Sci., 2011, 89(25-26), 975-981. doi: 10.1016/j.lfs.2011.10.012 PMID: 22056375
  59. Bahrehbar, K.; Valojerdi, M.R.; Esfandiari, F.; Fathi, R.; Hassani, S.N.; Baharvand, H. Human embryonic stem cell-derived mesenchymal stem cells improved premature ovarian failure. World J. Stem Cells, 2020, 12(8), 857-878. doi: 10.4252/wjsc.v12.i8.857 PMID: 32952863
  60. Fox, J.M.; Chamberlain, G.; Ashton, B.A.; Middleton, J. Recent advances into the understanding of mesenchymal stem cell trafficking. Br. J. Haematol., 2007, 137(6), 491-502. doi: 10.1111/j.1365-2141.2007.06610.x PMID: 17539772
  61. Jiang, S.S.; Wang, F.; Yu, L.M. Immunomodulatory properties of mesenchymal stem cells and their application in organ transplantation. Chinese J Tissue Eng Res, 2019, 23(1), 7. doi: 10.3969/j.issn.2095-4344.1530
  62. Luz-Crawford, P.; Kurte, M.; Bravo-Alegría, J. Mesenchymal stem cells generate a CD4+CD25+Foxp3+ regulatory T cell population during the differentiation process of Th1 and Th17 cells. Stem Cell Res. Ther., 2013, 4(3), 65. doi: 10.1186/scrt216 PMID: 23734780
  63. Cargnoni, A.; Romele, P.; Bonassi Signoroni, P. Amniotic MSCs reduce pulmonary fibrosis by hampering lung B-cell recruitment, retention, and maturation. Stem Cells Transl. Med., 2020, 9(9), 1023-1035. doi: 10.1002/sctm.20-0068 PMID: 32452646
  64. Weiss, A.R.R.; Dahlke, M.H. Immunomodulation by mesenchymal stem cells (MSCs): Mechanisms of action of living, apoptotic, and dead MSCs. Front. Immunol., 2019, 10, 1191. doi: 10.3389/fimmu.2019.01191 PMID: 31214172
  65. Nauta, A.J.; Kruisselbrink, A.B.; Lurvink, E.; Willemze, R.; Fibbe, W.E. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J. Immunol., 2006, 177(4), 2080-2087. doi: 10.4049/jimmunol.177.4.2080 PMID: 16887966
  66. Fan, L.; Hu, C.; Chen, J.; Cen, P.; Wang, J.; Li, L. Interaction between mesenchymal stem cells and B-Cells. Int. J. Mol. Sci., 2016, 17(5), 650. doi: 10.3390/ijms17050650 PMID: 27164080
  67. Asari, S.; Itakura, S.; Ferreri, K. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp. Hematol., 2009, 37(5), 604-615. doi: 10.1016/j.exphem.2009.01.005 PMID: 19375651
  68. Tabera, S.; Pérez-Simón, J.A.; Díez-Campelo, M. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica, 2008, 93(9), 1301-1309. doi: 10.3324/haematol.12857 PMID: 18641017
  69. Magatti, M.; Masserdotti, A.; Bonassi Signoroni, P. B Lymphocytes as targets of the immunomodulatory properties of human amniotic mesenchymal stromal cells. Front. Immunol., 2020, 11, 1156. doi: 10.3389/fimmu.2020.01156 PMID: 32582218
  70. Park, H.; Lee, S.; Yu, Y. TGF-β secreted by human umbilical cord blood-derived mesenchymal stem cells ameliorates atopic dermatitis by inhibiting secretion of TNF-α and IgE. Stem Cells, 2020, 38(7), 904-916. doi: 10.1002/stem.3183 PMID: 32277785
  71. Dong, L.; Wang, Y.; Zheng, T. Hypoxic hUCMSC-derived extracellular vesicles attenuate allergic airway inflammation and airway remodeling in chronic asthma mice. Stem Cell Res. Ther., 2021, 12(1), 4. doi: 10.1186/s13287-020-02072-0 PMID: 33407872
  72. Liang, Y.H.; Zhang, Q.Y.; Guo, Z.K. Heterogeneity of immunomodulatory function of exosomes derived from human umbilical cord mesenchymal stem cells. Military Med Sci, 2017, (6) doi: 10.7644/j.issn.1674-9960.2017.06.006
  73. Shokravi, S.; Borisov, V.; Zaman, B.A. Mesenchymal stromal cells (MSCs) and their exosome in acute liver failure (ALF): A comprehensive review. Stem Cell Res. Ther., 2022, 13(1), 192. doi: 10.1186/s13287-022-02825-z PMID: 35527304
  74. Cao, H.; Yang, J.; Yu, J. Therapeutic potential of transplanted placental mesenchymal stem cells in treating Chinese miniature pigs with acute liver failure. BMC Med., 2012, 10(1), 56. doi: 10.1186/1741-7015-10-56 PMID: 22673529
  75. Putra, A.; Rosdiana, I.; Darlan, D.M. Intravenous administration is the best route of mesenchymal stem cells migration in improving liver function enzyme of acute liver failure. Folia Med., 2020, 62(1), 52-58. doi: 10.3897/folmed.62.e47712 PMID: 32337897
  76. Lin, N.C.; Wu, H.H.; Ho, J.H.C.; Liu, C.S.; Lee, O.K.S. Mesenchymal stem cells prolong survival and prevent lethal complications in a porcine model of fulminant liver failure. Xenotransplantation, 2019, 26(6), e12542. doi: 10.1111/xen.12542 PMID: 31219208
  77. Guo, G.; Zhuang, X.; Xu, Q. Peripheral infusion of human umbilical cord mesenchymal stem cells rescues acute liver failure lethality in monkeys. Stem Cell Res. Ther., 2019, 10(1), 84. doi: 10.1186/s13287-019-1184-2 PMID: 30867056
  78. Yuan, S.; Jiang, T.; Sun, L.; Zheng, R.; Ahat, N.; Zhang, Y. The role of bone marrow mesenchymal stem cells in the treatment of acute liver failure. BioMed Res. Int., 2013, 2013, 1-9. doi: 10.1155/2013/251846 PMID: 24312909
  79. Deng, L.; Kong, X.; Liu, G. Transplantation of adipose-derived mesenchymal stem cells efficiently rescues thioacetamide-induced acute liver failure in mice. Transplant. Proc., 2016, 48(6), 2208-2215. doi: 10.1016/j.transproceed.2016.02.077 PMID: 27569972
  80. Li, T.; Yan, Y.; Wang, B. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev., 2013, 22(6), 845-854. doi: 10.1089/scd.2012.0395 PMID: 23002959
  81. Lee, M.J.; Jung, J.; Na, K.H. Anti-fibrotic effect of chorionic plate-derived mesenchymal stem cells isolated from human placenta in a rat model of CCl4-injured liver: Potential application to the treatment of hepatic diseases. J. Cell. Biochem., 2010, 111(6), 1453-1463. doi: 10.1002/jcb.22873 PMID: 20830742
  82. Yu, H; Feng, Y; Du, W Off-the-shelf GMP-grade UC-MSCs as therapeutic drugs for the amelioration of CCl4-induced acute-onchronic liver failure in NOD-SCID mice. Int Immunopharmacol, 2022, 113(Pt A), 109408. doi: 10.1016/j.intimp.2022.109408
  83. Liu, M.; He, J.; Zheng, S. Human umbilical cord mesenchymal stem cells ameliorate acute liver failure by inhibiting apoptosis, inflammation and pyroptosis. Ann. Transl. Med., 2021, 9(21), 1615. doi: 10.21037/atm-21-2885 PMID: 34926659
  84. Deng, Y.; Zhang, Y.; Ye, L. Umbilical cord-derived mesenchymal stem cells instruct monocytes towards an il10-producing phenotype by secreting IL6 and HGF. Sci. Rep., 2016, 6(1), 37566. doi: 10.1038/srep37566 PMID: 27917866
  85. Jiang, W.; Tan, Y.; Cai, M. Human umbilical cord msc-derived exosomes suppress the development of CCl 4 -induced liver injury through antioxidant effect. Stem Cells Int., 2018, 2018, 1-11. doi: 10.1155/2018/6079642 PMID: 29686713
  86. Fong, C.Y.; Richards, M.; Manasi, N.; Biswas, A.; Bongso, A. Comparative growth behaviour and characterization of stem cells from human Wharton’s jelly. Reprod. Biomed. Online, 2007, 15(6), 708-718. doi: 10.1016/S1472-6483(10)60539-1 PMID: 18062871
  87. Weiss, M.L.; Medicetty, S.; Bledsoe, A.R. Human umbilical cord matrix stem cells: Preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells, 2006, 24(3), 781-792. doi: 10.1634/stemcells.2005-0330 PMID: 16223852
  88. Gao, L.; Zhang, Y.; Hu, B. Phase II multicenter, randomized, double-blind controlled study of efficacy and safety of umbilical cord–derived mesenchymal stromal cells in the prophylaxis of chronic graft-versus-host disease after HLA-haploidentical stem-cell transplantation. J. Clin. Oncol., 2016, 34(24), 2843-2850. doi: 10.1200/JCO.2015.65.3642 PMID: 27400949
  89. Chen, G.; Yue, A.; Ruan, Z. Human umbilical cord-derived mesenchymal stem cells do not undergo malignant transformation during long-term culturing in serum-free medium. PLoS One, 2014, 9(6), e98565. doi: 10.1371/journal.pone.0098565 PMID: 24887492
  90. Hendijani, F.; Javanmard, ShH.; Rafiee, L.; Sadeghi-Aliabadi, H. Effect of human Wharton’s jelly mesenchymal stem cell secretome on proliferation, apoptosis and drug resistance of lung cancer cells. Res. Pharm. Sci., 2015, 10(2), 134-142. PMID: 26487890
  91. Peng, L.; Xie, D.; Lin, B.L. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: Short-term and long-term outcomes. Hepatology, 2011, 54(3), 820-828. doi: 10.1002/hep.24434 PMID: 21608000
  92. Kharaziha, P.; Hellström, P.M.; Noorinayer, B. Improvement of liver function in liver cirrhosis patients after autologous mesenchymal stem cell injection: A phase I–II clinical trial. Eur. J. Gastroenterol. Hepatol., 2009, 21(10), 1199-1205. doi: 10.1097/MEG.0b013e32832a1f6c PMID: 19455046
  93. Zhou, C.; Wang, W.; Mu, Y. Allogeneic mesenchymal stem cells therapy for the treatment of hepatitis B virus–related acute-on-chronic liver failure. Hepatology, 2018, 68(4), 1660-1661. doi: 10.1002/hep.30181 PMID: 30014511
  94. Salama, H.; Zekri, A.R.N.; Medhat, E. Peripheral vein infusion of autologous mesenchymal stem cells in Egyptian HCV-positive patients with end-stage liver disease. Stem Cell Res. Ther., 2014, 5(3), 70. doi: 10.1186/scrt459 PMID: 24886681
  95. Li, Y.H.; Xu, Y.; Wu, H.M.; Yang, J.; Yang, L.H.; Yue-Meng, W. Umbilical cord-derived mesenchymal stem cell transplantation in hepatitis B virus related acute-on-chronic liver failure treated with plasma exchange and entecavir: A 24-month prospective study. Stem Cell Rev., 2016, 12(6), 645-653. doi: 10.1007/s12015-016-9683-3 PMID: 27687792
  96. Jang, Y.O.; Kim, Y.J.; Baik, S.K. Histological improvement following administration of autologous bone marrow-derived mesenchymal stem cells for alcoholic cirrhosis: A pilot study. Liver Int., 2014, 34(1), 33-41. doi: 10.1111/liv.12218 PMID: 23782511
  97. Wang, L.; Li, J.; Liu, H. A pilot study of umbilical cord-derived mesenchymal stem cell transfusion in patients with primary biliary cirrhosis. J. Gastroenterol. Hepatol., 2013, 28(Suppl. 1), 85-92. doi: 10.1111/jgh.12029 PMID: 23855301
  98. Yu, Y.B.; Song, Y.; Chen, Y.; Zhang, F.; Qi, F.Z. Differentiation of umbilical cord mesenchymal stem cells into hepatocytes in comparison with bone marrow mesenchymal stem cells. Mol. Med. Rep., 2018, 18(2), 2009-2016. doi: 10.3892/mmr.2018.9181 PMID: 29916543
  99. Wang, Y.; Yi, H.; Song, Y. The safety of MSC therapy over the past 15 years: A meta-analysis. Stem Cell Res. Ther., 2021, 12(1), 545. doi: 10.1186/s13287-021-02609-x PMID: 34663461
  100. Salama, H.; Zekri, A.R.; Bahnassy, A.A. Autologous CD34 + and CD133 + stem cells transplantation in patients with end stage liver disease. World J. Gastroenterol., 2010, 16(42), 5297-5305. doi: 10.3748/wjg.v16.i42.5297 PMID: 21072892
  101. Amer, M.E.M.; El-Sayed, S.Z.; El-Kheir, W.A. Clinical and laboratory evaluation of patients with end-stage liver cell failure injected with bone marrow-derived hepatocyte-like cells. Eur. J. Gastroenterol. Hepatol., 2011, 23(10), 936-941. doi: 10.1097/MEG.0b013e3283488b00 PMID: 21900788
  102. El-Ansary, M.; Abdel-Aziz, I.; Mogawer, S. Phase II trial: Undifferentiated versus differentiated autologous mesenchymal stem cells transplantation in Egyptian patients with HCV induced liver cirrhosis. Stem Cell Rev., 2012, 8(3), 972-981. doi: 10.1007/s12015-011-9322-y PMID: 21989829
  103. Mohamadnejad, M.; Alimoghaddam, K.; Bagheri, M. Randomized placebo-controlled trial of mesenchymal stem cell transplantation in decompensated cirrhosis. Liver Int., 2013, 33(10), 1490-1496. doi: 10.1111/liv.12228 PMID: 23763455
  104. Xu, L.; Gong, Y.; Wang, B. Randomized trial of autologous bone marrow mesenchymal stem cells transplantation for hepatitis B virus cirrhosis: Regulation of Treg/Th17 cells. J. Gastroenterol. Hepatol., 2014, 29(8), 1620-1628. doi: 10.1111/jgh.12653 PMID: 24942592
  105. Suk, K.T.; Yoon, J.H.; Kim, M.Y. Transplantation with autologous bone marrow-derived mesenchymal stem cells for alcoholic cirrhosis: Phase 2 trial. Hepatology, 2016, 64(6), 2185-2197. doi: 10.1002/hep.28693 PMID: 27339398
  106. Yu-zhuo, W.; Le, Y.; Yu-feng, Z. Therapeutic effect of autologous bone marrow mesenchymal stem cells on hepatic fibrosis, liver function, MELD score and 1-year survival rate in patients with decompensated hepatitis B. Chinese J Tissue Eng Res, 2017, 21(13), 2049-2055. doi: 10.3969/j.issn.2095-4344.2017.13.014
  107. Gong, J.Z.; Du, C.X.; Chen, Y.N. Human umbilical cord blood mscs transplantation in treatment of decompensated liver cirrhosis. Chinese General Prac, 2014, (20), 2392-2395. doi: 10.3969/j.issn.1007-9572.2014.20.028
  108. Gui-jin, L.; Ping-guang, L. Effect of human umbilical cord mesenchymal stem cell adjuvant therapy on liver function and fibrosis indicators as well as the degree of inflammation in patients with hepatitis B cirrhosis. Hainan Yixueyuan Xuebao, 2016, 22(11), 1069-1072. doi: 10.13210/j.cnki.jhmu.20160301.006
  109. Cao, Y.M.; Zou, Z.Q.; Liu, Y.C. Early efficacy of umbilical cord mesenchymal stem cells in decompensated hepatitis B cirrhosis. Shandong Yiyao, 2012, 52(33), 62-64. doi: 10.3969/j.issn.1002-266X.2012.33.023
  110. Ji, Y.H.; Xu, C.; Shu, D. Therapeutic effect of human umbilical cord mesenchymal stem cells combined with Biejiruangan Tablets on decompensated hepatitis B cirrhosis. J Clin Res, 2017, 34(1), 178-180. doi: 10.3969/j.issn.1671-7171.2017.01.066
  111. Yan-hang, L.; Shan-shan, W.U.; Zhen-chang, W. Clinical observation of rougan huaxian granules combined with bone marrow mesenchymal stem cell transplantation in the treatment of hepatitis B cirrhosis. Guiding JTrad Chinese Med Pharmacol, 2019, 25(20), 115-118.
  112. Zhang, J.F.; Song, H.Y.; Chen, X. Clinical observation of intrahepatic human umbilical cord mesenchymal stem cell transplantation in the treatment of patients with hepatitis B-induced decompensated liver cirrhosis. Shiyong Ganzangbing Zazhi, 2018, 21(5), 693-696. doi: 10.3969/j.issn.1672-5069.2018.05.010
  113. Xiao-ke, J.; Xiu-ling, L.I.; Yang-qiu, B. Long-term efficacy of human umbilical cord derived-mesenchymal stem cell transplantation for treating patients with HBV-related decompensated cirrhosis. J Med Forum, 2018, 39(2), 30-34.
  114. Lin, H.; Zhang, Z.; Shi, M. Prospective controlled trial of safety of human umbilical cord derived-mesenchymal stem cell transplantation in patients with decompensated liver cirrhosis. Zhonghua Gan Zang Bing Za Zhi, 2012, 20(7), 487-91. doi: 10.3760/cma.j.issn.1007-3418.2012.07.002 PMID: 23044231
  115. Yu, S.J.; Chen, L.M.; Lyu, S. Safety and efficacy of human umbilical cord derived-mesenchymal stem cell transplantation for treating patients with HBV-related decompensated cirrhosis. Zhonghua Gan Zang Bing Za Zhi, 2016, 24(1), 51-55. doi: 10.3760/cma.j.issn.1007-3418.2016.01.010 PMID: 26983390
  116. Fang, X.Q.; Zhang, J.F.; Song, H.Y. Effect of umbilical cord mesenchymal stem cell transplantation on immune function and prognosis of patients with decompensated hepatitis B cirrhosis. Zhonghua Gan Zang Bing Za Zhi, 2016, 24(12), 907-10. doi: 10.3760/cma.j.issn.1007-3418.2016.12.006 PMID: 28073411
  117. Sheng, Z.H.E.N.G.; Juan, Y.; Qiong, L.I.U. Clinical study of autologous bone marrow mesenchymal stem cells transplantation through proper hepatic artery for decompensated cirrhosis patients. Chinese Hepatol, 2016, 21(2), 95-99. doi: 10.3969/j.issn.1008-1704.2016.02.004
  118. Fu, Q.C.; Jiang, S.; Wang, X.J. Safety and escalation study of human mesenchymal stem cells for patients with decompensated liver cirrhosis. Chinese Hepatol, 2014, 19(1), 3-7.
  119. Hu, L.; Zheng, Z.; Ming, S. The effect of human umbilical cord derived-mesenchymal stem cells transplantation on patients with decompensated liver cirrhosis: A prospective and control trial. Chinese Hepatol, 2012, 17(2), 79-82. doi: 10.3969/j.issn.1008-1704.2012.02.002
  120. Sui, Z.; Bei, J.; Cui-min, G. Therapeutic effect of human umbilical cord mesenchymal stem cells transplantation via peripheral vein in the treatment of hepatitis B liver cirrhosis. J Hebei Med Uni, 2017, 38(3), 270-273. doi: 10.3969/j.issn.1007-3205.2017.03.006
  121. Yu, Z.; Yu, Z.; Daizhong, Z. Efficacy of intrahepatic transplantation of human umbilical cord mesenchymal stem cells combined with matrine in the treatment of patients with decompensated hepatitis B cirrhosis. Shiyong Ganzangbing Zazhi, 2018, 21(3), 360-363. doi: 10.3969/j.issn.1672-5069.2018.03.011
  122. Jian, S.L.; Zhao, X.R. Efficacy of autologous bone marrow mesenchymal stem cells transplantation in treatment of patients with decompensated alcoholic liver cirrhosis. Shiyong Ganzangbing Zazhi, 2017, 20(6), 773-774. doi: 10.3969/j.issn.1672-5069.2017.06.038
  123. Shen, J.K.; Zheng, L.Q.; Pan, X.N. Efficacy of intrahepatic transplantation of autologous bone marrow mesenchymal stem cells in the treatment of patients with decompensated alcohol-induced liver cirrhosis. Shiyong Ganzangbing Zazhi, 2015, (6), 628-632. doi: 10.3969/j.issn.1672-5069.2015.06.016
  124. Li, Z.J.; Yang, G.L.; Li, X.L. Clinical observation of mesenchymal stem cells derived from umbilical cord blood for therapy of 45 patients with decompensated liver cirrhosis. Curr Immunol, 2013, 33(6), 484-487.
  125. Ke, C.Z.; Liu, L.; Li, D. Clinical observation of intravenous transplantation of human umbilical cord blood mesenchymal stem cells for decompensated liver cirrhosis. Zhejiang Clin Med J, 2014, (8), 1185-1187.
  126. Minghui, Z.; Xuhua, L.; Jiao, H. Curative effect of human umbilical cord mesenchymal stem cells on patients with decompensated cirrhosis. J Zhengzhou Uni(Med Sci), 2013, 48(1), 117-120. doi: 10.3969/j.issn.1671-6825.2013.01.033
  127. Zhi-yu, Z.; Dong-liang, L.; Jian, F. Umbilical cord mesenchymal stem cells with bone marrow stem cells in the treatment of decompensated cirrhosis:A 1-year follow-up study. J. Clin. Rehabil. Tissue Eng. Res., 2015, (10), 1533-1538. doi: 10.3969/j.issn.2095-4344.2015.10.011
  128. Xue-qing, F.; Jun-fei, Z.; Hai-yan, S. Effects of human umbilical cord mesenchymal stem cell therapy on the immune function and prognosis in patients with decompensated liver cirrhosis due to hepatitis B. Chinese J Tissue Eng Res, 2017, 21(17), 2696-2701. doi: 10.3969/j.issn.2095-4344.2017.17.012
  129. Yue-fan, Z.; Nan, L.; Jun-shan, Z. Short-term effects of human umbilical cord-derived mesenchymal stem cells in treatment of patients with decompensated cirrhosis. J. Clin. Rehabil. Tissue Eng. Res., 2012, 16(14), 2585-2588. doi: 10.3969/j.issn.1673-8225.2012.14.024
  130. Shi, O.; Shu-ren, L.; Tao, C. Hepatic arterial transplantation of autologous bone marrow mesenchymal stem cells in treatment of decompensated liver cirrhosis. J. Clin. Rehabil. Tissue Eng. Res., 2013, (36), 6455-6461. doi: 10.3969/j.issn.2095-4344.2013.36.012

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers