Therapeutic and Safety Promise of Mesenchymal Stem Cells for Liver Failure: From Preclinical Experiment to Clinical Application
- Authors: Xie Q.1, Gu J.2
-
Affiliations:
- National Engineering Research Center of Cell Products,, AmCellGene Engineering Co., Ltd,
- National Engineering Research Center of Cell Products, AmCellGene Engineering Co., Ltd,
- Issue: Vol 19, No 10 (2024)
- Pages: 1351-1368
- Section: Medicine
- URL: https://rjpbr.com/1574-888X/article/view/645467
- DOI: https://doi.org/10.2174/011574888X260690230921174343
- ID: 645467
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
- Navarro, V.J.; Senior, J.R. Drug-related hepatotoxicity. N. Engl. J. Med., 2006, 354(7), 731-739. doi: 10.1056/NEJMra052270 PMID: 16481640
- 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
- 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
- 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
- Naghavi, M.; Abajobir, A.A.; Abbafati, C. Global, regional, and national age-sex specific mortality for 264 causes of death, 19802016: 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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, Whartons Jelly and bone marrow sources. Cell. Immunol., 2010, 264(2), 171-179. doi: 10.1016/j.cellimm.2010.06.006 PMID: 20619400
- 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
- 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
- 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
- McGuirk, J.; Smith, J.; Divine, C.; Zuniga, M.; Weiss, M. Whartons 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
- 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
- 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
- Chen, JY Characteristics of menstrual-blood-derived endometrial stem cells and their role in liver injury models., 2014.
- 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
- 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
- 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
- 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
- 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
- Weiss, M.L.; Anderson, C.; Medicetty, S. Immune properties of human umbilical cord Whartons jelly-derived cells. Stem Cells, 2008, 26(11), 2865-2874. doi: 10.1634/stemcells.2007-1028 PMID: 18703664
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Chen, S. Xu, Lin N, Pan W, Hu K, Xu R. Activation of Notch1 signaling by marrow-derived mesenchymal stem cells through cellcell 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Fong, C.Y.; Richards, M.; Manasi, N.; Biswas, A.; Bongso, A. Comparative growth behaviour and characterization of stem cells from human Whartons jelly. Reprod. Biomed. Online, 2007, 15(6), 708-718. doi: 10.1016/S1472-6483(10)60539-1 PMID: 18062871
- 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 Parkinsons disease. Stem Cells, 2006, 24(3), 781-792. doi: 10.1634/stemcells.2005-0330 PMID: 16223852
- Gao, L.; Zhang, Y.; Hu, B. Phase II multicenter, randomized, double-blind controlled study of efficacy and safety of umbilical cordderived 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
- 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
- Hendijani, F.; Javanmard, ShH.; Rafiee, L.; Sadeghi-Aliabadi, H. Effect of human Whartons 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
- 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
- Kharaziha, P.; Hellström, P.M.; Noorinayer, B. Improvement of liver function in liver cirrhosis patients after autologous mesenchymal stem cell injection: A phase III clinical trial. Eur. J. Gastroenterol. Hepatol., 2009, 21(10), 1199-1205. doi: 10.1097/MEG.0b013e32832a1f6c PMID: 19455046
- Zhou, C.; Wang, W.; Mu, Y. Allogeneic mesenchymal stem cells therapy for the treatment of hepatitis B virusrelated acute-on-chronic liver failure. Hepatology, 2018, 68(4), 1660-1661. doi: 10.1002/hep.30181 PMID: 30014511
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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.
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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.
- 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.
- 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
- 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
- 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
- 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
- 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
