Immunological basis of stem cell therapy in liver diseases

Expert Review of Clinical Immunology

Volumn 10, Issue 9, 2014, Pages 1185-1196

  Cui, Lina ^a   Shi, Yongquan ^a   Han, Ying ^a   Fan, Daiming ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

hepatic microenvironment; immunology; liver disease; stem cell therapy; stem cells

Indexed keywords

ALLOGENEIC STEM CELL TRANSPLANTATION; AUTOIMMUNE LIVER DISEASE; CELL DIFFERENTIATION; CELL INFILTRATION; DOWN REGULATION; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; LIVER DISEASE; LIVER FIBROSIS; LIVER INJURY; LIVER REGENERATION; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NONHUMAN; PHENOTYPE; REVIEW; STEM CELL TRANSPLANTATION; ANIMAL; IMMUNOLOGY; LIVER CELL; LIVER DISEASES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; HEPATOCYTES; HUMANS; IMMUNOMODULATION; LIVER DISEASES; LIVER REGENERATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS;

EID: 84906060263     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2014.930665     Document Type: Review

References (102)

1. Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006; 43(2 Suppl 1):S54-62
2. Tacke F, Zimmermann HW. Macrophage heterogeneity in liver injury and fibrosis. J Hepatol 2014;60(5):1090-6
3. Fallowfield JA, Mizuno M, Kendall TJ, et al. Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis. J Immunol 2007;178(8): 5288-95
4. Pellicoro A, Aucott RL, Ramachandran P, et al. Elastin accumulation is regulated at the level of degradation by macrophage metalloelastase (MMP-12) during experimental liver fibrosis. Hepatology 2012;55(6):1965-75
5. Heymann F, Hammerich L, Storch D, et al. Hepatic macrophage migration and differentiation critical for liver fibrosis is mediated by the chemokine receptor C-C motif chemokine receptor 8 in mice. Hepatology 2012;55(3):898-909
6. Collins BH, Holzknecht ZE, Lynn KA, et al. Association of age-dependent liver injury and fibrosis with immune cell populations. Liver Int 2013;33(8): 1175-86
7. Imamura M, Ogawa T, Sasaguri Y, et al. Suppression of macrophage infiltration inhibits activation of hepatic stellate cells and liver fibrogenesis in rats. Gastroenterology 2005;128(1):138-46
8. Thomas JA, Pope C, Wojtacha D, et al. Macrophage therapy for murine liver fibrosis recruits host effector cells improving fibrosis, regeneration, and function. Hepatology 2011;53(6):2003-15
9. Baeck C, Wehr A, Karlmark KR, et al. Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 2012;61(3): 416-26
10. Cripps JG, Wang J, Maria A, et al. Type 1 T helper cells induce the accumulation of myeloid-derived suppressor cells in the inflamed Tgfb1 knockout mouse liver. Hepatology 2010;52(4):1350-9
11. Muller T, Beutler C, Pico AH, et al. Increased T-helper 2 cytokines in bile from patients with IgG4-related cholangitis disrupt the tight junction-associated biliary epithelial cell barrier. Gastroenterology 2013;144(5):1116-28
12. Yang ZL, Cheng K, Sun HG, et al. Changes in peripheral blood Th1 and Th2 cells in rat liver transplantation under different immune statuses. Genet Mol Res 2013;12(4):6939-46
13. Brenndorfer ED, Brass A, Karthe J, et al. Cleavage of the T cell protein tyrosine phosphatase by the hepatitis C virus nonstructural 3/4A protease induces a Th1 to Th2 shift reversible by ribavirin therapy. J Immunol 2014;192(4):1671-80
14. Zhu X, Uetrecht J. A novel T(H)17-type cell is rapidly increased in the liver in response to acetaminophen-induced liver injury: T(H)17 cells and the innate immune response. J Immunotoxicol 2013;10(3): 287-91
15. Hammerich L, Heymann F, Tacke F. Role of IL-17 and Th17 cells in liver diseases. Clin Dev Immunol 2011;2011:345803
16. Park O, Wang H, Weng H, et al. In vivo consequences of liver-specific interleukin- 22 expression in mice: implications for human liver disease progression. Hepatology 2011;54(1):252-61
17. Hou L, Jie Z, Desai M, et al. Early IL-17 production by intrahepatic T cells is important for adaptive immune responses in viral hepatitis. J Immunol 2013;190(2): 621-9
18. Wang XF, Lei Y, Chen M, et al. PD-1/ PDL1 and CD28/CD80 pathways modulate natural killer T cell function to inhibit hepatitis B virus replication. J Viral Hepat 2013;20(Suppl 1):27-39
19. Kumar V. NKT-cell subsets: promoters and protectors in inflammatory liver disease. J Hepatol 2013;59(3):618-20
20. Lu L, Feng M, Gu J, et al. Restoration of intrahepatic regulatory T cells through MMP-9/13-dependent activation of TGF-beta is critical for immune homeostasis following acute liver injury. J Mol Cell Biol 2013;5(6):369-79
21. Li X, Liu Z, Yan X, et al. Induction of regulatory T cells by high-dose gp96 suppresses murine liver immune hyperactivation. PLoS One 2013;8(7): e68997
22. Dienes HP, Drebber U. Pathology of immune-mediated liver injury. Dig Dis 2010;28(1):57-62
23. Tucker RM, Feldman AG, Fenner EK, Mack CL. Regulatory T cells inhibit Th1 cell-mediated bile duct injury in murine biliary atresia. J Hepatol 2013; 59(4):790-6
24. Wang X, Jiang Z, Cao W, et al. Th17/Treg imbalance in triptolide-induced liver injury. Fitoterapia 2014;93:245-51
25. Soto-Gutierrez A, Zhang L, Medberry C, et al. A whole-organ regenerative medicine approach for liver replacement. Tissue Eng Part C Methods 2011;17(6): 677-86
26. Lee KD, Kuo TK, Whang-Peng J, et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 2004; 40(6):1275-84
27. Schwartz RE, Fleming HE, Khetani SR, Bhatia SN. Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv 2014; 32(2):504-13
28. Gebler A, Zabel O, Seliger B. The immunomodulatory capacity of mesenchymal stem cells. Trends Mol Med 2012;18(2):128-34
29. Deuse T, Stubbendorff M, Tang-Quan K, et al. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant 2011;20(5):655-67
30. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25(11):2739-49
31. Kitazawa Y, Li XK, Xie L, et al. Bone marrow-derived conventional, but not cloned, mesenchymal stem cells suppress lymphocyte proliferation and prevent graft-versus-host disease in rats. Cell Transplant 2012;21(2-3):581-90
32. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99(10):3838-43
33. Luo C, Jia W, Wang K, et al. Human amniotic fluid stem cells suppress PBMC proliferation through IDO and IL-10-dependent pathways. Curr Stem Cell Res Ther 2014;9(1):36-45
34. Tobin LM, Healy ME, English K, Mahon BP. Human mesenchymal stem cells suppress donor CD4(+) T cell proliferation and reduce pathology in a humanized mouse model of acute graft-versus-host disease. Clin Exp Immunol 2013;172(2): 333-48
35. Krampera M, Glennie S, Dyson J, et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003;101(9):3722-9
36. Svobodova E, Krulova M, Zajicova A, et al. The role of mouse mesenchymal stem cells in differentiation of naive T-cells into anti-inflammatory regulatory T-cell or proinflammatory helper T-cell 17 population. Stem Cells Dev 2012;21(6): 901-10
37. Makino Y, Yamaza H, Akiyama K, et al. Immune therapeutic potential of stem cells from human supernumerary teeth. J Dent Res 2013;92(7):609-15
38. Zhang W, Ge W, Li C, et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 2004;13(3):263-71
39. Nauta AJ, Kruisselbrink AB, Lurvink E, et al. Mesenchymal stem cells inhibit generation and function of both CD34+- derived and monocyte-derived dendritic cells. J Immunol 2006;177(4):2080-7
40. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105(4): 1815-22
41. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363(9419):1439-41
42. Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008;371(9624):1579-86
43. Duijvestein M, Vos AC, Roelofs H, et al. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 2010;59(12):1662-9
44. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010;67(10):1187-94
45. Yu J, Zheng C, Ren X, et al. Intravenous administration of bone marrow mesenchymal stem cells benefits experimental autoimmune myasthenia gravis mice through an immunomodulatory action. Scand J Immunol 2010;72(3):242-9
46. Swart JF, de Roock S, Hofhuis FM, et al. Mesenchymal stem cell therapy in proteoglycan induced arthritis. Ann Rheum Dis 2014. [Epub ahead of print]
47. Anderson P, Souza-Moreira L, Morell M, et al. Adipose-derived mesenchymal stromal cells induce immunomodulatory macrophages which protect from experimental colitis and sepsis. Gut 2013; 62(8):1131-41
48. Kuo YR, Chen CC, Goto S, et al. Immunomodulatory effects of bone marrow-derived mesenchymal stem cells in a swine hemi-facial allotransplantation model. PLoS One 2012;7(4):e35459
49. Petersen BE, Bowen WC, Patrene KD, et al. Bone marrow as a potential source of hepatic oval cells. Science 1999;284(5417): 1168-70
50. Yan L, Han Y, Wang J, et al. Peripheral blood monocytes from patients with HBV related decompensated liver cirrhosis can differentiate into functional hepatocytes. Am J Hematol 2007;82(11):949-54
51. Yan L, Han Y, Wang J, et al. Peripheral blood monocytes from the decompensated liver cirrhosis could migrate into nude mouse liver with human hepatocyte-markers expression. Biochem Biophys Res Commun 2008;371(4):635-8
52. Wang J, Zhou X, Cui L, et al. The significance of CD14+ monocytes in peripheral blood stem cells for the treatment of rat liver cirrhosis. Cytotherapy 2010; 12(8):1022-34
53. Sakaida I, Terai S, Yamamoto N, et al. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Hepatology 2004;40(6):1304-11
54. Khurana S, Mukhopadhyay A. Characterization of the potential subpopulation of bone marrow cells involved in the repair of injured liver tissue. Stem Cells 2007;25:1439-47
55. am Esch JS 2nd, Knoefel WT, Klein M, et al. Portal application of autologous CD133+ bone marrow cells to the liver: a novel concept to support hepatic regeneration. Stem Cells 2005;23(4):463-70
56. ClinicalTrials.gov. 2014. Available from: www.clinicaltrials.gov
57. Sancho-Bru P, Najimi M, Caruso M, et al. Stem and progenitor cells for liver repopulation: can we standardise the process from bench to bedside? Gut 2009;58(4): 594-603
58. Von Luttichau I, Notohamiprodjo M, Wechselberger A, et al. Human adult CD34- progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev 2005;14(3): 329-36
59. Lin H, Xu, R, Zhang Z, et al. Implications of the immunoregulatory functions of mesenchymal stem cells in the treatment of human liver diseases. Cell Mol Immunol 2011;8(1):19-22
60. Li Q, Zhou X, Shi Y, et al. In vivo tracking and comparison of the therapeutic effects of MSCs and HSCs for liver injury. PLoS One 2013;8(4):e62363
61. Lee MJ, Jung J, Na KH, et al. Anti-fibrotic effect of chorionic plate-derived mesenchymal stem cells isolated from human placenta in a rat model of CCl(4)- injured liver: potential application to the treatment of hepatic diseases. J Cell Biochem 2010;111(6):1453-63
62. Tanimoto H, Terai S, Taro T, et al. Improvement of liver fibrosis by infusion of cultured cells derived from human bone marrow. Cell Tissue Res 2013;354(3): 717-28
63. Parekkadan B, van Poll D, Megeed Z, et al. Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun 2007; 363(2):247-52
64. Lin N, Hu K, Chen S, et al. Nerve growth factor-mediated paracrine regulation of hepatic stellate cells by multipotent mesenchymal stromal cells. Life Sci 2009; 85(7-8):291-5
65. Du Z, Wei C, Cheng K, et al. Mesenchymal stem cell-conditioned medium reduces liver injury and enhances regeneration in reduced-size rat liver transplantation. J Surg Res 2013;183(2): 907-15
66. Higashimoto M, Sakai Y, Takamura M, et al. Adipose tissue derived stromal stem cell therapy in murine ConA-derived hepatitis is dependent on myeloid-lineage and CD4+ T-cell suppression. Eur J Immunol 2013;43(11):2956-68
67. Busch SA, Hamilton JA, Horn KP, et al. Multipotent adult progenitor cells prevent macrophage-mediated axonal dieback and promote regrowth after spinal cord injury. J Neurosci 2011;31(3):944-53
68. Dayan V, Yannarelli G, Billia F, et al. Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/ macrophages after acute myocardial infarction. Basic Res Cardiol 2011;106(6): 1299-310
69. Ylostalo JH, Bartosh TJ, Coble K, Prockop DJ. Human mesenchymal stem/ stromal cells cultured as spheroids are self-activated to produce prostaglandin E2 that directs stimulated macrophages into an anti-inflammatory phenotype. Stem Cells 2012;30(10):2283-96
70. Mathias LJ, Khong SM, Spyroglou L, et al. Alveolar macrophages are critical for the inhibition of allergic asthma by mesenchymal stromal cells. J Immunol 2013;191(12):5914-24
71. Furuhashi K, Tsuboi N, Shimizu A, et al. Serum-starved adipose-derived stromal cells ameliorate crescentic GN by promoting immunoregulatory macrophages. J Am Soc Nephrol 2013;24(4):587-603
72. Zheng L, Chu J, Shi Y, et al. Bone marrow-derived stem cells ameliorate hepatic fibrosis by down-regulating interleukin-17. Cell Biosci 2013;3(1):46
73. Ezquer M, Ezquer F, Ricca M, et al. Intravenous administration of multipotent stromal cells prevents the onset of non-alcoholic steatohepatitis in obese mice with metabolic syndrome. J Hepatol 2011; 55(5):1112-20
74. Bernuzzi F, Fenoglio D, Battaglia F, et al. Phenotypical and functional alterations of CD8 regulatory T cells in primary biliary cirrhosis. J Autoimmun 2010;35(3): 176-80
75. Hirschfield GM, Gershwin ME. The immunobiology and pathophysiology of primary biliary cirrhosis. Annu Rev Pathol 2013;8:303-30
76. Aso-Ishimoto Y, Yamagiwa S, Ichida T, et al. Increased activated natural killer T cells in the liver of patients with advancedstage primary biliary cirrhosis. Biomed Res 2014;35(2):161-9
77. Tsikrikoni A, Kyriakou DS, Rigopoulou EI, et al. Markers of cell activation and apoptosis in bone marrow mononuclear cells of patients with autoimmune hepatitis type 1 and primary biliary cirrhosis. J Hepatol 2005;42(3):393-9
78. Wang L, Li J, Liu H, et al. 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
79. Wang D, Zhang H, Liang J, et al. Effect of allogeneic bone marrow-derived mesenchymal stem cells transplantation in a polyI:C-induced primary biliary cirrhosis mouse model. Clin Exp Med 2011;11(1): 25-32
80. Li J, Lu S, Yang S, et al. Impaired immunomodulatory ability of bone marrow mesenchymal stem cells on CD4(+) T cells in aplastic anemia. Results Immunol 2012;2:142-7
81. Terai S, Ishikawa T, Omori K, et al. Improved liver function in patients with liver cirrhosis after autologous bone marrow cell infusion therapy. Stem Cells 2006; 24(10):2292-8
82. Gordon MY, Levicar N, Pai M, et al. Characterization and clinical application of human CD34+ stem/progenitor cell populations mobilized into the blood by granulocyte colony-stimulating factor. Stem Cells 2006;24(7):1822-30
83. Yannaki E, Anagnostopoulos A, Kapetanos D, et al. Lasting amelioration in the clinical course of decompensated alcoholic cirrhosis with boost infusions of mobilized peripheral blood stem cells. Exp Hematol 2006;34(11):1583-7
84. Mohamadnejad M, Namiri M, Bagheri M, et al. Phase 1 human trial of autologous bone marrow-hematopoietic stem cell transplantation in patients with decompensated cirrhosis. World J Gastroenterol 2007;13(24):3359-63
85. Mohamadnejad M, Alimoghaddam K, Mohyeddin-Bonab M, et al. Phase 1 trial of autologous bone marrow mesenchymal stem cell transplantation in patients with decompensated liver cirrhosis. Arch Iran Med 2007;10(4):459-66
86. Lyra AC, Soares MB, da Silva LF, et al. Feasibility and safety of autologous bone marrow mononuclear cell transplantation in patients with advanced chronic liver disease. World J Gastroenterol 2007;13(7):1067-73
87. Furst G, Schulte am Esch J, Poll LW, et al. Portal vein embolization and autologous CD133+ bone marrow stem cells for liver regeneration: initial experience. Radiology 2007;243(1):171-9
88. Chernykh ER, Starostina NM, Paltsev AI, et al. Autologous bone marrow cells in the treatment of cirrhosis of the liver. Bull Exp Biol Med 2007;144(4):640-5
89. Han Y, Yan L, Han G, et al. Controlled trials in hepatitis B virus-related decompensate liver cirrhosis: peripheral blood monocyte transplant versus granulocyte-colony-stimulating factor mobilization therapy. Cytotherapy 2008; 10(4):390-6
90. Pai M, Zacharoulis D, Milicevic MN, et al. Autologous infusion of expanded mobilized adult bone marrow-derived CD34+ cells into patients with alcoholic liver cirrhosis. Am J Gastroenterol 2008;103(8):1952-8
91. Kharaziha P, Hellstrom PM, Noorinayer B, et al. 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):1199-205
92. Lyra AC, Soares MB, da Silva LF, et al. Infusion of autologous bone marrow mononuclear cells through hepatic artery results in a short-term improvement of liver function in patients with chronic liver disease: a pilot randomized controlled study. Eur J Gastroenterol Hepatol 2010;22(1): 33-42
93. Salama H, Zekri AR, Zern M, et al. Autologous hematopoietic stem cell transplantation in 48 patients with end-stage chronic liver diseases. Cell Transplant 2010; 19(11):1475-86
94. Salama H, Zekri AR, Bahnassy AA, et al. Autologous CD34+ and CD133+ stem cells transplantation in patients with end stage liver disease. World J Gastroenterol 2010; 16(42):5297-305
95. Ismail A, Fouad O, Abdelnasser A, et al. Stem cell therapy improves the outcome of liver resection in cirrhotics. J Gastrointest Cancer 2010;41(1):17-23
96. Couto BG, Goldenberg RC, da Fonseca LM, et al. Bone marrow mononuclear cell therapy for patients with cirrhosis: a Phase 1 study. Liver Int 2011; 31(3):391-400
97. Nikeghbalian S, Pournasr B, Aghdami N, et al. Autologous transplantation of bone marrow-derived mononuclear and CD133 (+) cells in patients with decompensated cirrhosis. Arch Iran Med 2011;14(1):12-17
98. Peng L, Xie DY, Lin BL, et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and longterm outcomes. Hepatology 2011;54(3): 820-8
99. Amer ME, El-Sayed SZ, El-Kheir WA, et al. 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):936-41
100. El-Ansary M, Abdel-Aziz I, Mogawer S, et al. 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):972-81
101. Zhang Z, Lin H, Shi M, et al. Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients. J Gastroenterol Hepatol 2012;27(Suppl 2): 112-20
102. Spahr L, Chalandon Y, Terraz S, et al. Autologous bone marrow mononuclear cell transplantation in patients with decompensated alcoholic liver disease: a randomized controlled trial. PLoS One 2013;8(1):e53719