Molecular mechanisms of stem cell therapy in alcoholic liver disease

Digestive and Liver Disease

Volumn 46, Issue 5, 2014, Pages 391-397

  Levine, Phillip ^a,b   McDaniel, Kelly ^b   Francis, Heather ^a,b   Kennedy, Lindsey ^b   Alpini, Gianfranco ^a,b   Meng, Fanyin ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

Author keywords

Alcoholic liver diseases; Exosomes; Hepatic stem cells; Mesenchymal stem cells; Microvesicles

Indexed keywords

ALCOHOL LIVER DISEASE; BASIC RESEARCH; CELL VACUOLE; CLINICAL TRIAL (TOPIC); EXOSOME; HEMATOPOIETIC STEM CELL; HUMAN; LIVER CELL; LIVER REGENERATION; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; LIVER DISEASES, ALCOHOLIC; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROVASCULATURE; PHYSIOLOGY;

EXOSOMES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEPATOCYTES; HUMANS; LIVER DISEASES, ALCOHOLIC; LIVER REGENERATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROVESSELS;

EID: 84898863534     PISSN: 15908658     EISSN: 18783562     Source Type: Journal    
DOI: 10.1016/j.dld.2013.11.015     Document Type: Review

References (100)

1. Lieber C.S., Jones D.P., DeCarli L.M. Effects of prolonged ethanol intake: production of fatty liver despite adequate diets. Journal of Clinical Investigation 1965, 44:1009-1021.
2. Lieber C.S. Susceptibility to alcohol-related liver injury. Alcohol and Alcoholism. Supplement 1994, 2:315-326.
3. Thurman R.G., Bradford B.U., Iimuro Y., et al. The role of gut-derived bacterial toxins and free radicals in alcohol-induced liver injury. Journal of Gastroenterology and Hepatology 1998, 13(Suppl.):S39-S50.
4. Tsukamoto H., Lu S.C. Current concepts in the pathogenesis of alcoholic liver injury. FASEB Journal 2001, 15:1335-1349.
5. Hoek J.B., Cahill A., Pastorino J.G. Alcohol and mitochondria: a dysfunctional relationship. Gastroenterology 2002, 122:2049-2063.
6. Shen Z., Ajmo J.M., Rogers C.Q., et al. Role of SIRT1 in regulation of LPS- or two ethanol metabolites-induced TNF-alpha production in cultured macrophage cell lines. American Journal of Physiology: Gastrointestinal and Liver Physiology 2009, 296:G1047-G1053.
7. Hritz I., Mandrekar P., Velayudham A., et al. The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 2008, 48:1224-1231.
8. McMullen M.R., Pritchard M.T., Wang Q., et al. Early growth response-1 transcription factor is essential for ethanol-induced fatty liver injury in mice. Gastroenterology 2005, 128:2066-2076.
9. Gao B., Bataller R. Alcoholic liver disease: pathogenesis and new therapeutic targets. Gastroenterology 2011, 141:1572-1585.
10. Minino A.M., Murphy S.L. Death in the United States, 2010. NCHS Data Brief 2010, 1-8.
11. Zaret K.S., Grompe M. Generation and regeneration of cells of the liver and pancreas. Science Signalling 2008, 322:1490.
12. Duncan A.W., Dorrell C., Grompe M. Stem cells and liver regeneration. Gastroenterology 2009, 137:466-481.
13. Lowes K.N., Brennan B.A., Yeoh G.C., et al. Oval cell numbers in human chronic liver diseases are directly related to disease severity. American Journal of Pathology 1999, 154:537.
14. Grisham J. A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver: autoradiography with thymidine-H3. Cancer Research 1962, 22:842-849.
15. Wands J., Carter E., Bucher N., et al. Inhibition of hepatic regeneration in rats by acute and chronic ethanol intoxication. Gastroenterology 1979, 77:528.
16. Duguay L., Coutu D., Hetu C., et al. Inhibition of liver regeneration by chronic alcohol administration. Gut 1982, 23:8-13.
17. Dey A., Cederbaum A.I. Alcohol and oxidative liver injury. Hepatology 2006, 43:S63-S74.
18. Bailey S.M., Cunningham C.C. Acute and chronic ethanol increases reactive oxygen species generation and decreases viability in fresh, isolated rat hepatocytes. Hepatology 1998, 28:1318-1326.
19. Block G.D., Locker J., Bowen W.C., et al. Population expansion, clonal growth, and specific differentiation patterns in primary cultures of hepatocytes induced by HGF/SF, EGF and TGF alpha in a chemically defined (HGM) medium. Journal of Cell Biology 1996, 132:1133-1149.
20. Naldini L., Vigna E., Narsimhan R., et al. Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-MET. Oncogene 1991, 6:501.
21. 2+ mobilization in rat hepatocytes. Alcoholism, Clinical and Experimental Research 1996, 20:330A-334A.
22. O'Rourke M.F., Tuma D.J., Casey C.A. Decreased binding and autophosphorylation of the epidermal growth factor receptor in ethanol-fed rats. Biochemical Pharmacology 1997, 53:1445-1450.
23. Saso K., Moehren G., Higashi K., et al. Differential inhibition of epidermal growth factor signaling pathways in rat hepatocytes by long-term ethanol treatment. Gastroenterology 1997, 112:2073-2088.
24. Natarajan A., Wagner B., Sibilia M. The EGF receptor is required for efficient liver regeneration. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:17081-17086.
25. Michalopoulos G.K. Liver regeneration. Journal of Cellular Physiology 2007, 213:286-300.
26. Yang S.Q., Lin H.Z., Yin M., et al. Effects of chronic ethanol consumption on cytokine regulation of liver regeneration. American Journal of Physiology: Gastrointestinal and Liver Physiology 1998, 275:G696-G704.
27. Lee Y.J., Aroor A.R., Shukla S.D. Temporal activation of p42/44 mitogen-activated protein kinase and c-Jun N-terminal kinase by acetaldehyde in rat hepatocytes and its loss after chronic ethanol exposure. Journal of Pharmacology and Experimental Therapeutics 2002, 301:908-914.
28. Jung Y., Brown K.D., Witek R.P., et al. Accumulation of hedgehog-responsive progenitors parallels alcoholic liver disease severity in mice and humans. Gastroenterology 2008, 134:1532-1543. e1533.
29. Kuwahara R., Kofman A.V., Landis C.S., et al. The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology 2008, 47:1994-2002.
30. Forbes S., Vig P., Poulsom R., et al. Hepatic stem cells. Journal of Pathology 2002, 197:510-518.
31. Newsome P., Hussain M., Theise N. Hepatic oval cells: helping redefine a paradigm in stem cell biology. Current Topics in Developmental Biology 2004, 61:1-28.
32. Wang Y., Yao H.L., Cui C.B., et al. Paracrine signals from mesenchymal cell populations govern the expansion and differentiation of human hepatic stem cells to adult liver fates. Hepatology 2010, 52:1443-1454.
33. Turner R., Lozoya O., Wang Y., et al. Human hepatic stem cell and maturational liver lineage biology. Hepatology 2011, 53:1035-1045.
34. Libbrecht L., Desmet V., Van Damme B., et al. Deep intralobular extension of human hepatic 'progenitor cells' correlates with parenchymal inflammation in chronic viral hepatitis: can 'progenitor cells' migrate. Journal of Pathology 2000, 192:373-378.
35. Paku S., Schnur J., Nagy P., et al. Origin and structural evolution of the early proliferating oval cells in rat liver. American Journal of Pathology 2001, 158:1313-1323.
36. Sancho-Bru P., Altamirano J., Rodrigo-Torres D., et al. Liver progenitor cell markers correlate with liver damage and predict short-term mortality in patients with alcoholic hepatitis. Hepatology 2012.
37. Apte U., Thompson M.D., Cui S., et al. Wnt/β-catenin signaling mediates oval cell response in rodents. Hepatology 2008, 47:288-295.
38. Fleig S.V., Choi S.S., Yang L., et al. Hepatic accumulation of Hedgehog-reactive progenitors increases with severity of fatty liver damage in mice. Laboratory Investigation 2007, 87:1227-1239.
39. Taipale J., Beachy P.A., The Hedgehog Wnt signalling pathways in cancer. Nature 2001, 411:349-354.
40. Friedman S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008, 134:1655-1669.
41. Parekkadan B., Van Poll D., Suganuma K., et al. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS ONE 2007, 2:e941.
42. Lagasse E., Connors H., Al-Dhalimy M., et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nature Medicine 2000, 6:1229-1234.
43. Petersen B., Bowen W., Patrene K., et al. Bone marrow as a potential source of hepatic oval cells. Science 1999, 284:1168-1170.
44. Körbling M., Katz R.L., Khanna A., et al. Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. New England Journal of Medicine 2002, 346:738-746.
45. Theise N.D., Nimmakayalu M., Gardner R., et al. Liver from bone marrow in humans. Hepatology 2000, 32:11-16.
46. Sato Y., Araki H., Kato J., et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005, 106:756-763.
47. Schwartz R.E., Reyes M., Koodie L., et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. Journal of Clinical Investigation 2002, 109:1291-1302.
48. Dalakas E., Newsome P.N., Harrison D.J., et al. Hematopoietic stem cell trafficking in liver injury. The FASEB Journal 2005, 19:1225-1231.
49. Cantz T., Sharma A.D., Jochheim-Richter A., et al. Reevaluation of bone marrow-derived cells as a source for hepatocyte regeneration. Cell Transplantation 2004, 13:659-666.
50. Menthena A., Deb N., Oertel M., et al. Bone marrow progenitors are not the source of expanding oval cells in injured liver. Stem Cells 2004, 22:1049-1061.
51. Masson S., Harrison D.J., Plevris J.N., et al. Potential of hematopoietic stem cell therapy in hepatology: a critical review. Stem Cells 2004, 22:897-907.
52. Harris R.G., Herzog E.L., Bruscia E.M., et al. Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 2004, 305:90-93.
53. Vassilopoulos G., Wang P.R., Russell D.W. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003, 422:901-904.
54. Sun Z., Zhang X., Locke J.E., et al. Recruitment of host progenitor cells in rat liver transplants. Hepatology 2008, 49:587-597.
55. Gehling U.M., Willems M., Dandri M., et al. Partial hepatectomy induces mobilization of a unique population of haematopoietic progenitor cells in human healthy liver donors. Journal of Hepatology 2005, 43:845-853.
56. Hisada M., Ota Y., Zhang X., et al. Successful transplantation of reduced-sized rat alcoholic fatty livers made possible by mobilization of host stem cells. American Journal of Transplantation 2012.
57. Petit I., Szyper-Kravitz M., Nagler A., et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR 4. Nature Immunology 2002, 3:687-694.
58. Aiuti A., Webb I., Bleul C., et al. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. Journal of Experimental Medicine 1997, 185:111-120.
59. Coulomb-L'Hermin A., Amara A., Schiff C., et al. Stromal cell-derived factor 1 (SDF-1) and antenatal human B cell lymphopoiesis: expression of SDF-1 by mesothelial cells and biliary ductal plate epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:8585-8590.
60. Kollet O., Shivtiel S., Chen Y.Q., et al. HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. Journal of Clinical Investigation 2003, 112:160-169.
61. Terada R., Yamamoto K., Hakoda T., et al. Stromal cell-derived factor-1 from biliary epithelial cells recruits CXCR4-positive cells: implications for inflammatory liver diseases. Laboratory Investigation 2003, 83:665-672.
62. D'Apuzzo M., Rolink A., Loetscher M., et al. The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4. European Journal of Immunology 2005, 27:1788-1793.
63. Möhle R., Bautz F., Denzlinger C., et al. Transendothelial migration of hematopoietic progenitor cells. Annals of the New York Academy of Sciences 2006, 938:26-35.
64. Lévesque J.P., Hendy J., Takamatsu Y., et al. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. Journal of Clinical Investigation 2003, 111:187-196.
65. Hill D.L.B., Marsano L.S., McClain C.J. Increased plasma interleukin-8 concentrations in alcoholic hepatitis. Hepatology 2005, 18:576-580.
66. Huang Y.S., Chan C.Y., Wu J.C., et al. Serum levels of interleukin-8 in alcoholic liver disease: relationship with disease stage, biochemical parameters and survival. Journal of Hepatology 1996, 24:377-384.
67. Sheron N., Bird G., Koskinas J., et al. Circulating and tissue levels of the neutrophil chemotaxin interleukin 8 are elevated in severe acute alcoholic hepatitis, and tissue levels correlate with neutrophil infiltration. Hepatology 1993, 18:41-46.
68. Kwon O.S., Lim D.Y., Kwon K.A., et al. Clinical usefulness of plasma activities of gelatinase (matrix metalloproteinase-2 and 9) in chronic liver disease. Korean Journal of Hepatology 2003, 9:222-230.
69. McQuibban G.A., Butler G.S., Gong J.H., et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. Journal of Biological Chemistry 2001, 276:43503-43508.
70. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nature Medicine 2004, 10:858-864.
71. Quesenberry P.J., Aliotta J.M. The paradoxical dynamism of marrow stem cells: considerations of stem cells, niches, and microvesicles. Stem Cell Reviews 2008, 4:137-147.
72. Ratajczak J., Wysoczynski M., Hayek F., et al. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006, 20:1487-1495.
73. Deregibus M.C., Cantaluppi V., Calogero R., et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110:2440-2448.
74. Herrera M.B., Fonsato V., Gatti S., et al. Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. Journal of Cellular and Molecular Medicine 2010, 14:1605-1618.
75. Fonsato V., Herrera M.B., Buttiglieri S., et al. Use of a rotary bioartificial liver in the differentiation of human liver stem cells. Tissue Engineering Part C: Methods 2010, 16:123-132.
76. Fonsato V., Collino F., Herrera M.B., et al. Human liver stem cell-derived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor microRNAs. Stem Cells 2012, 30:1985-1998.
77. Wetmore B.A., Brees D.J., Singh R., et al. Quantitative analyses and transcriptomic profiling of circulating messenger RNAs as biomarkers of rat liver injury. Hepatology 2010, 51:2127-2139.
78. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. Journal of Cell Biology 2013, 200:373-383.
79. Bala S., Petrasek J., Mundkur S., et al. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 2012, 56:1946-1957.
80. Arroyo J.D., Chevillet J.R., Kroh E.M., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:5003-5008.
81. Meng F., Glaser S.S., Francis H., et al. Epigenetic regulation of miR-34a expression in alcoholic liver injury. American Journal of Pathology 2012, 181:804-817.
82. Gallo A., Tandon M., Alevizos I., et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE 2012, 7:e30679.
83. Masyuk A.I., Masyuk T.V., LaRusso N.F. Exosomes in the pathogenesis, diagnostics and therapeutics of liver diseases. Journal of Hepatology 2013.
84. Ohno S.-i., Takanashi M., Sudo K., et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Molecular Therapy 2012.
85. Lv L.-H., Wan Y.-L., Lin Y., et al. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. Journal of Biological Chemistry 2012, 287:15874-15885.
86. Herrera M., Fonsato V., Gatti S., et al. Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. Journal of Cellular and Molecular Medicine 2010, 14:1605-1618.
87. Houlihan D.D., Newsome P.N. Critical review of clinical trials of bone marrow stem cells in liver disease. Gastroenterology 2008, 135:438-450.
88. Pai M., Spalding D., Xi F., et al. Autologous bone marrow stem cells in the treatment of chronic liver disease. International Journal of Hepatology 2011, 2012.
89. Lyra A.C., Soares M.B.P., da Silva L.F.M., 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. European Journal of Gastroenterology and Hepatology 2010, 22:33.
90. Spahr L., Lambert J.F., Rubbia-Brandt L., et al. Granulocyte-colony stimulating factor induces proliferation of hepatic progenitors in alcoholic steatohepatitis: a randomized trial. Hepatology 2008, 48:221-229.
91. 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:e53719.
92. Di Bonzo L.V., Ferrero I., Cravanzola C., et al. Human mesenchymal stem cells as a two-edged sword in hepatic regenerative medicine: engraftment and hepatocyte differentiation versus profibrogenic potential. Gut 2008, 57:223-231.
93. Cui Q., Wang G.-J., Balian G. Steroid-induced adipogenesis in a pluripotential cell line from bone marrow. Journal of Bone & Joint Surgery 1997, 79:1054-1063.
94. Hong S.H., Nah H.Y., Lee Y.J., et al. Expression of estrogen receptor-alpha and-beta, glucocorticoid receptor, and progesterone receptor genes in human embryonic stem cells and embryoid bodies. Molecules and Cells 2004, 18:320-325.
95. Yannaki E., Athanasiou E., Xagorari A., et al. G-CSF-primed hematopoietic stem cells or G-CSF per se accelerate recovery and improve survival after liver injury, predominantly by promoting endogenous repair programs. Experimental Hematology 2005, 33:108-119.
96. Pai M., Zacharoulis D., Milicevic M.N., et al. Autologous infusion of expanded mobilized adult bone marrow-derived CD34+ cells into patients with alcoholic liver cirrhosis. American Journal of Gastroenterology 2008, 103:1952-1958.
97. Szkolnicka D., Zhou W., Lucendo-Villarin B., et al. Pluripotent stem cell-derived hepatocytes: potential and challenges in pharmacology. Annual Review of Pharmacology and Toxicology 2013, 53:147-159.
98. Muralidharan-Chari V., Clancy J.W., Sedgwick A., et al. Microvesicles: mediators of extracellular communication during cancer progression. Journal of Cell Science 2010, 123:1603-1611.
99. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends in Cell Biology 2009, 19:43-51.
100. Pap E., Pallinger E., Pasztoi M., et al. Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflammation Research 2009, 58:1-8.