Lipid-Induced Hepatocyte-Derived Extracellular Vesicles Regulate Hepatic Stellate Cells via MicroRNA Targeting Peroxisome Proliferator-Activated Receptor-γ

Cellular and Molecular Gastroenterology and Hepatology

Volumn 1, Issue 6, 2015, Pages 646-663.e4

  Povero, Davide ^a   Panera, Nadia ^b   Eguchi, Akiko ^a   Johnson, Casey D ^a   Papouchado, Bettina G ^c   de Araujo Horcel, Lucas ^a,d   Pinatel, Eva M ^e   Alisi, Anna ^b   Nobili, Valerio ^b   Feldstein, Ariel E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d Centro Universitario Lusiada   (Brazil)

^e CNR   (Italy)

Author keywords

Extracellular vesicles; Hepatic stellate cell; Lipotoxicity; Liver fibrosis; MiRNAs

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; LIPID; MICRORNA; MICRORNA 128 3P; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; CORRELATION ANALYSIS; EXOSOME; FIBROGENESIS; GAIN OF FUNCTION MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; LIPOTOXICITY; LIVER CELL; LIVER FIBROSIS; LOSS OF FUNCTION MUTATION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STELLATE CELL; WOUND HEALING;

EID: 84944445999     PISSN: None     EISSN: 2352345X     Source Type: Journal    
DOI: 10.1016/j.jcmgh.2015.07.007     Document Type: Article

References (56)

1. Roberts E.A. Non-alcoholic steatohepatitis in children. Clin Liver Dis 2007, 11:155-172.
2. Bellentani S., Saccoccio G., Masutti F., et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 2000, 132:112-117.
3. Angulo P., Keach J.C., Batts K.P., et al. Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology 1999, 30:1356-1362.
4. Knobler H., Schattner A., Zhornicki T., et al. Fatty liver-an additional and treatable feature of the insulin resistance syndrome. QJM 1999, 92:73-79.
5. Ratziu V., Giral P., Charlotte F., et al. Liver fibrosis in overweight patients. Gastroenterology 2000, 118:1117-1123.
6. Vernon G., Baranova A., Younossi Z.M. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011, 34:274-285.
7. Marchesini G., Brizi M., Morselli-Labate A.M., et al. Association of nonalcoholic fatty liver disease with insulin resistance. Am J Med 1999, 107:450-455.
8. Angulo P. Nonalcoholic fatty liver disease. New Engl J Med 2002, 346:1221-1231.
9. Andersen T., Gluud C., Franzmann M.B., et al. Hepatic effects of dietary weight loss in morbidly obese subjects. J Hepatol 1991, 12:224-229.
10. Teli M.R., James O.F., Burt A.D., et al. The natural history of nonalcoholic fatty liver: a follow-up study. Hepatology 1995, 22:1714-1719.
11. Ratziu V., Bonyhay L., Di Martino V., et al. Survival, liver failure, and hepatocellular carcinoma in obesity-related cryptogenic cirrhosis. Hepatology 2002, 35:1485-1493.
12. Bugianesi E., Leone N., Vanni E., et al. Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 2002, 123:134-140.
13. Friedman S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008, 134:1655-1669.
14. Rippe R.A., Brenner D.A. From quiescence to activation: gene regulation in hepatic stellate cells. Gastroenterology 2004, 127:1260-1262.
15. Olaso E., Friedman S.L. Molecular regulation of hepatic fibrogenesis. J Hepatol 1998, 29:836-847.
16. Povero D., Eguchi A., Niesman I.R., et al. Lipid-induced toxicity stimulates hepatocytes to release angiogenic microparticles that require Vanin-1 for uptake by endothelial cells. Sci Signa 2013, 6:ra88.
17. Povero D., Eguchi A., Li H., et al. Circulating extracellular vesicles with specific proteome and liver MicroRNAs are potential biomarkers for liver injury in experimental fatty liver disease. PLoS One 2014, 9:e113651.
18. Miura K., Yang L., van Rooijen N., et al. Hepatic recruitment of macrophages promotes nonalcoholic steatohepatitis through CCR2. Am J Physio Gastrointest Liver Physiol 2012, 302:G1310-G1321.
19. Buettner R., Scholmerich J., Bollheimer L.C. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007, 15:798-808.
20. Li Z., Berk M., McIntyre T.M., et al. The lysosomal-mitochondrial axis in free fatty acid-induced hepatic lipotoxicity. Hepatology 2008, 47:1495-1503.
21. D'Ambrosio D.N., Walewski J.L., et al. Distinct populations of hepatic stellate cells in the mouse liver have different capacities for retinoid and lipid storage. PLoS One 2011, 6:e24993.
22. Seki E., De Minicis S., Osterreicher C.H., et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007, 13:1324-1332.
23. Kornek M., Popov Y., Libermann T.A., et al. Human T cell microparticles circulate in blood of hepatitis patients and induce fibrolytic activation of hepatic stellate cells. Hepatology 2011, 53:230-242.
24. Marra F., Efsen E., Romanelli R.G., et al. Ligands of peroxisome proliferator-activated receptor gamma modulate profibrogenic and proinflammatory actions in hepatic stellate cells. Gastroenterology 2000, 119:466-478.
25. Miyahara T., Schrum L., Rippe R., et al. Peroxisome proliferator-activated receptors and hepatic stellate cell activation. J Biol Chem 2000, 275:35715-35722.
26. Sharvit E., Abramovitch S., Reif S., Bruck R. Amplified inhibition of stellate cell activation pathways by PPAR-gamma, RAR and RXR agonists. PLoS One 2013, 8:e76541.
27. Hazra S., Xiong S., Wang J., et al. Peroxisome proliferator-activated receptor gamma induces a phenotypic switch from activated to quiescent hepatic stellate cells. J Biol Chem 2004, 279:11392-11401.
28. 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.
29. Garzetti L., Menon R., Finardi A., et al. Activated macrophages release microvesicles containing polarized M1 or M2 mRNAs. J Leukocyte Biol 2014, 95:817-825.
30. Li J., Zhang Y., Liu Y., et al. Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. J Biol Chem 2013, 288:23586-23596.
31. Jansen F., Yang X., Hoelscher M., et al. Endothelial microparticle-mediated transfer of MicroRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 2013, 128:2026-2038.
32. Guo C.J., Pan Q., Xiong H., et al. Dynamic expression of miR-126 and its effects on proliferation and contraction of hepatic stellate cells. FEBS Lett 2013, 587:3792-3801.
33. Venugopal S.K., Jiang J., Kim T.H., et al. Liver fibrosis causes downregulation of miRNA-150 and miRNA-194 in hepatic stellate cells, and their overexpression causes decreased stellate cell activation. Am J Physio Gastrointest Liver Physiol 2010, 298:G101-G106.
34. He Y., Huang C., Zhang S.P., et al. The potential of microRNAs in liver fibrosis. Cell Signal 2012, 24:2268-2272.
35. Jennewein C., von Knethen A., Schmid T., et al. MicroRNA-27b contributes to lipopolysaccharide-mediated peroxisome proliferator-activated receptor gamma (PPARgamma) mRNA destabilization. J Biol Chem 2010, 285:11846-11853.
36. Ji J., Zhang J., Huang G., et al. Over-expressed microRNA-27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation. FEBS letters 2009, 583:759-766.
37. Pan S., Yang X., Jia Y., et al. Microvesicle-shuttled miR-130b reduces fat deposition in recipient primary cultured porcine adipocytes by inhibiting PPAR-g expression. J Cell Physiol 2014, 229:631-639.
38. Motohashi N., Alexander M.S., Casar J.C., et al. Identification of a novel microRNA that regulates the proliferation and differentiation in muscle side population cells. Stem Cells Dev 2012, 21:3031-3043.
39. Huang J., Yu X., Fries J.W., et al. MicroRNA function in the profibrogenic interplay upon chronic liver disease. Int J Mol Sci 2014, 15:9360-9371.
40. Bellentani S., Scaglioni F., Marino M., et al. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010, 28:155-161.
41. Loomba R., Sirlin C.B., Schwimmer J.B., et al. Advances in pediatric nonalcoholic fatty liver disease. Hepatology 2009, 50:1282-1293.
42. Li Z.Z., Berk M., McIntyre T.M., et al. Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J Biol Chem 2009, 284:5637-5644.
43. Alkhouri N., Dixon L.J., Feldstein A.E. Lipotoxicity in nonalcoholic fatty liver disease: not all lipids are created equal. Expert Rev Gastroenterol Hepatol 2009, 3:445-451.
44. Bhala N., Angulo P., van der Poorten D., et al. The natural history of nonalcoholic fatty liver disease with advanced fibrosis or cirrhosis: an international collaborative study. Hepatology 2011, 54:1208-1216.
45. Browning J.D., Szczepaniak L.S., Dobbins R., et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004, 40:1387-1395.
46. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008, 88:125-172.
47. Canbay A., Friedman S., Gores G.J. Apoptosis: the nexus of liver injury and fibrosis. Hepatology 2004, 39:273-278.
48. Watanabe A., Hashmi A., Gomes D.A., et al. Apoptotic hepatocyte DNA inhibits hepatic stellate cell chemotaxis via toll-like receptor 9. Hepatology 2007, 46:1509-1518.
49. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009, 19:43-51.
50. 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.
51. Diehl P., Fricke A., Sander L., et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 2012, 93:633-644.
52. Yuan A., Farber E.L., Rapoport A.L., et al. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 2009, 4:e4722.
53. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013, 200:373-383.
54. Kornek M., Lynch M., Mehta S.H., et al. Circulating microparticles as disease-specific biomarkers of severity of inflammation in patients with hepatitis C or nonalcoholic steatohepatitis. Gastroenterology 2012, 143:448-458.
55. 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.
56. Cheung O., Puri P., Eicken C., et al. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology 2008, 48:1810-1820.