Extracellular vesicles in liver pathobiology: Small particles with big impact

Hepatology

Volumn 64, Issue 6, 2016, Pages 2219-2233

  Hirsova, Petra ^a   Ibrahim, Samar H ^a   Verma, Vikas K ^a   Morton, Leslie A ^a   Shah, Vijay H ^a   LaRusso, Nicholas F ^a   Gores, Gregory J ^a   Malhi, Harmeet ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

ALCOHOL LIVER DISEASE; BILE DUCT CARCINOMA; BILE DUCT DISEASE; BIOGENESIS; CELL COMMUNICATION; DISEASE CLASSIFICATION; EXOSOME; HEPATITIS VIRUS; HUMAN; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER FIBROSIS; LIVER METASTASIS; LIVER REGENERATION; MOLECULAR PATHOLOGY; NONALCOHOLIC FATTY LIVER; PRIORITY JOURNAL; REVIEW; TARGET CELL; TOXIC HEPATITIS; VIRUS HEPATITIS; ANIMAL; HEPATITIS; LIVER DISEASES; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGANELLE BIOGENESIS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL COMMUNICATION; EXTRACELLULAR VESICLES; HEPATITIS; HUMANS; LIVER DISEASES; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGANELLE BIOGENESIS;

EID: 84995768489     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28814     Document Type: Review

References (97)

1. Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015;4:27066.
2. Sato K, Meng F, Glaser S, Alpini G. Exosomes in liver pathology. J Hepatol 2016;65:213–221.
3. Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell 2016;164:1226–1232.
4. Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol 2015;40:41–51.
5. Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA 2016;113:E968–E977.
6. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013;2:20360.
7. Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2013;2:20389.
8. Kowal J, Tkach M, Thery C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014;29:116–125.
9. Hurley JH, Odorizzi G. Get on the exosome bus with ALIX. Nat Cell Biol 2012;14:654–655.
10. Babst M. MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol 2011;23:452–457.
11. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008;319:1244–1247.
12. Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 2013;126:5553–5565.
13. Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F, Pageaux JF, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 2004;380:161–171.
14. Mobius W, van Donselaar E, Ohno-Iwashita Y, Shimada Y, Heijnen HF, Slot JW, et al. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 2003;4:222–231.
15. Andreu Z, Yanez-Mo M. Tetraspanins in extracellular vesicle formation and function. Front Immunol 2014;5:442.
16. Buschow SI, Nolte-'t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 2009;10:1528–1542.
17. van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 2011;21:708–721.
18. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200:373–383.
19. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009;10:513–525.
20. Fader CM, Savina A, Sanchez D, Colombo MI. Exosome secretion and red cell maturation: exploring molecular components involved in the docking and fusion of multivesicular bodies in K562 cells. Blood Cells Mol Dis 2005;35:153–157.
21. Savina A, Fader CM, Damiani MT, Colombo MI. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 2005;6:131–143.
22. Li W, Hu Y, Jiang T, Han Y, Han G, Chen J, et al. Rab27A regulates exosome secretion from lung adenocarcinoma cells A549: involvement of EPI64. APMIS 2014;122:1080–1087.
23. Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 2012;72:4920–4930.
24. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010;12:19–30.
25. Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, Lauterbach MA, et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 2010;189:223–232.
26. Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 2010;123:1603–1611.
27. Tetta C, Ghigo E, Silengo L, Deregibus MC, Camussi G. Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine 2013;44:11–19.
28. Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P, Raposo G, et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 2009;19:1875–1885.
29. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci USA 2012;109:4146–4151.
30. Fang Y, Wu N, Gan X, Yan W, Morrell JC, Gould SJ. Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 2007;5:e158.
31. Povero D, Eguchi A, Niesman IR, Andronikou N, de Mollerat du Jeu X, Mulya A, et al. Lipid-induced toxicity stimulates hepatocytes to release angiogenic microparticles that require Vanin-1 for uptake by endothelial cells. Sci Signal 2013;6:ra88.
32. Hirsova P, Ibrahim SH, Krishnan A, Verma VK, Bronk SF, Werneburg NW, et al. Lipid-induced signaling causes release of inflammatory extracellular vesicles from hepatocytes. Gastroenterology 2016;150:956–967.
33. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 2014;3.
34. Muller L, Mitsuhashi M, Simms P, Gooding WE, Whiteside TL. Tumor-derived exosomes regulate expression of immune function-related genes in human T cell subsets. Sci Rep 2016;6:20254.
35. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009;284:34211–34222.
36. Povero D, Eguchi A, Li H, Johnson CD, Papouchado BG, Wree A, 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.
37. Garcia-Martinez I, Santoro N, Chen Y, Hoque R, Ouyang X, Caprio S, et al. Hepatocyte mitochondrial DNA drives nonalcoholic steatohepatitis by activation of TLR9. J Clin Invest 2016;126:859–864.
38. Deng ZB, Liu Y, Liu C, Xiang X, Wang J, Cheng Z, et al. Immature myeloid cells induced by a high-fat diet contribute to liver inflammation. Hepatology 2009;50:1412–1420.
39. Ibrahim SH, Hirsova P, Tomita K, Bronk SF, Werneburg NW, Harrison SA, et al. Mixed lineage kinase 3 mediates release of C-X-C motif ligand 10-bearing chemotactic extracellular vesicles from lipotoxic hepatocytes. Hepatology 2016;63:731–744.
40. Ibrahim SH, Gores GJ, Hirsova P, Kirby M, Miles L, Jaeschke A, et al. Mixed lineage kinase 3 deficient mice are protected against the high fat high carbohydrate diet-induced steatohepatitis. Liver Int 2014;34:427–437.
41. Kakazu E, Mauer AS, Yin M, Malhi H. Hepatocytes release ceramide-enriched pro-inflammatory extracellular vesicles in an IRE1alpha-dependent manner. J Lipid Res 2016;57:233–245.
42. Eguchi A, Mulya A, Lazic M, Radhakrishnan D, Berk MP, Povero D, et al. Microparticles release by adipocytes act as “find-me” signals to promote macrophage migration. PloS One 2015;10:e0123110.
43. Povero D, Panera N, Eguchi A, Johnson CD, Papouchado BG, de Araujo Horcel L, et al. Lipid-induced hepatocyte-derived extracellular vesicles regulate hepatic stellate cell via microRNAs targeting PPAR-gamma. Cell Mol Gastroenterol Hepatol 2015;1:646–663.
44. Kornek M, Lynch M, Mehta SH, Lai M, Exley M, Afdhal NH, 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.
45. Murakami Y, Toyoda H, Tanahashi T, Tanaka J, Kumada T, Yoshioka Y, et al. Comprehensive miRNA expression analysis in peripheral blood can diagnose liver disease. PloS One 2012;7:e48366.
46. Bala S, Petrasek J, Mundkur S, Catalano D, Levin I, Ward J, et al. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 2012;56:1946–1957.
47. Momen-Heravi F, Bala S, Kodys K, Szabo G. Exosomes derived from alcohol-treated hepatocytes horizontally transfer liver specific miRNA-122 and sensitize monocytes to LPS. Sci Rep 2015;5:9991.
48. Verma VK, Li H, Wang R, Hirsova P, Mushref M, Liu Y, et al. Alcohol stimulates macrophage activation through caspase-dependent hepatocyte derived release of CD40L containing extracellular vesicles. J Hepatol 2016;64:651–660.
49. Saha B, Momen-Heravi F, Kodys K, Szabo G. MicroRNA cargo of extracellular vesicles from alcohol-exposed monocytes signals naive monocytes to differentiate into M2 macrophages. J Biol Chem 2016;291:149–159.
50. Momen-Heravi F, Saha B, Kodys K, Catalano D, Satishchandran A, Szabo G. Increased number of circulating exosomes and their microRNA cargos are potential novel biomarkers in alcoholic hepatitis. J Transl Med 2015;13:261.
51. Ramakrishnaiah V, Thumann C, Fofana I, Habersetzer F, Pan Q, de Ruiter PE, et al. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. Proc Natl Acad Sci USA 2013;110:13109–13113.
52. Bukong TN, Momen-Heravi F, Kodys K, Bala S, Szabo G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog 2014;10:e1004424.
53. Nagashima S, Jirintai S, Takahashi M, Kobayashi T, Tanggis, Nishizawa T, et al. Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J Gen Virol 2014;95:2166–2175.
54. Lambert C, Doring T, Prange R. Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 2007;81:9050–9060.
55. Kornek M, Popov Y, Libermann TA, Afdhal NH, Schuppan D. Human T cell microparticles circulate in blood of hepatitis patients and induce fibrolytic activation of hepatic stellate cells. Hepatology 2011;53:230–242.
56. Giugliano S, Kriss M, Golden-Mason L, Dobrinskikh E, Stone AE, Soto-Gutierrez A, et al. Hepatitis C virus infection induces autocrine interferon signaling by human liver endothelial cells and release of exosomes, which inhibits viral replication. Gastroenterology 2015;148:392–402.
57. Li J, Liu K, Liu Y, Xu Y, Zhang F, Yang H, et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat Immunol 2013;14:793–803.
58. Nojima H, Freeman CM, Schuster RM, Japtok L, Kleuser B, Edwards MJ, et al. Hepatocyte exosomes mediate liver repair and regeneration via sphingosine-1-phosphate. J Hepatol 2016;64:60–68.
59. Rodriguez-Suarez E, Gonzalez E, Hughes C, Conde-Vancells J, Rudella A, Royo F, et al. Quantitative proteomic analysis of hepatocyte-secreted extracellular vesicles reveals candidate markers for liver toxicity. J Proteomics 2014;103:227–240.
60. Holman NS, Mosedale M, Wolf KK, LeCluyse EL, Watkins PB. Subtoxic alterations in hepatocyte-derived exosomes: an early step in drug-induced liver injury? Toxicol Sci 2016;151:365–375.
61. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008;88:125–172.
62. Wang R, Ding Q, Yaqoob U, de Assuncao TM, Verma VK, Hirsova P, et al. Exosome adherence and internalization by hepatic stellate cells triggers sphingosine 1-phosphate dependent migration. J Biol Chem 2015;290:30684–30696.
63. Chen L, Charrier A, Zhou Y, Chen R, Yu B, Agarwal K, et al. Epigenetic regulation of connective tissue growth factor by MicroRNA-214 delivery in exosomes from mouse or human hepatic stellate cells. Hepatology 2014;59:1118–1129.
64. Charrier A, Chen R, Chen L, Kemper S, Hattori T, Takigawa M, et al. Exosomes mediate intercellular transfer of pro-fibrogenic connective tissue growth factor (CCN2) between hepatic stellate cells, the principal fibrotic cells in the liver. Surgery 2014;156:548–555.
65. Witek RP, Yang L, Liu R, Jung Y, Omenetti A, Syn WK, et al. Liver cell-derived microparticles activate hedgehog signaling and alter gene expression in hepatic endothelial cells. Gastroenterology 2009;136:320–330.
66. Thabut D, Shah V. Intrahepatic angiogenesis and sinusoidal remodeling in chronic liver disease: new targets for the treatment of portal hypertension? J Hepatol 2010;53:976–980.
67. Owens AP 3rd, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011;108:1284–1297.
68. Nieuwland R, Berckmans RJ, McGregor S, Boing AN, Romijn FP, Westendorp RG, et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood 2000;95:930–935.
69. Valla DC. Thrombosis and anticoagulation in liver disease. Hepatology 2008;47:1384–1393.
70. Masyuk AI, Huang BQ, Ward CJ, Gradilone SA, Banales JM, Masyuk TV, et al. Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia. Am J Physiol Gastrointest Liver Physiol 2010;299:G990–G999.
71. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008;10:619–624.
72. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 2009;106:3794–3799.
73. Jaiswal R, Gong J, Sambasivam S, Combes V, Mathys JM, Davey R, et al. Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J 2012;26:420–429.
74. + T lymphocytes. J Immunol 2009;183:3720–3730.
75. Sidhu SS, Mengistab AT, Tauscher AN, LaVail J, Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004;23:956–963.
76. Tesselaar ME, Romijn FP, Van Der Linden IK, Prins FA, Bertina RM, Osanto S. Microparticle-associated tissue factor activity: a link between cancer and thrombosis? J Thromb Haemost 2007;5:520–527.
77. 2 to tumor cells. J Immunol 2013;191:3453–3461.
78. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011;54:1237–1248.
79. Wei JX, Lv LH, Wan YL, Cao Y, Li GL, Lin HM, et al. Vps4A functions as a tumor suppressor by regulating the secretion and uptake of exosomal microRNAs in human hepatoma cells. Hepatology 2015;61:1284–1294.
80. Lv LH, Wan YL, Lin Y, Zhang W, Yang M, Li GL, 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. J Biol Chem 2012;287:15874–15885.
81. Takahashi K, Yan IK, Wood J, Haga H, Patel T. Involvement of extracellular vesicle long noncoding RNA (linc-VLDLR) in tumor cell responses to chemotherapy. Mol Cancer Res 2014;12:1377–1387.
82. Mohankumar S, Patel T. Extracellular vesicle long noncoding RNA as potential biomarkers of liver cancer. Brief Funct Genomics 2016;15:249–256.
83. Haga H, Yan IK, Takahashi K, Wood J, Zubair A, Patel T. Tumour cell-derived extracellular vesicles interact with mesenchymal stem cells to modulate the microenvironment and enhance cholangiocarcinoma growth. J Extracell Vesicles 2015;4:24900.
84. Li L, Masica D, Ishida M, Tomuleasa C, Umegaki S, Kalloo AN, et al. Human bile contains microRNA-laden extracellular vesicles that can be used for cholangiocarcinoma diagnosis. Hepatology 2014;60:896–907.
85. Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol 2015;17:816–826.
86. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015;527:329–335.
87. Minciacchi VR, You S, Spinelli C, Morley S, Zandian M, Aspuria PJ, et al. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget 2015;6:11327–11341.
88. Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010;120:457–471.
89. Cai Z, Yang F, Yu L, Yu Z, Jiang L, Wang Q, et al. Activated T cell exosomes promote tumor invasion via Fas signaling pathway. J Immunol 2012;188:5954–5961.
90. Khan M, Nickoloff E, Abramova T, Johnson J, Verma SK, Krishnamurthy P, et al. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ Res 2015;117:52–64.
91. Sluijter JP, Verhage V, Deddens JC, van den Akker F, Doevendans PA. Microvesicles and exosomes for intracardiac communication. Cardiovasc Res 2014;102:302–311.
92. Li T, Yan Y, Wang B, Qian H, Zhang X, Shen L, et al. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev 2013;22:845–854.
93. Lener T, Gimona M, Aigner L, Borger V, Buzas E, Camussi G, et al. Applying extracellular vesicles based therapeutics in clinical trials—an ISEV position paper. J Extracell Vesicles 2015;4:30087.
94. Wang Q, Zhuang X, Mu J, Deng ZB, Jiang H, Zhang L, et al. Delivery of therapeutic agents by nanoparticles made of grapefruit-derived lipids. Nat Commun 2013;4:1867.
95. Pallet N, Sirois I, Bell C, Hanafi LA, Hamelin K, Dieude M, et al. A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 2013;13:1108–1120.
96. Altan-Bonnet N, Chen YH. Intercellular transmission of viral populations with vesicles. J Virol 2015;89:12242–12244.
97. Chen YH, Du W, Hagemeijer MC, Takvorian PM, Pau C, Cali A, et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 2015;160:619–630.