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Epigenetic regulation of hepatic stellate cell activation and liver fibrosis

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El Taghdouini, Adil [UCL] van Grunsven, Leo A.

Introduction: Chronic liver injury to hepatocytes or cholangiocytes, when left unmanaged, leads to the development of liver fibrosis, a condition characterized by the excessive intrahepatic deposition of extracellular matrix proteins. Activated hepatic stellate cells constitute the predominant source of extracellular matrix in fibrotic livers and their transition from a quiescent state during fibrogenesis is associated with important alterations in their transcriptional and epigenetic landscape. Areas covered: We briefly describe the processes involved in hepatic stellate cell activation and discuss our current understanding of alterations in the epigenetic landscape, i.e DNA methylation, histone modifications and the functional role of non-coding RNAs that accompany this key event in the development of chronic liver disease. Expert commentary: Although great progress has been made, our understanding of the epigenetic regulation of hepatic stellate cell activation is limited and, thus far, insufficient to allow the development of epigenetic drugs that can selectively interrupt liver fibrosis. © 2016 Informa UK Limited, trading as Taylor & Francis Group.

Document type Article de périodique (Journal article)
Publication date 2016
Language Anglais
Journal information "Expert Review of Gastroenterology & Hepatology" - Vol. 10, no.12, p. 1397-1408 (2016)
Peer reviewed yes
Publisher Expert Reviews Ltd. (London)
issn 1747-4124
e-issn 1747-4132
Publication status Publié
Affiliations UCL - (SLuc) Centre de thérapie tissulaire et cellulaire
UCL - SSS/IREC - Institut de recherche expérimentale et clinique
Links
  1. Wynn TA, Cellular and molecular mechanisms of fibrosis, 10.1002/path.2277
  2. Zeisberg Elisabeth M, Zeisberg Michael, The role of promoter hypermethylation in fibroblast activation and fibrogenesis : Role of promoter hypermethylation in fibroblast activation and fibrogenesis, 10.1002/path.4120
  3. Forner Alejandro, Llovet Josep M, Bruix Jordi, Hepatocellular carcinoma, 10.1016/s0140-6736(11)61347-0
  4. Parkin D. Maxwell, Bray Freddie, Ferlay Jacques, Pisani Paola, Estimating the world cancer burden: Globocan 2000, 10.1002/ijc.1440
  5. Blachier Martin, Leleu Henri, Peck-Radosavljevic Markus, Valla Dominique-Charles, Roudot-Thoraval Françoise, The burden of liver disease in Europe: A review of available epidemiological data, 10.1016/j.jhep.2012.12.005
  6. Curry Michael P., O’Leary Jacqueline G., Bzowej Natalie, Muir Andrew J., Korenblat Kevin M., Fenkel Jonathan M., Reddy K. Rajender, Lawitz Eric, Flamm Steven L., Schiano Thomas, Teperman Lewis, Fontana Robert, Schiff Eugene, Fried Michael, Doehle Brian, An Di, McNally John, Osinusi Anu, Brainard Diana M., McHutchison John G., Brown Robert S., Charlton Michael, Sofosbuvir and Velpatasvir for HCV in Patients with Decompensated Cirrhosis, 10.1056/nejmoa1512614
  7. Krishna Murli, Microscopic anatomy of the liver, 10.1002/cld.147
  8. Michelotti GA, J Clin Invest, 123, 2380 (2013)
  9. Henderson Neil C, Arnold Thomas D, Katamura Yoshio, Giacomini Marilyn M, Rodriguez Juan D, McCarty Joseph H, Pellicoro Antonella, Raschperger Elisabeth, Betsholtz Christer, Ruminski Peter G, Griggs David W, Prinsen Michael J, Maher Jacquelyn J, Iredale John P, Lacy-Hulbert Adam, Adams Ralf H, Sheppard Dean, Targeting of αv integrin identifies a core molecular pathway that regulates fibrosis in several organs, 10.1038/nm.3282
  10. Mederacke Ingmar, Hsu Christine C., Troeger Juliane S., Huebener Peter, Mu Xueru, Dapito Dianne H., Pradere Jean-Philippe, Schwabe Robert F., Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology, 10.1038/ncomms3823
  11. Puche Juan E., Lee Youngmin A., Jiao Jingjing, Aloman Costica, Fiel Maria I., Muñoz Ursula, Kraus Thomas, Lee Tingfang, Yee Hal F., Friedman Scott L., A novel murine model to deplete hepatic stellate cells uncovers their role in amplifying liver damage in mice, 10.1002/hep.26053
  12. Iwaisako K., Jiang C., Zhang M., Cong M., Moore-Morris T. J., Park T. J., Liu X., Xu J., Wang P., Paik Y.-H., Meng F., Asagiri M., Murray L. A., Hofmann A. F., Iida T., Glass C. K., Brenner D. A., Kisseleva T., Origin of myofibroblasts in the fibrotic liver in mice, 10.1073/pnas.1400062111
  13. Blaner William S., O'Byrne Sheila M., Wongsiriroj Nuttaporn, Kluwe Johannes, D'Ambrosio Diana M., Jiang Hongfeng, Schwabe Robert F., Hillman Elizabeth M.C., Piantedosi Roseann, Libien Jenny, Hepatic stellate cell lipid droplets: A specialized lipid droplet for retinoid storage, 10.1016/j.bbalip.2008.11.001
  14. Lee Youngmin A, Wallace Michael C, Friedman Scott L, Pathobiology of liver fibrosis: a translational success story, 10.1136/gutjnl-2014-306842
  15. Friedman S. L., Hepatic Stellate Cells: Protean, Multifunctional, and Enigmatic Cells of the Liver, 10.1152/physrev.00013.2007
  16. DeLeve Laurie D., Liver sinusoidal endothelial cells in hepatic fibrosis : DELEVE, 10.1002/hep.27376
  17. Holland-Fischer P., Gronbaek H., Sandahl T. D., Moestrup S. K., Riggio O., Ridola L., Aagaard N. K., Moller H. J., Vilstrup H., Kupffer cells are activated in cirrhotic portal hypertension and not normalised by TIPS, 10.1136/gut.2010.234542
  18. Weiskirchen R, Hepatobiliary Surg Nutr, 3, 344 (2014)
  19. Rojkind M., Rojkind M.H., Cordero-Hernandez J., In vivo Collagen Synthesis and Deposition in Fibrotic and Regenerating Rat Livers, 10.1016/s0174-173x(83)80015-6
  20. Bataller Ramón, Brenner David A., Liver fibrosis, 10.1172/jci24282
  21. Zhan Shan-Shan, Jiang Joy X., Wu Jian, Halsted Charles, Friedman Scott L., Zern Mark A., Torok Natalie J., Phagocytosis of apoptotic bodies by hepatic stellate cells induces NADPH oxidase and is associated with liver fibrosisin vivo, 10.1002/hep.21093
  22. Bataller Ramón, Schwabe Robert F., Choi Youkyung H., Yang Liu, Paik Yong Han, Lindquist Jeffrey, Qian Ting, Schoonhoven Robert, Hagedorn Curt H., Lemasters John J., Brenner David A., NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis, 10.1172/jci18212
  23. Adachi Tohru, Togashi Hitoshi, Suzuki Akihiko, Kasai Shigenobu, Ito Junitsu, Sugahara Kazuhiko, Kawata Sumio, NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells, 10.1002/hep.20719
  24. Guimarães Eduardo L.M., Empsen Christophe, Geerts Albert, van Grunsven Leo A., Advanced glycation end products induce production of reactive oxygen species via the activation of NADPH oxidase in murine hepatic stellate cells, 10.1016/j.jhep.2009.12.007
  25. García-Trevijano Elena R., Iraburu María J., Fontana Luis, Domínguez-Rosales José A., Auster Anitra, Covarrubias-Pinedo Amador, Rojkind Marcos, Transforming growth factor β1induces the expression of α1(i) procollagen mRNA by a hydrogen peroxide-C/EBPβ-dependent mechanism in rat hepatic stellate cells : Transforming Growth Factor β1 Induces the Expression of α1(I) Procollagen mRNA by a Hydrogen Peroxide-C/EBPβ-Dependent Mechanism in Rat Hepatic Stella, 10.1002/hep.510290346
  26. Tahan Gulgun, Tarcin Orhan, Tahan Veysel, Eren Fatih, Gedik Nursal, Sahan Elife, Biberoglu Nilgun, Guzel Savas, Bozbas Aysun, Tozun Nurdan, Yucel Osman, The Effects of N-Acetylcysteine on Bile Duct Ligation–Induced Liver Fibrosis in Rats, 10.1007/s10620-006-9717-9
  27. Baumgardner JN, J Nutr, 138, 1872 (2008)
  28. Cichoż-Lach Halina, Oxidative stress as a crucial factor in liver diseases, 10.3748/wjg.v20.i25.8082
  29. Dranoff Jonathan A., Wells Rebecca G., Portal fibroblasts: Underappreciated mediators of biliary fibrosis, 10.1002/hep.23405
  30. Beaussier Marc, Wendum Dominique, Schiffer Eduardo, Dumont Sylvie, Rey Colette, Lienhart André, Housset Chantal, Prominent contribution of portal mesenchymal cells to liver fibrosis in ischemic and obstructive cholestatic injuries, 10.1038/labinvest.3700513
  31. Xie Guanhua, Wang Xiangdong, Wang Lei, Wang Lin, Atkinson Roscoe D., Kanel Gary C., Gaarde William A., DeLeve Laurie D., Role of Differentiation of Liver Sinusoidal Endothelial Cells in Progression and Regression of Hepatic Fibrosis in Rats, 10.1053/j.gastro.2011.12.017
  32. Zimmermann Henning W., Trautwein Christian, Tacke Frank, Functional Role of Monocytes and Macrophages for the Inflammatory Response in Acute Liver Injury, 10.3389/fphys.2012.00056
  33. Yu Q, Genes Dev, 14, 163 (2000)
  34. Pradere Jean-Philippe, Kluwe Johannes, De Minicis Samuele, Jiao Jing-Jing, Gwak Geum-Youn, Dapito Dianne H., Jang Myoung-Kuk, Guenther Nina D., Mederacke Ingmar, Friedman Richard, Dragomir Ana-Cristina, Aloman Costica, Schwabe Robert F., Hepatic macrophages but not dendritic cells contribute to liver fibrosis by promoting the survival of activated hepatic stellate cells in mice : Hepatology, Vol. 57, No. X, 2013, 10.1002/hep.26429
  35. Tacke Frank, Zimmermann Henning W., Macrophage heterogeneity in liver injury and fibrosis, 10.1016/j.jhep.2013.12.025
  36. Scott Charlotte L., Zheng Fang, De Baetselier Patrick, Martens Liesbet, Saeys Yvan, De Prijck Sofie, Lippens Saskia, Abels Chloé, Schoonooghe Steve, Raes Geert, Devoogdt Nick, Lambrecht Bart N., Beschin Alain, Guilliams Martin, Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells, 10.1038/ncomms10321
  37. Hernández–Gea Virginia, Ghiassi–Nejad Zahra, Rozenfeld Raphael, Gordon Ronald, Fiel Maria Isabel, Yue Zhenyu, Czaja Mark J., Friedman Scott L., Autophagy Releases Lipid That Promotes Fibrogenesis by Activated Hepatic Stellate Cells in Mice and in Human Tissues, 10.1053/j.gastro.2011.12.044
  38. Thoen Lien F.R., Guimarães Eduardo L.M., Dollé Laurent, Mannaerts Inge, Najimi Mustapha, Sokal Etienne, van Grunsven Leo A., A role for autophagy during hepatic stellate cell activation, 10.1016/j.jhep.2011.07.010
  39. Kluwe J., Wongsiriroj N., Troeger J. S., Gwak G.-Y., Dapito D. H., Pradere J.-P., Jiang H., Siddiqi M., Piantedosi R., O'Byrne S. M., Blaner W. S., Schwabe R. F., Absence of hepatic stellate cell retinoid lipid droplets does not enhance hepatic fibrosis but decreases hepatic carcinogenesis, 10.1136/gut.2010.209551
  40. Urtasun Raquel, Lopategi Aritz, George Joseph, Leung Tung-Ming, Lu Yongke, Wang Xiaodong, Ge Xiaodong, Fiel Maria Isabel, Nieto Natalia, Osteopontin, an oxidant stress sensitive cytokine, up-regulates collagen-I via integrin αVβ3 engagement and PI3K/pAkt/NFκB signaling, 10.1002/hep.24701
  41. Liu Yan, Liu Heng, Meyer Christoph, Li Jun, Nadalin Silvio, Königsrainer Alfred, Weng Honglei, Dooley Steven, ten Dijke Peter, Transforming Growth Factor-β (TGF-β)-mediated Connective Tissue Growth Factor (CTGF) Expression in Hepatic Stellate Cells Requires Stat3 Signaling Activation, 10.1074/jbc.m113.478685
  42. Melton Andrew C., Yee Hal F., Hepatic stellate cell protrusions couple platelet-derived growth factor-BB to chemotaxis, 10.1002/hep.21606
  43. Yang Changqing, Zeisberg Michael, Mosterman Barbara, Sudhakar Akulapalli, Yerramalla Udaya, Holthaus Kathryn, Xu Lieming, Eng Francis, Afdhal Nezam, Kalluri Raghu, Liver fibrosis: Insights into migration of hepatic stellate cells in response to extracellular matrix and growth factors, 10.1053/gast.2003.50012
  44. Liu Zhenan, Rossen Elke Van, Timmermans Jean-Pierre, Geerts Albert, van Grunsven Leo A., Reynaert Hendrik, Distinct roles for non-muscle myosin II isoforms in mouse hepatic stellate cells, 10.1016/j.jhep.2010.06.020
  45. Dib N., Current management of the complications of portal hypertension: variceal bleeding and ascites, 10.1503/cmaj.051700
  46. Louis Hubert, Van Laethem Jean-Luc, Wu Wei, Quertinmont Eric, Degraef Chantal, Van den Berg Kit, Demols Anne, Goldman Michel, Le Moine Olivier, Geerts Albert, Devière Jacques, Interleukin-10 controls neutrophilic infiltration, hepatocyte proliferation, and liver fibrosis induced by carbon tetrachloride in mice : Interleukin-10 Controls Neutrophilic Infiltration, Hepatocyte Proliferation, and Liver Fibrosis Induced by Carbon Tetrachloride in Mice, 10.1002/hep.510280621
  47. Kisseleva T., Cong M., Paik Y., Scholten D., Jiang C., Benner C., Iwaisako K., Moore-Morris T., Scott B., Tsukamoto H., Evans S. M., Dillmann W., Glass C. K., Brenner D. A., Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis, 10.1073/pnas.1201840109
  48. Troeger Juliane S., Mederacke Ingmar, Gwak Geum–Youn, Dapito Dianne H., Mu Xueru, Hsu Christine C., Pradere Jean–Philippe, Friedman Richard A., Schwabe Robert F., Deactivation of Hepatic Stellate Cells During Liver Fibrosis Resolution in Mice, 10.1053/j.gastro.2012.06.036
  49. Oakley Fiona, Trim Nathan, Constandinou Christothea M., Ye Weilan, Gray Alane M., Frantz Gretchen, Hillan Kenneth, Kendall Tim, Benyon R. Christopher, Mann Derek A., Iredale John P., Hepatocytes Express Nerve Growth Factor during Liver Injury, 10.1016/s0002-9440(10)63544-4
  50. Radaeva Svetlana, Sun Rui, Jaruga Barbara, Nguyen Van T., Tian Zhigang, Gao Bin, Natural Killer Cells Ameliorate Liver Fibrosis by Killing Activated Stellate Cells in NKG2D-Dependent and Tumor Necrosis Factor–Related Apoptosis-Inducing Ligand–Dependent Manners, 10.1053/j.gastro.2005.10.055
  51. Fischer Richard, Cariers Alexandra, Reinehr Roland, Häussinger Dieter, Caspase 9–dependent killing of hepatic stellate cells by activated Kupffer cells, 10.1053/gast.2002.35384
  52. Kisseleva Tatiana, Brenner David A., Inactivation of myofibroblasts during regression of liver fibrosis, 10.4161/cc.23549
  53. Sharma S., Kelly T. K., Jones P. A., Epigenetics in cancer, 10.1093/carcin/bgp220
  54. Page Agata, Mann Derek A., Epigenetic regulation of liver fibrosis, 10.1016/j.clinre.2015.05.013
  55. Schübeler Dirk, Function and information content of DNA methylation, 10.1038/nature14192
  56. Auclair Ghislain, Weber Michael, Mechanisms of DNA methylation and demethylation in mammals, 10.1016/j.biochi.2012.05.016
  57. Jones Peter A., Functions of DNA methylation: islands, start sites, gene bodies and beyond, 10.1038/nrg3230
  58. Chen Zhao-xia, Riggs Arthur D., DNA Methylation and Demethylation in Mammals, 10.1074/jbc.r110.205286
  59. Rabinovich Einat I., Kapetanaki Maria G., Steinfeld Israel, Gibson Kevin F., Pandit Kusum V., Yu Guoying, Yakhini Zohar, Kaminski Naftali, Global Methylation Patterns in Idiopathic Pulmonary Fibrosis, 10.1371/journal.pone.0033770
  60. Sanders Yan Y., Ambalavanan Namasivayam, Halloran Brian, Zhang Xiangyu, Liu Hui, Crossman David K., Bray Molly, Zhang Kui, Thannickal Victor J., Hagood James S., Altered DNA Methylation Profile in Idiopathic Pulmonary Fibrosis, 10.1164/rccm.201201-0077oc
  61. Huang Steven K., Scruggs Anne M., McEachin Richard C., White Eric S., Peters-Golden Marc, Lung Fibroblasts from Patients with Idiopathic Pulmonary Fibrosis Exhibit Genome-Wide Differences in DNA Methylation Compared to Fibroblasts from Nonfibrotic Lung, 10.1371/journal.pone.0107055
  62. Bechtel Wibke, McGoohan Scott, Zeisberg Elisabeth M, Müller Gerhard A, Kalbacher Hubert, Salant David J, Müller Claudia A, Kalluri Raghu, Zeisberg Michael, Methylation determines fibroblast activation and fibrogenesis in the kidney, 10.1038/nm.2135
  63. Russell Shirley B., Russell James D., Trupin Kathryn M., Gayden Angela E., Opalenik Susan R., Nanney Lillian B., Broquist Alan H., Raju Latha, Williams Scott M., Epigenetically Altered Wound Healing in Keloid Fibroblasts, 10.1038/jid.2010.162
  64. Murphy Susan K., Yang Hyuna, Moylan Cynthia A., Pang Herbert, Dellinger Andrew, Abdelmalek Manal F., Garrett Melanie E., Ashley–Koch Allison, Suzuki Ayako, Tillmann Hans L., Hauser Michael A., Diehl Anna Mae, Relationship Between Methylome and Transcriptome in Patients With Nonalcoholic Fatty Liver Disease, 10.1053/j.gastro.2013.07.047
  65. Hardy Timothy, Zeybel Mujdat, Day Christopher P, Dipper Christian, Masson Steven, McPherson Stuart, Henderson Elsbeth, Tiniakos Dina, White Steve, French Jeremy, Mann Derek A, Anstee Quentin M, Mann Jelena, Plasma DNA methylation: a potential biomarker for stratification of liver fibrosis in non-alcoholic fatty liver disease, 10.1136/gutjnl-2016-311526
  66. Robinson Claire M., Watson Chris J., Baugh John A., Epigenetics within the matrix : A neo-regulator of fibrotic disease, 10.4161/epi.21567
  67. Mann J, Oakley F, Akiboye F, Elsharkawy A, Thorne A W, Mann D A, Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: implications for wound healing and fibrogenesis, 10.1038/sj.cdd.4401979
  68. Mann Jelena, Chu David C.K., Maxwell Aidan, Oakley Fiona, Zhu Nian–Ling, Tsukamoto Hidekazu, Mann Derek A., MeCP2 Controls an Epigenetic Pathway That Promotes Myofibroblast Transdifferentiation and Fibrosis, 10.1053/j.gastro.2009.10.002
  69. El Taghdouini Adil, Sørensen Anita L., Reiner Andrew H., Coll Mar, Verhulst Stefaan, Mannaerts Inge, Øie Cristina I., Smedsrød Bård, Najimi Mustapha, Sokal Etienne, Luttun Aernout, Sancho-Bru Pau, Collas Philippe, van Grunsven Leo A., Genome-wide analysis of DNA methylation and gene expression patterns in purified, uncultured human liver cells and activated hepatic stellate cells, 10.18632/oncotarget.4925
  70. Götze Silke, Schumacher Eva C., Kordes Claus, Häussinger Dieter, Epigenetic Changes during Hepatic Stellate Cell Activation, 10.1371/journal.pone.0128745
  71. Matsui Hiroko, Kawada Norifumi, Effect of S-adenosyl-l-methionine on the activation, proliferation and contraction of hepatic stellate cells, 10.1016/j.ejphar.2004.12.041
  72. Rohlf Thimo, Steiner Lydia, Przybilla Jens, Prohaska Sonja, Binder Hans, Galle Jörg, Modeling the dynamic epigenome: from histone modifications towards self-organizing chromatin, 10.2217/epi.11.117
  73. Bannister Andrew J, Kouzarides Tony, Regulation of chromatin by histone modifications, 10.1038/cr.2011.22
  74. Portela Anna, Esteller Manel, Epigenetic modifications and human disease, 10.1038/nbt.1685
  75. Lam Michael T.Y., Li Wenbo, Rosenfeld Michael G., Glass Christopher K., Enhancer RNAs and regulated transcriptional programs, 10.1016/j.tibs.2014.02.007
  76. Vermeulen Michiel, Mulder Klaas W., Denissov Sergei, Pijnappel W.W.M.Pim, van Schaik Frederik M.A., Varier Radhika A., Baltissen Marijke P.A., Stunnenberg Henk G., Mann Matthias, Timmers H.Th.Marc, Selective Anchoring of TFIID to Nucleosomes by Trimethylation of Histone H3 Lysine 4, 10.1016/j.cell.2007.08.016
  77. Perugorria Maria Jesus, Wilson Caroline L., Zeybel Mujdat, Walsh Meagan, Amin Shilu, Robinson Stuart, White Steven A., Burt Alastair D., Oakley Fiona, Tsukamoto Hidekazu, Mann Derek A., Mann Jelena, Histone methyltransferase ASH1 orchestrates fibrogenic gene transcription during myofibroblast transdifferentiation, 10.1002/hep.25754
  78. KIM JEE-SOO, SHUKLA SHIVENDRA D., HISTONE H3 MODIFICATIONS IN RAT HEPATIC STELLATE CELLS BY ETHANOL, 10.1093/alcalc/agh170
  79. Page Agata, Paoli Pier P., Hill Stephen J., Howarth Rachel, Wu Raymond, Kweon Soo-Mi, French Jeremy, White Steve, Tsukamoto Hidekazu, Mann Derek A., Mann Jelena, Alcohol directly stimulates epigenetic modifications in hepatic stellate cells, 10.1016/j.jhep.2014.09.033
  80. Tian Wenfang, Xu Huihui, Fang Fei, Chen Qi, Xu Yong, Shen Aiguo, Brahma-related gene 1 bridges epigenetic regulation of proinflammatory cytokine production to steatohepatitis in mice, 10.1002/hep.26207
  81. Bulger Michael, Groudine Mark, Functional and Mechanistic Diversity of Distal Transcription Enhancers, 10.1016/j.cell.2011.01.024
  82. Kim Tae-Kyung, Hemberg Martin, Gray Jesse M., Enhancer RNAs: A Class of Long Noncoding RNAs Synthesized at Enhancers: Figure 1., 10.1101/cshperspect.a018622
  83. Mannaerts Inge, Nuytten Nele R., Rogiers Vera, Vanderkerken Karin, van Grunsven Leo A., Geerts Albert, Chronic administration of valproic acid inhibits activation of mouse hepatic stellate cellsin vitroandin vivo, 10.1002/hep.23334
  84. Van Beneden Katrien, Mannaerts Inge, Pauwels Marina, Van den Branden Christiane, van Grunsven Leo A, HDAC inhibitors in experimental liver and kidney fibrosis, 10.1186/1755-1536-6-1
  85. Lee Sung Hee, Zhao Yu-Zhe, Park Eun-Jeon, Che Xian-Hua, Seo Geom Seog, Sohn Dong Hwan, 2′,4′,6′-Tris(methoxymethoxy) chalcone induces apoptosis by enhancing Fas-ligand in activated hepatic stellate cells, 10.1016/j.ejphar.2011.01.067
  86. Qin Lan, Han Yuan-Ping, Epigenetic Repression of Matrix Metalloproteinases in Myofibroblastic Hepatic Stellate Cells through Histone Deacetylases 4, 10.2353/ajpath.2010.100011
  87. Mannaerts Inge, Eysackers Nathalie, Onyema Oscar O., Van Beneden Katrien, Valente Sergio, Mai Antonello, Odenthal Margarete, van Grunsven Leo A., Class II HDAC Inhibition Hampers Hepatic Stellate Cell Activation by Induction of MicroRNA-29, 10.1371/journal.pone.0055786
  88. Wang Yu-Gang, Givinostat inhibition of hepatic stellate cell proliferation and protein acetylation, 10.3748/wjg.v21.i27.8326
  89. Park Ki Cheong, Park Ji Hyun, Jeon Jeong Yong, Kim Sang Yong, Kim Jung Min, Lim Chang Yong, Lee Tae Hyung, Kim Hyung Kwan, Lee Hyun Gyu, Kim Sung Min, Kwon Ho Jeong, Suh Jin Suck, Kim Seung Won, Choi Seung Hoon, A new histone deacetylase inhibitor improves liver fibrosis in BDL rats through suppression of hepatic stellate cells : Suppression of hepatic fibrosis, 10.1111/bph.12590
  90. Bartel David P, MicroRNAs, 10.1016/s0092-8674(04)00045-5
  91. Bueno María José, Malumbres Marcos, MicroRNAs and the cell cycle, 10.1016/j.bbadis.2011.02.002
  92. Scott Michelle S., Ono Motoharu, From snoRNA to miRNA: Dual function regulatory non-coding RNAs, 10.1016/j.biochi.2011.05.026
  93. He Lin, Hannon Gregory J., MicroRNAs: small RNAs with a big role in gene regulation, 10.1038/nrg1379
  94. Li Zhonghan, Rana Tariq M., Therapeutic targeting of microRNAs: current status and future challenges, 10.1038/nrd4359
  95. Guo Huili, Ingolia Nicholas T., Weissman Jonathan S., Bartel David P., Mammalian microRNAs predominantly act to decrease target mRNA levels, 10.1038/nature09267
  96. Huang Jia, Yu Xiaojie, Fries Jochen, Zhang Li'ang, Odenthal Margarete, MicroRNA Function in the Profibrogenic Interplay upon Chronic Liver Disease, 10.3390/ijms15069360
  97. Lambrecht Joeri, Mannaerts Inge, van Grunsven Leo A., The role of miRNAs in stress-responsive hepatic stellate cells during liver fibrosis, 10.3389/fphys.2015.00209
  98. Guo Can-Jie, Pan Qin, Cheng Tao, Jiang Bo, Chen Guang-Yu, Li Ding-Guo, Changes in microRNAs associated with hepatic stellate cell activation status identify signaling pathways : Signaling pathways regulated in HSCs by miRNAs, 10.1111/j.1742-4658.2009.07213.x
  99. Maubach Gunter, miRNA studies inin vitroandin vivoactivated hepatic stellate cells, 10.3748/wjg.v17.i22.2748
  100. Ji Juling, Zhang Jinsheng, Huang Guangcun, Qian Jin, Wang Xueqing, Mei Shuang, Over-expressed microRNA-27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation, 10.1016/j.febslet.2009.01.034
  101. Lakner Ashley M., Steuerwald Nury M., Walling Tracy L., Ghosh Sriparna, Li Ting, McKillop Iain H., Russo Mark W., Bonkovsky Herbert L., Schrum Laura W., Inhibitory effects of microRNA 19b in hepatic stellate cell-mediated fibrogenesis, 10.1002/hep.25613
  102. Chen Chao, Wu Chao-Qun, Zhang Zong-Qi, Yao Ding-Kang, Zhu Liang, Loss of expression of miR-335 is implicated in hepatic stellate cell migration and activation, 10.1016/j.yexcr.2011.05.001
  103. Roderburg Christoph, Urban Gerd-Willem, Bettermann Kira, Vucur Mihael, Zimmermann Henning, Schmidt Sabine, Janssen Jörn, Koppe Christiane, Knolle Percy, Castoldi Mirco, Tacke Frank, Trautwein Christian, Luedde Tom, Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis, 10.1002/hep.23922
  104. Pogribny Igor P, Starlard-Davenport Athena, Tryndyak Volodymyr P, Han Tao, Ross Sharon A, Rusyn Ivan, Beland Frederick A, Difference in expression of hepatic microRNAs miR-29c, miR-34a, miR-155, and miR-200b is associated with strain-specific susceptibility to dietary nonalcoholic steatohepatitis in mice, 10.1038/labinvest.2010.113
  105. Bandyopadhyay Sarmistha, Friedman Robin C., Marquez Rebecca T., Keck Kathy, Kong Benjamin, Icardi Michael S., Brown Kyle E., Burge Christopher B., Schmidt Warren N., Wang Yulei, McCaffrey Anton P., Hepatitis C Virus Infection and Hepatic Stellate Cell Activation Downregulate miR-29: miR-29 Overexpression Reduces Hepatitis C Viral Abundance in Culture, 10.1093/infdis/jir186
  106. Mott J L, Kobayashi S, Bronk S F, Gores G J, mir-29 regulates Mcl-1 protein expression and apoptosis, 10.1038/sj.onc.1210436
  107. Xiong Y, Hepatology, 51, 836 (2010)
  108. Garzon R., Liu S., Fabbri M., Liu Z., Heaphy C. E.A., Callegari E., Schwind S., Pang J., Yu J., Muthusamy N., Havelange V., Volinia S., Blum W., Rush L. J., Perrotti D., Andreeff M., Bloomfield C. D., Byrd J. C., Chan K., Wu L.-C., Croce C. M., Marcucci G., MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1, 10.1182/blood-2008-07-170589
  109. Kwiecinski Monika, Noetel Andrea, Elfimova Natalia, Trebicka Jonel, Schievenbusch Stephanie, Strack Ingo, Molnar Levente, von Brandenstein Melanie, Töx Ulrich, Nischt Roswitha, Coutelle Oliver, Dienes Hans Peter, Odenthal Margarete, Hepatocyte Growth Factor (HGF) Inhibits Collagen I and IV Synthesis in Hepatic Stellate Cells by miRNA-29 Induction, 10.1371/journal.pone.0024568
  110. Sekiya Yumiko, Ogawa Tomohiro, Yoshizato Katsutoshi, Ikeda Kazuo, Kawada Norifumi, Suppression of hepatic stellate cell activation by microRNA-29b, 10.1016/j.bbrc.2011.07.041
  111. Kwiecinski Monika, Elfimova Natalia, Noetel Andrea, Töx Ulrich, Steffen Hans-Michael, Hacker Ulrich, Nischt Roswitha, Dienes Hans Peter, Odenthal Margarete, Expression of platelet-derived growth factor-C and insulin-like growth factor I in hepatic stellate cells is inhibited by miR-29, 10.1038/labinvest.2012.70
  112. Lakner Ashley M, Daily genetic profiling indicates JAK/STAT signaling promotes early hepatic stellate cell transdifferentiation, 10.3748/wjg.v16.i40.5047
  113. Chen Shao-Long, Zheng Ming-Hua, Yang Tao, Song Mei, Chen Yong-Ping, Disparate profiles of dys-regulated miRNAs in activated hepatic stellate cells, 10.1002/hep.25975
  114. Coll Mar, Taghdouini Adil El, Perea Luis, Mannaerts Inge, Vila-Casadesús Maria, Blaya Delia, Rodrigo-Torres Daniel, Affò Silvia, Morales-Ibanez Oriol, Graupera Isabel, Lozano Juan José, Najimi Mustapha, Sokal Etienne, Lambrecht Joeri, Ginès Pere, van Grunsven Leo A., Sancho-Bru Pau, Integrative miRNA and Gene Expression Profiling Analysis of Human Quiescent Hepatic Stellate Cells, 10.1038/srep11549
  115. Beermann Julia, Piccoli Maria-Teresa, Viereck Janika, Thum Thomas, Non-coding RNAs in Development and Disease: Background, Mechanisms, and Therapeutic Approaches, 10.1152/physrev.00041.2015
  116. Zhou Chan, York Samuel R., Chen Jennifer Y., Pondick Joshua V., Motola Daniel L., Chung Raymond T., Mullen Alan C., Long noncoding RNAs expressed in human hepatic stellate cells form networks with extracellular matrix proteins, 10.1186/s13073-016-0285-0
  117. Yu Fujun, Lu Zhongqiu, Cai Jing, Huang Kate, Chen Bicheng, Li Guojun, Dong Peihong, Zheng Jianjian, MALAT1 functions as a competing endogenous RNA to mediate Rac1 expression by sequestering miR-101b in liver fibrosis, 10.1080/15384101.2015.1120917
  118. Zheng Jianjian, Yu Fujun, Dong Peihong, Wu Limei, Zhang Yuan, Hu Yanwei, Zheng Lei, Long non-coding RNA PVT1 activates hepatic stellate cells through competitively binding microRNA-152, 10.18632/oncotarget.11709
  119. Liang Wei-Cheng, Fu Wei-Ming, Wong Cheuk-Wa, Wang Yan, Wang Wei-Mao, Hu Guo-Xin, Zhang Li, Xiao Li-Jia, Chi-Cheong Wan David, Zhang Jin-Fang, Miu-Yee Waye Mary, The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer, 10.18632/oncotarget.4154
  120. Yang Jing-Jing, Liu Li-Ping, Tao Hui, Hu Wei, Shi Peng, Deng Zi-Yu, Li Jun, MeCP2 silencing of LncRNA H19 controls hepatic stellate cell proliferation by targeting IGF1R, 10.1016/j.tox.2016.06.016
  121. Dimitrova Nadya, Zamudio Jesse R., Jong Robyn M., Soukup Dylan, Resnick Rebecca, Sarma Kavitha, Ward Amanda J., Raj Arjun, Lee Jeannie T., Sharp Phillip A., Jacks Tyler, LincRNA-p21 Activates p21 In cis to Promote Polycomb Target Gene Expression and to Enforce the G1/S Checkpoint, 10.1016/j.molcel.2014.04.025
  122. Zheng Jianjian, Dong Peihong, Mao Yuqing, Chen Shaolong, Wu Xiaoli, Li Guojun, Lu Zhongqiu, Yu Fujun, lincRNA-p21 inhibits hepatic stellate cell activation and liver fibrogenesis via p21, 10.1111/febs.13544
  123. Yu Fujun, Lu Zhongqiu, Chen Bicheng, Dong Peihong, Zheng Jianjian, Identification of a Novel lincRNA-p21-miR-181b-PTEN Signaling Cascade in Liver Fibrosis, 10.1155/2016/9856538
  124. He Yong, Wu Yu-ting, Huang Cheng, Meng Xiao-Ming, Ma Tao-tao, Wu Bao-Ming, Xu Feng-yun, Zhang Lei, Lv Xiong-Wen, Li Jun, Inhibitory effects of long noncoding RNA MEG3 on hepatic stellate cells activation and liver fibrogenesis, 10.1016/j.bbadis.2014.08.015
  125. Poelstra Klaas, Schuppan Detlef, Targeted therapy of liver fibrosis/cirrhosis and its complications, 10.1016/j.jhep.2011.04.008
  126. Zeisel A., Munoz-Manchado A. B., Codeluppi S., Lonnerberg P., La Manno G., Jureus A., Marques S., Munguba H., He L., Betsholtz C., Rolny C., Castelo-Branco G., Hjerling-Leffler J., Linnarsson S., Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq, 10.1126/science.aaa1934
  127. Davie Kristofer, Jacobs Jelle, Atkins Mardelle, Potier Delphine, Christiaens Valerie, Halder Georg, Aerts Stein, Discovery of Transcription Factors and Regulatory Regions Driving In Vivo Tumor Development by ATAC-seq and FAIRE-seq Open Chromatin Profiling, 10.1371/journal.pgen.1004994
Bibliographic reference El Taghdouini, Adil ; van Grunsven, Leo A.. Epigenetic regulation of hepatic stellate cell activation and liver fibrosis. In: Expert Review of Gastroenterology & Hepatology, Vol. 10, no.12, p. 1397-1408 (2016)
Permanent URL http://hdl.handle.net/2078.1/183063