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Citations to this article

Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma
Diego F. Calvisi, … , Valentina M. Factor, Snorri S. Thorgeirsson
Diego F. Calvisi, … , Valentina M. Factor, Snorri S. Thorgeirsson
Published September 4, 2007
Citation Information: J Clin Invest. 2007;117(9):2713-2722. https://doi.org/10.1172/JCI31457.
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Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma

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Abstract

Hepatocellular carcinoma (HCC) is the fifth most common cancer worldwide, accounting for an estimated 600,000 deaths annually. Aberrant methylation, consisting of DNA hypomethylation and/or promoter gene CpG hypermethylation, is implicated in the development of a variety of solid tumors, including HCC. We analyzed the global levels of DNA methylation as well as the methylation status of 105 putative tumor suppressor genes and found that the extent of genome-wide hypomethylation and CpG hypermethylation correlates with biological features and clinical outcome of HCC patients. We identified activation of Ras and downstream Ras effectors (ERK, AKT, and RAL) due to epigenetic silencing of inhibitors of the Ras pathway in all HCC. Further, selective inactivation of SPRY1 and -2, DAB2, and SOCS4 and -5 genes and inhibitors of angiogenesis (BNIP3, BNIP3L, IGFBP3, and EGLN2) was associated with poor prognosis. Importantly, several epigenetically silenced putative tumor suppressor genes found in HCC were also inactivated in the nontumorous liver. Our results assign both therapeutic and chemopreventive significance to methylation patterns in human HCC and open the possibility of using molecular targets, including those identified in this study, to effectively inhibit HCC development and progression.

Authors

Diego F. Calvisi, Sara Ladu, Alexis Gorden, Miriam Farina, Ju-Seog Lee, Elizabeth A. Conner, Insa Schroeder, Valentina M. Factor, Snorri S. Thorgeirsson

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M Tarocchi, S Polvani, G Marroncini, A Galli
World journal of gastroenterology : WJG 2014
Aberrant DNA methylation in hepatocellular carcinoma tumor suppression (Review)
Y Dong, A Wang
Oncology Letters 2014
SKP2 cooperates with N-Ras or AKT to induce liver tumor development in mice
Delogu S, Wang C, Cigliano A, Utpatel K, Sini M, Longerich T, Waldburger N, Breuhahn K, Jiang L, Ribback S, Dombrowski F, Evert M, Chen X, Calvisi DF
Oncotarget 2014
CLDN3 inhibits cancer aggressiveness via Wnt-EMT signaling and is a potential prognostic biomarker for hepatocellular carcinoma
Jiang L, Yang YD, Fu L, Xu W, Liu D, Liang Q, Zhang X, Xu L, Guan XY, Wu B, Sung JJ, Yu J
Oncotarget 2014
Mitochondrial Dysfunction in Cancer
ML Boland, AH Chourasia, KF Macleod
Frontiers in Oncology 2013
Salirasib sensitizes hepatocarcinoma cells to TRAIL-induced apoptosis through DR5 and survivin-dependent mechanisms
N Charette, CD Saeger, Y Horsmans, I Leclercq, P Stärkel
Cell Death and Disease 2013
An integrated analysis of SOCS1 down-regulation in HBV infection-related hepatocellular carcinoma
X Zhang, J Wang, J Cheng, S Ding, M Li, S Sun, L Zhang, S Liu, X Chen, H Zhuang, F Lu
Journal of Viral Hepatitis 2013
Sirtuin-6-dependent genetic and epigenetic alterations are associated with poor clinical outcome in hepatocellular carcinoma patients
JU Marquardt, K Fischer, K Baus, A Kashyap, S Ma, M Krupp, M Linke, A Teufel, U Zechner, D Strand, SS Thorgeirsson, PR Galle, S Strand
Hepatology 2013
Linking metabolism and epigenetic regulation in development of hepatocellular carcinoma
WM Puszyk, TL Trinh, SJ Chapple, C Liu
Laboratory Investigation 2013
Hypomethylation of long interspersed nuclear element-1 promoter is associated with poor outcomes for curative resected hepatocellular carcinoma
X Gao, J Qu, X Chang, Y Lu, W Bai, H Wang, Z Xu, L An, C Wang, Z Zeng, Y Yang
Liver International 2013
Towards incorporating epigenetic mechanisms into carcinogen identification and evaluation
Z Herceg, MP Lambert, K Veldhoven, C Demetriou, P Vineis, MT Smith, K Straif, CP Wild
Carcinogenesis 2013
miR-93-directed downregulation of DAB2 defines a novel oncogenic pathway in lung cancer
L Du, Z Zhao, X Ma, TH Hsiao, Y Chen, E Young, M Suraokar, I Wistuba, JD Minna, A Pertsemlidis
Oncogene 2013
Genome-Wide Methylation Analysis and Epigenetic Unmasking Identify Tumor Suppressor Genes in Hepatocellular Carcinoma
K Revill, T Wang, A Lachenmayer, K Kojima, A Harrington, J Li, Y Hoshida, JM Llovet, S Powers
Gastroenterology 2013
DNA methylation and apoptosis resistance in cancer cells
E Hervouet, M Cheray, FM Vallette, PF Cartron
Cells 2013
Unique association between global DNA hypomethylation and chromosomal alterations in human hepatocellular carcinoma
N Nishida, M Kudo, T Nishimura, T Arizumi, M Takita, S Kitai, N Yada, S Hagiwara, T Inoue, Y Minami, K Ueshima, T Sakurai, N Yokomichi, T Nagasaka, A Goel
PloS one 2013
Suppressor of Cytokine Signaling (SOCS) 5 utilises distinct domains for regulation of JAK1 and interaction with the adaptor protein Shc-1
EM Linossi, IR Chandrashekaran, TB Kolesnik, JM Murphy, AI Webb, TA Willson, L Kedzierski, AN Bullock, JJ Babon, RS Norton, NA Nicola, SE Nicholson
PloS one 2013
Hepatitis B virus X protein-induced aberrant epigenetic modifications contributing to human hepatocellular carcinoma pathogenesis
Y Tian, W Yang, J Song, Y Wu, B Ni
Molecular and cellular biology 2013
DNA methyltransferase inhibitor zebularine inhibits human hepatic carcinoma cells proliferation and induces apoptosis
K Nakamura, K Aizawa, K Nakabayashi, N Kato, J Yamauchi, K Hata, A Tanoue
PloS one 2013
The AKT Inhibitor MK-2206 is Cytotoxic in Hepatocarcinoma Cells Displaying Hyperphosphorylated AKT-1 and Synergizes with Conventional Chemotherapy
Simioni C, Martelli AM, Cani A, Cetin-Atalay R, McCubrey JA, Capitani S, Neri LM
Oncotarget 2013
MicroRNAs Regulate Methionine Adenosyltransferase 1A Expression and Tumorigenicity in Hepatocellular Carcinoma
Heping Yang, Michele E. Cho, Tony W.H. Li, Hui Peng, Kwang Suk Ko, José Maria Mato, Shelly Lu
Journal of Clinical Investigation 2012
Mutant HrasG12V and KrasG12D have overlapping, but non-identical effects on hepatocyte growth and transformation frequency in transgenic mice
ML Figueiredo, TJ Stein, A Jochem, EP Sandgren
Liver International 2012
Role of epigenetic aberrations in the development and progression of human hepatocellular carcinoma
IP Pogribny, I Rusyn
Cancer Letters 2012
Pathogenetic and Prognostic Significance of Inactivation of RASSF Proteins in Human Hepatocellular Carcinoma
DF Calvisi, M Evert, F Dombrowski
Molecular Biology International 2012
Genome-wide DNA methylation profiles in hepatocellular carcinoma
J Shen, S Wang, YJ Zhang, M Kappil, HC Wu, MG Kibriya, Q Wang, F Jasmine, H Ahsan, PH Lee, MW Yu, CJ Chen, RM Santella
Hepatology 2012
Translational medicine in hepatocellular carcinoma
Q Gao, Y Shi, X Wang, J Zhou, S Qiu, J Fan
Frontiers of Medicine 2012
IGFBP3 impedes aggressive growth of pediatric liver cancer and is epigenetically silenced in vascular invasive and metastatic tumors
I Regel, M Eichenmüller, S Joppien, J Liebl, B Häberle, J Müller-Höcker, A Vollmar, D Schweinitz, R Kappler
Molecular Cancer 2012
Global hypomethylation in hepatocellular carcinoma and its relationship to aflatoxin B1 exposure
YJ Zhang, HC Wu, H Yazici, MW Yu, PH Lee, RM Santella
World journal of hepatology 2012
Pharmacological Unmasking Microarray Approach-Based Discovery of Novel DNA Methylation Markers for Hepatocellular Carcinoma
N Jung, JK Won, BH Kim, KS Suh, JJ Jang, GH Kang
Journal of Korean Medical Science 2012
Evaluation of epigenetic modulation of cyclooxygenase-2 as a prognostic marker for hepatocellular carcinoma
A Fernández-Alvarez, C Llorente-Izquierdo, R Mayoral, N Agra, L Boscá, M Casado, P Martín-Sanz
Oncogenesis 2012
Detection of cancer-specific epigenomic changes in biofluids: Powerful tools in biomarker discovery and application
AN da Costa, Z Herceg
Molecular Oncology 2012
Mutations and deregulation of Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascades which alter therapy response.
McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Montalto G, Cervello M, Nicoletti F, Fagone P, Malaponte G, Mazzarino MC, Candido S, Libra M, Bäsecke J, Mijatovic S, Maksimovic-Ivanic D, Milella M, Tafuri A, Cocco L, Evangelisti C, Chiarini F, Martelli AM
Oncotarget 2012
Targeted therapy for hepatocellular carcinoma: novel agents on the horizon.
Cervello M, McCubrey JA, Cusimano A, Lampiasi N, Azzolina A, Montalto G
Oncotarget 2012
Inactivation of Ras GTPase-activating proteins promotes unrestrained activity of wild-type Ras in human liver cancer
DF Calvisi, S Ladu, EA Conner, D Seo, JT Hsieh, VM Factor, SS Thorgeirsson
Journal of Hepatology 2011
Mechanisms and Biology of B-Cell Leukemia/Lymphoma 2/Adenovirus E1B Interacting Protein 3 and Nip-Like Protein X
J Zhang, PA Ney
Antioxidants & Redox Signaling 2011
Aberrant methylation of Polo-like kinase CpG islands in Plk4 heterozygous mice
A Ward, A Morettin, D Shum, JW Hudson
BMC Cancer 2011
Oxidative stress and ERK1/2 phosphorylation as predictors of outcome in hepatocellular carcinoma patients treated with sorafenib plus octreotide LAR
M Caraglia, G Giuberti, M Marra, R Addeo, L Montella, M Murolo, P Sperlongano, B Vincenzi, S Naviglio, SD Prete, A Abbruzzese, P Stiuso
Cell Death and Disease 2011
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
M Greco, A Chiappetta, L Bruno, MB Bitonti
Journal of Experimental Botany 2011
SOCS5 and SOCS6 have similar expression patterns in normal and cancer tissues
S Yoon, YS Yi, SS Kim, JH Kim, WS Park, SW Nam
Tumor Biology 2011
Epigenetics: Principles and Practice
JP Hamilton
Digestive diseases (Basel, Switzerland) 2011
Effect of Benzothiazole based conjugates in causing apoptosis by Regulating p53, PTEN and MAP Kinase proteins affecting miR-195a and miR-101-1
S Pushpavalli, MJ Ramaiah, C Srinivas, D Mukhopadhya, J Aditya, RM Kumbhare, U Bhadra, MP Bhadra
Cancer Cell International 2011
AKT and N-Ras co-activation in the mouse liver promotes rapid carcinogenesis via mTORC1, FOXM1/SKP2, and c-Myc pathways
C Ho, C Wang, S Mattu, G Destefanis, S Ladu, S Delogu, J Armbruster, L Fan, SA Lee, L Jiang, F Dombrowski, M Evert, X Chen, DF Calvisi
Hepatology 2011
Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR pathways in controlling growth and sensitivity to therapy-implications for cancer and aging
Steelman LS, Chappell WH, Abrams SL, Kempf CR, Long J, Laidler P, Mijatovic S, Maksimovic-Ivanic D, Stivala F, Mazzarino MC, Donia M, Fagone P, Malaponte G, Nicoletti F, Libra M, Milella M, Tafuri A, Bonati A, Bäsecke J, Cocco L, Evangelisti C, Martelli AM, Montalto G, Cervello M, McCubrey JA
Aging 2011
Hypomethylation of the hsa-miR-191 Locus Causes High Expression of hsa-miR-191 and Promotes the Epithelial-to-Mesenchymal Transition in Hepatocellular Carcinoma
He Y, Cui Y, Wang W, Gu J, Guo S, Ma K, Luo X
Neoplasia (New York, N.Y.) 2011
Epigenetic downregulation of human Disabled-2 switches TGF-beta from a tumor suppressor to a tumor promoter
Adele Hannigan, Paul Smith, Gabriela Klana, Christiana Lo Nigro, Clare Orange, Darren O'Brien, Reshma Shah, Nelofer Syed, Lindsay Spender, Blanca Herrera, Johanna Thurlow, Laura Lattanzio, Martino Monteverde, Meghan Maurer, Francesca Buffa, Jelena Mann, David Chu, Catherine West, Maxine Partridge, Karin Oien, Jonathan Cooper, Margaret Frame, Adrian Harris, Louise Hiller, Linda Nicholson, Milena Gasco, Tim Crook, Gareth Inman
Journal of Clinical Investigation 2010
Molecular classification and novel targets in hepatocellular carcinoma: recent advancements
Y Hoshida, S Toffanin, A Lachenmayer, A Villanueva, B Minguez, JM Llovet
Seminars in liver disease 2010
High-throughput assessment of CpG site methylation for distinguishing between HCV-cirrhosis and HCV-associated hepatocellular carcinoma
KJ Archer, VR Mas, DG Maluf, RA Fisher
Molecular Genetics and Genomics 2010
Epigenetic mechanisms involved in the pathogenesis of hepatobiliary malignancies
JP Hamilton
Epigenomics 2010
An Integrated Genomic and Epigenomic Approach Predicts Therapeutic Response to Zebularine in Human Liver Cancer
JB Andersen, VM Factor, JU Marquardt, C Raggi, YH Lee, D Seo, EA Conner, SS Thorgeirsson
Science Translational Medicine 2010
Identification of Novel Methylation Markers in Hepatocellular Carcinoma using a Methylation Array
SH Shin, B Kim, JJ Jang, KS Suh, GH Kang
Journal of Korean Medical Science 2010
Epigenetic regulation of cancer stem cell marker CD133 by transforming growth factor-β
H You, W Ding, CB Rountree
Hepatology 2010
Salirasib inhibits the growth of hepatocarcinoma cell lines in vitro and tumor growth in vivo through ras and mTOR inhibition
N Charette, CD Saeger, V Lannoy, Y Horsmans, I Leclercq, P Stärkel
Molecular Cancer 2010
Hepatocellular carcinoma displays distinct DNA methylation signatures with potential as clinical predictors
H Hernandez-Vargas, MP Lambert, FL Calvez-Kelm, G Gouysse, S McKay-Chopin, SV Tavtigian, JY Scoazec, Z Herceg
PloS one 2010
Methylation of Dickkopf-3 as a prognostic factor in cirrhosis-related hepatocellular carcinoma
B Yang, Z Du, YT Gao, C Lou, SG Zhang, T Bai, YJ Wang, WQ Song
World journal of gastroenterology : WJG 2010
NEW STRATEGIES IN HEPATOCELLULAR CARCINOMA: GENOMIC PROGNOSTIC MARKERS
A Villanueva, Y Hoshida, S Toffanin, A Lachenmayer, C Alsinet, R Savic, H Cornella, JM Llovet
Clinical cancer research 2010
Comparative analysis of promoter methylation and gene expression endpoints between tumorous and non-tumorous tissues from HCV-positive patients with hepatocellular carcinoma
EJ Formeister, M Tsuchiya, H Fujii, S Shpyleva, IP Pogribny, I Rusyn
Mutation research 2010
An Overview of Biomarkers and Molecular Signatures in HCC
SH Yim, YJ Chung
Cancers 2010
Identifying genes progressively silenced in preneoplastic and neoplastic liver tissues
KJ Archer, Z Zhao, T Guennel, DG Maluf, RA Fisher, VR Mas
International Journal of Computational Biology and Drug Design 2010
Epigenetic regulation of cancer stem cells in liver cancer: current concepts and clinical implications
JU Marquardt, VM Factor, SS Thorgeirsson
Journal of Hepatology 2010
Nix Nought Nothing: Fairy Tale or Real Deal
GW Dorn
Journal of Molecular and Cellular Cardiology 2010
Array-based profiling of the differential methylation status of CpG islands in hepatocellular carcinoma cell lines
BB Liu, D Zheng, YK Liu, XN Kang, LU SUN, K Guo, RX Sun, J Chen, Y Zhao
Oncology Letters 2010
S-adenosylmethionine inhibits the growth of cancer cells by reversing the hypomethylation status of c-myc and H-ras in human gastric cancer and colon cancer.
Luo J, Li YN, Wang F, Zhang WM, Geng X
International journal of biological sciences 2010
Identification of genes preferentially methylated in hepatitis C virus‐related hepatocellular carcinoma
Deng Y, Nagae G, Midorikawa Y, Yagi K, Tsutsumi S, Yamamoto S, Hasegawa K, Kokudo N, Aburatani H, Kaneda A
Cancer Science 2010
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009
Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis
B Pyrzynska, I Pilecka, M Miaczynska
Molecular Oncology 2009
Dysregulation of apoptosis in hepatocellular carcinoma cells
I Fabregat
World journal of gastroenterology : WJG 2009
Changes in the expression of methionine adenosyltransferase genes and S-adenosylmethionine homeostasis during hepatic stellate cell activation
K Ramani, H Yang, J Kuhlenkamp, L Tomasi, H Tsukamoto, JM Mato, SC Lu
Hepatology 2009
Ras pathway activation in hepatocellular carcinoma and anti-tumoral effect of combined sorafenib and rapamycin in vivo
P Newell, S Toffanin, A Villanueva, DY Chiang, B Minguez, L Cabellos, R Savic, Y Hoshida, KH Lim, P Melgar-Lesmes, S Yea, J Peix, K Deniz, MI Fiel, S Thung, C Alsinet, V Tovar, V Mazzaferro, J Bruix, S Roayaie, M Schwartz, SL Friedman, JM Llovet
Journal of Hepatology 2009
Hepatocellular Carcinoma: Tumorigenesis and Prediction Markers
C Braicu
Gastroenterology Research 2009
NORE1A Tumor Suppressor Candidate Modulates p21 CIP1 via p53
DF Calvisi, H Donninger, MD Vos, MJ Birrer, L Gordon, V Leaner, GJ Clark
Cancer research 2009
SOCS regulation of the JAK/STAT signalling pathway
BA Croker, H Kiu, SE Nicholson
Seminars in Cell & Developmental Biology 2008
Liver insulin-like growth factor 2 methylation in hepatitis C virus cirrhosis and further occurrence of hepatocellular carcinoma
P Couvert, A Carrié, J Pariès, J Vaysse, A Miroglio, A Kerjean, P Nahon, J Chelly, JC Trinchet, M Beaugrand, N Ganne-Carrié
World journal of gastroenterology : WJG 2008
BNIP3 subfamily BH3-only proteins: mitochondrial stress sensors in normal and pathological functions
G Chinnadurai, S Vijayalingam, SB Gibson
Oncogene 2008
Gene expression and hepatitis C virus infection
T Asselah, I Bièche, A Sabbagh, P Bedossa, R Moreau, D Valla, M Vidaud, P Marcellin
Gut 2008
Mechanisms of peroxisome proliferator-induced DNA hypomethylation in rat liver
IP Pogribny, VP Tryndyak, A Boureiko, S Melnyk, TV Bagnyukova, B Montgomery, I Rusyn
Mutation research 2008
Focal Gains of VEGFA and Molecular Classification of Hepatocellular Carcinoma
DY Chiang, A Villanueva, Y Hoshida, J Peix, P Newell, B Minguez, AC LeBlanc, DJ Donovan, SN Thung, M Solé, V Tovar, C Alsinet, AH Ramos, J Barretina, S Roayaie, M Schwartz, S Waxman, J Bruix, V Mazzaferro, AH Ligon, V Najfeld, SL Friedman, WR Sellers, M Meyerson, JM Llovet
Cancer research 2008
Evolving therapies in the treatment of hepatocellular carcinoma
Spangenberg HC, Thimme R, Blum HE
Biologics : targets & therapy 2008
Homozygous Deletions and Recurrent Amplifications Implicate New Genes Involved in Prostate Cancer
Liu W, Xie CC, Zhu Y, Li T, Sun J, Cheng Y, Ewing CM, Dalrymple S, Turner AR, Sun J, Isaacs JT, Chang BL, Zheng SL, Isaacs WB, Xu J
Neoplasia (New York, N.Y.) 2008

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