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Title: Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets

Abstract

Our genomic analyses promise to improve tumor characterization to optimize personalized treatment for patients with hepatocellular carcinoma (HCC). Exome sequencing analysis of 243 liver tumors identified mutational signatures associated with specific risk factors, mainly combined alcohol and tobacco consumption and exposure to aflatoxin B1. We identified 161 putative driver genes associated with 11 recurrently altered pathways. Associations of mutations defined 3 groups of genes related to risk factors and centered on CTNNB1 (alcohol), TP53 (hepatitis B virus, HBV) and AXIN1. These analyses according to tumor stage progression identified TERT promoter mutation as an early event, whereasFGF3, FGF4, FGF19 or CCND1 amplification and TP53 and CDKN2A alterations appeared at more advanced stages in aggressive tumors. In 28% of the tumors, we identified genetic alterations potentially targetable by US Food and Drug Administration (FDA)–approved drugs. Finally, we identified risk factor–specific mutational signatures and defined the extensive landscape of altered genes and pathways in HCC, which will be useful to design clinical trials for targeted therapy.

Authors:
 [1];  [1];  [1];  [2];  [3];  [1];  [1];  [1];  [1];  [1];  [1];  [4];  [1];  [5];  [6];  [7];  [8];  [1];  [9];  [10] more »;  [7];  [11];  [12];  [3] « less
  1. INSERM, Paris (France); Paris Descartes Univ., (France); Paris 13 Univ. (France); Paris Diderot Univ. (France)
  2. Wellcome Trust Sanger Inst., Hinxton (United Kingdom); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. INSERM, Paris (France); Paris Descartes Univ., (France); Paris 13 Univ. (France); Paris Diderot Univ. (France); Public Assistance Hospital of Paris (France)
  4. Hepatocellular Carcinoma Translational Research Laboratory, Barcelona (Spain)
  5. INSERM, Bordeaux (France)
  6. Public Assistance Hospital of Paris (France); INSERM, Creteil (France)
  7. INSERM, Bordeaux (France); Bordeaux Univ. Hospital (France)
  8. Fondazione Inst., Milan (Italy)
  9. Hepatocellular Carcinoma Translational Research Laboratory, Barcelona (Spain); Mount Sinai School of Medicine, New York, NY (United States)
  10. INSERM, Paris (France); Paris Descartes Univ., (France); Paris 13 Univ. (France); Paris Diderot Univ. (France); Univ. Hospital of Paris (France)
  11. Wellcome Trust Sanger Inst., Hinxton (United Kingdom)
  12. Hepatocellular Carcinoma Translational Research Laboratory, Barcelona (Spain); Mount Sinai School of Medicine, New York, NY (United States); Catalan Inst. for Research Studies, Barcelona (Spain)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1235730
Report Number(s):
LA-UR-14-28199
Journal ID: ISSN 1061-4036; ng.3252
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Nature Genetics
Additional Journal Information:
Journal Volume: 47; Journal Issue: 5; Journal ID: ISSN 1061-4036
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; DNA sequencing; liver cancer

Citation Formats

Schulze, Kornelius, Imbeaud, Sandrine, Letouzé, Eric, Alexandrov, Ludmil B., Calderaro, Julien, Rebouissou, Sandra, Couchy, Gabrielle, Meiller, Clément, Shinde, Jayendra, Soysouvanh, Frederic, Calatayud, Anna-Line, Pinyol, Roser, Pelletier, Laura, Balabaud, Charles, Laurent, Alexis, Blanc, Jean-Frederic, Mazzaferro, Vincenzo, Calvo, Fabien, Villanueva, Augusto, Nault, Jean-Charles, Bioulac-Sage, Paulette, Stratton, Michael R., Llovet, Josep M., and Zucman-Rossi, Jessica. Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets. United States: N. p., 2015. Web. doi:10.1038/ng.3252.
Schulze, Kornelius, Imbeaud, Sandrine, Letouzé, Eric, Alexandrov, Ludmil B., Calderaro, Julien, Rebouissou, Sandra, Couchy, Gabrielle, Meiller, Clément, Shinde, Jayendra, Soysouvanh, Frederic, Calatayud, Anna-Line, Pinyol, Roser, Pelletier, Laura, Balabaud, Charles, Laurent, Alexis, Blanc, Jean-Frederic, Mazzaferro, Vincenzo, Calvo, Fabien, Villanueva, Augusto, Nault, Jean-Charles, Bioulac-Sage, Paulette, Stratton, Michael R., Llovet, Josep M., & Zucman-Rossi, Jessica. Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets. United States. https://doi.org/10.1038/ng.3252
Schulze, Kornelius, Imbeaud, Sandrine, Letouzé, Eric, Alexandrov, Ludmil B., Calderaro, Julien, Rebouissou, Sandra, Couchy, Gabrielle, Meiller, Clément, Shinde, Jayendra, Soysouvanh, Frederic, Calatayud, Anna-Line, Pinyol, Roser, Pelletier, Laura, Balabaud, Charles, Laurent, Alexis, Blanc, Jean-Frederic, Mazzaferro, Vincenzo, Calvo, Fabien, Villanueva, Augusto, Nault, Jean-Charles, Bioulac-Sage, Paulette, Stratton, Michael R., Llovet, Josep M., and Zucman-Rossi, Jessica. Mon . "Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets". United States. https://doi.org/10.1038/ng.3252. https://www.osti.gov/servlets/purl/1235730.
@article{osti_1235730,
title = {Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets},
author = {Schulze, Kornelius and Imbeaud, Sandrine and Letouzé, Eric and Alexandrov, Ludmil B. and Calderaro, Julien and Rebouissou, Sandra and Couchy, Gabrielle and Meiller, Clément and Shinde, Jayendra and Soysouvanh, Frederic and Calatayud, Anna-Line and Pinyol, Roser and Pelletier, Laura and Balabaud, Charles and Laurent, Alexis and Blanc, Jean-Frederic and Mazzaferro, Vincenzo and Calvo, Fabien and Villanueva, Augusto and Nault, Jean-Charles and Bioulac-Sage, Paulette and Stratton, Michael R. and Llovet, Josep M. and Zucman-Rossi, Jessica},
abstractNote = {Our genomic analyses promise to improve tumor characterization to optimize personalized treatment for patients with hepatocellular carcinoma (HCC). Exome sequencing analysis of 243 liver tumors identified mutational signatures associated with specific risk factors, mainly combined alcohol and tobacco consumption and exposure to aflatoxin B1. We identified 161 putative driver genes associated with 11 recurrently altered pathways. Associations of mutations defined 3 groups of genes related to risk factors and centered on CTNNB1 (alcohol), TP53 (hepatitis B virus, HBV) and AXIN1. These analyses according to tumor stage progression identified TERT promoter mutation as an early event, whereasFGF3, FGF4, FGF19 or CCND1 amplification and TP53 and CDKN2A alterations appeared at more advanced stages in aggressive tumors. In 28% of the tumors, we identified genetic alterations potentially targetable by US Food and Drug Administration (FDA)–approved drugs. Finally, we identified risk factor–specific mutational signatures and defined the extensive landscape of altered genes and pathways in HCC, which will be useful to design clinical trials for targeted therapy.},
doi = {10.1038/ng.3252},
journal = {Nature Genetics},
number = 5,
volume = 47,
place = {United States},
year = {Mon Mar 30 00:00:00 EDT 2015},
month = {Mon Mar 30 00:00:00 EDT 2015}
}

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Identification of the Consistently Altered Metabolic Targets in Human Hepatocellular Carcinoma
journal, September 2017

  • Nwosu, Zeribe Chike; Megger, Dominik Andre; Hammad, Seddik
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 4, Issue 2
  • DOI: 10.1016/j.jcmgh.2017.05.004

There Is Something Fishy About Liver Cancer: Zebrafish Models of Hepatocellular Carcinoma
journal, January 2019

  • Wrighton, Paul J.; Oderberg, Isaac M.; Goessling, Wolfram
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 8, Issue 3
  • DOI: 10.1016/j.jcmgh.2019.05.002

Toward a Better Understanding of Hepatocellular Carcinoma Immune Infiltrates
journal, January 2020

  • Buettner, Nico; Thimme, Robert
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 9, Issue 2
  • DOI: 10.1016/j.jcmgh.2019.11.007

Neutrophils: driving progression and poor prognosis in hepatocellular carcinoma?
journal, November 2017

  • Margetts, Jane; Ogle, Laura F.; Chan, Stephen L.
  • British Journal of Cancer, Vol. 118, Issue 2
  • DOI: 10.1038/bjc.2017.386

p62/Sqstm1 promotes malignancy of HCV-positive hepatocellular carcinoma through Nrf2-dependent metabolic reprogramming
journal, June 2016

  • Saito, Tetsuya; Ichimura, Yoshinobu; Taguchi, Keiko
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12030

Recurrently deregulated lncRNAs in hepatocellular carcinoma
journal, February 2017

  • Yang, Yang; Chen, Lei; Gu, Jin
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14421

The spatial organization of intra-tumour heterogeneity and evolutionary trajectories of metastases in hepatocellular carcinoma
journal, February 2017

  • Zhai, Weiwei; Lim, Tony Kiat-Hon; Zhang, Tong
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14565

Human primary liver cancer–derived organoid cultures for disease modeling and drug screening
journal, November 2017

  • Broutier, Laura; Mastrogiovanni, Gianmarco; Verstegen, Monique MA
  • Nature Medicine, Vol. 23, Issue 12
  • DOI: 10.1038/nm.4438

Base changes in tumour DNA have the power to reveal the causes and evolution of cancer
journal, June 2016

  • Hollstein, M.; Alexandrov, L. B.; Wild, C. P.
  • Oncogene, Vol. 36, Issue 2
  • DOI: 10.1038/onc.2016.192

The PI3K inhibitor copanlisib synergizes with sorafenib to induce cell death in hepatocellular carcinoma
journal, April 2019


APOBEC3A is an oral cancer prognostic biomarker in Taiwanese carriers of an APOBEC deletion polymorphism
journal, September 2017


miR-122 removal in the liver activates imprinted microRNAs and enables more effective microRNA-mediated gene repression
journal, December 2018


Author Correction: The effects of mutational processes and selection on driver mutations across cancer types
journal, April 2020


DEPDC5 deficiency contributes to resistance to leucine starvation via p62 accumulation in hepatocellular carcinoma
journal, January 2018


The critical role of glucose deprivation in epithelial-mesenchymal transition in hepatocellular carcinoma under hypoxia
journal, January 2020


Hepatocellular carcinoma cell lines retain the genomic and transcriptomic landscapes of primary human cancers
journal, June 2016

  • Qiu, Zhixin; Zou, Keke; Zhuang, Liping
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep27411

Early detection of the aflatoxin B1 mutational fingerprint: A diagnostic tool for liver cancer
journal, May 2017

  • Fedeles, Bogdan I.; Chawanthayatham, Supawadee; Croy, Robert G.
  • Molecular & Cellular Oncology, Vol. 4, Issue 4
  • DOI: 10.1080/23723556.2017.1329693

Exploring background mutational processes to decipher cancer genetic heterogeneity
journal, May 2017

  • Goncearenco, Alexander; Rager, Stephanie L.; Li, Minghui
  • Nucleic Acids Research, Vol. 45, Issue W1
  • DOI: 10.1093/nar/gkx367

Spatial and temporal expansion of intrahepatic metastasis by molecularly‐defined clonality in multiple liver cancers
journal, January 2020

  • Yamamoto, Shogo; Midorikawa, Yutaka; Nagae, Genta
  • Cancer Science, Vol. 111, Issue 2
  • DOI: 10.1111/cas.14282

Polyploidy spectrum: a new marker in HCC classification
journal, April 2019


Multi-OMICs and Genome Editing Perspectives on Liver Cancer Signaling Networks
journal, January 2016

  • Lin, Shengda; Yin, Yi A.; Jiang, Xiaoqian
  • BioMed Research International, Vol. 2016
  • DOI: 10.1155/2016/6186281

New Insights into the Epigenetics of Hepatocellular Carcinoma
journal, January 2017

  • Wahid, Braira; Ali, Amjad; Rafique, Shazia
  • BioMed Research International, Vol. 2017
  • DOI: 10.1155/2017/1609575

Epigenetic versus Genetic Deregulation of the KEAP1/NRF2 Axis in Solid Tumors: Focus on Methylation and Noncoding RNAs
journal, January 2018

  • Fabrizio, F. P.; Sparaneo, A.; Trombetta, D.
  • Oxidative Medicine and Cellular Longevity, Vol. 2018
  • DOI: 10.1155/2018/2492063

The biology of Hepatocellular carcinoma: implications for genomic and immune therapies
journal, August 2017


Correction to: Liver cancer cell lines distinctly mimic the metabolic gene expression pattern of the corresponding human tumours
journal, November 2018

  • Nwosu, Zeribe C.; Battello, Nadia; Rothley, Melanie
  • Journal of Experimental & Clinical Cancer Research, Vol. 37, Issue 1
  • DOI: 10.1186/s13046-018-0939-4

SIRT7 regulates hepatocellular carcinoma response to therapy by altering the p53-dependent cell death pathway
journal, June 2019

  • Zhao, Jie; Wozniak, Ann; Adams, Abby
  • Journal of Experimental & Clinical Cancer Research, Vol. 38, Issue 1
  • DOI: 10.1186/s13046-019-1246-4

Molecular profiling for precision cancer therapies
journal, January 2020


Circulating tumor DNA in hepatocellular carcinoma: trends and challenges
journal, May 2016


A precision therapeutic strategy for hexokinase 1-null, hexokinase 2-positive cancers
journal, June 2018


Epigenomic annotation of noncoding mutations identifies mutated pathways in primary liver cancer
journal, March 2017


aCNViewer: Comprehensive genome-wide visualization of absolute copy number and copy neutral variations
journal, December 2017


Mice lacking RAP1 show early onset and higher rates of DEN-induced hepatocellular carcinomas in female mice
journal, October 2018


DKK1 promotes hepatocellular carcinoma inflammation, migration and invasion: Implication of TGF-β1
journal, September 2019


Chromatin remodeling gene ARID2 targets cyclin D1 and cyclin E1 to suppress hepatoma cell progression
journal, June 2016


Mutations acquired by hepatocellular carcinoma recurrence give rise to an aggressive phenotype
journal, December 2016


Silencing of karyopherin α2 inhibits cell growth and survival in human hepatocellular carcinoma
journal, March 2017


Precision medicine for hepatocellular carcinoma: driver mutations and targeted therapy
journal, June 2017


The ubiquitous ‘cancer mutational signature’ 5 occurs specifically in cancers with deleted FHIT alleles
journal, November 2017


Molecular alterations in hepatocellular carcinoma associated with hepatitis B and hepatitis C infections
journal, March 2016


Cancer Metabolism as a Mechanism of Treatment Resistance and Potential Therapeutic Target in Hepatocellular Carcinoma
journal, January 2018


Roles of FGFs As Paracrine or Endocrine Signals in Liver Development, Health, and Disease
journal, April 2016

  • Itoh, Nobuyuki; Nakayama, Yoshiaki; Konishi, Morichika
  • Frontiers in Cell and Developmental Biology, Vol. 4
  • DOI: 10.3389/fcell.2016.00030

Host and Viral Genetic Variation in HBV-Related Hepatocellular Carcinoma
journal, July 2018


Circulating Cell-Free DNA in Hepatocellular Carcinoma: Current Insights and Outlook
journal, March 2018

  • Ng, Charlotte K. Y.; Di Costanzo, Giovan Giuseppe; Terracciano, Luigi M.
  • Frontiers in Medicine, Vol. 5
  • DOI: 10.3389/fmed.2018.00078

The KEAP1–NRF2 System in Cancer
journal, May 2017


MTHFD1L-Mediated Redox Homeostasis Promotes Tumor Progression in Tongue Squamous Cell Carcinoma
journal, December 2019


A Guide to PIN1 Function and Mutations Across Cancers
journal, January 2019

  • El Boustani, Maguie; De Stefano, Lucia; Caligiuri, Isabella
  • Frontiers in Pharmacology, Vol. 9
  • DOI: 10.3389/fphar.2018.01477

Lipid Metabolic Reprogramming in Hepatocellular Carcinoma
journal, November 2018


Dysregulation of Nrf2 in Hepatocellular Carcinoma: Role in Cancer Progression and Chemoresistance
journal, December 2018


Animal Models of Hepatocellular Carcinoma: The Role of Immune System and Tumor Microenvironment
journal, October 2019


Genomic Perspective on Mouse Liver Cancer Models
journal, October 2019


Chaperone-Mediated Autophagy in the Liver: Good or Bad?
journal, October 2019


A Surgical Perspective on Targeted Therapy of Hepatocellular Carcinoma
journal, September 2015


Systemic Chemotherapy for Advanced Hepatocellular Carcinoma: Past, Present, and Future
journal, December 2015


Hepatitis B Virus-Associated Hepatocellular Carcinoma and Hepatic Cancer Stem Cells
journal, March 2018


EZH2 in Cancer Progression and Potential Application in Cancer Therapy: A Friend or Foe?
journal, May 2017

  • Yan, Ke-Sin; Lin, Chia-Yuan; Liao, Tan-Wei
  • International Journal of Molecular Sciences, Vol. 18, Issue 6
  • DOI: 10.3390/ijms18061172

A Comprehensive Analysis of Argonaute-CLIP Data Identifies Novel, Conserved and Species-Specific Targets of miR-21 in Human Liver and Hepatocellular Carcinoma
journal, March 2018

  • Koenig, Aaron; Barajas, Juan; Guerrero, María
  • International Journal of Molecular Sciences, Vol. 19, Issue 3
  • DOI: 10.3390/ijms19030851

Methylation Density Pattern of KEAP1 Gene in Lung Cancer Cell Lines Detected by Quantitative Methylation Specific PCR and Pyrosequencing
journal, May 2019

  • Fabrizio, Federico; Sparaneo, Angelo; Centra, Flavia
  • International Journal of Molecular Sciences, Vol. 20, Issue 11
  • DOI: 10.3390/ijms20112697

Tumor-Stroma Crosstalk Enhances REG3A Expressions that Drive the Progression of Hepatocellular Carcinoma
journal, January 2020

  • Cho, Yuri; Park, Min Ji; Kim, Koeun
  • International Journal of Molecular Sciences, Vol. 21, Issue 2
  • DOI: 10.3390/ijms21020472

Molecular Targets in Hepatocarcinogenesis and Implications for Therapy
journal, August 2018

  • Wu, Meng-Yu; Yiang, Giuo-Teng; Cheng, Pei-Wen
  • Journal of Clinical Medicine, Vol. 7, Issue 8
  • DOI: 10.3390/jcm7080213

Positive Immuno-Modulation Following Radiofrequency Assisted Liver Resection in Hepatocellular Carcinoma
journal, March 2019

  • Huang, Kai Wen; Jayant, Kumar; Lee, Po-Huang
  • Journal of Clinical Medicine, Vol. 8, Issue 3
  • DOI: 10.3390/jcm8030385

Genetic alterations in hepatocellular carcinoma: An update
journal, January 2016

  • Niu, Zhao-Shan; Niu, Xiao-Jun; Wang, Wen-Hong
  • World Journal of Gastroenterology, Vol. 22, Issue 41
  • DOI: 10.3748/wjg.v22.i41.9069

Dimensions of hepatocellular carcinoma phenotypic diversity
journal, October 2018

  • Désert, Romain; Nieto, Natalia; Musso, Orlando
  • World Journal of Gastroenterology, Vol. 24, Issue 40
  • DOI: 10.3748/wjg.v24.i40.4536

Role of liver biopsy in hepatocellular carcinoma
journal, October 2019

  • Tommaso, Luca Di; Spadaccini, Marco; Donadon, Matteo
  • World Journal of Gastroenterology, Vol. 25, Issue 40
  • DOI: 10.3748/wjg.v25.i40.6041

Clinical significance of microRNA-449a in hepatocellular carcinoma with microarray data mining together with initial bioinformatics analysis
journal, February 2018

  • Yang, Xia; Wang, Han‑Lin; Liang, Hai‑Wei
  • Experimental and Therapeutic Medicine
  • DOI: 10.3892/etm.2018.5836

Aberrantly DNA Methylated-Differentially Expressed Genes and Pathways in Hepatocellular Carcinoma
journal, January 2019

  • Cai, Changzhou; Wang, Weilin; Tu, Zhenhua
  • Journal of Cancer, Vol. 10, Issue 2
  • DOI: 10.7150/jca.27832