Home LiteratureArticle Details
PMID: 18701503 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Focal gains of VEGFA and molecular classification of hepatocellular carcinoma.

Cancer research ·Vol. 68 ·No. 16 ·2008-08-15 ·Pages 6779-88

Chiang DY, Villanueva A, Hoshida Y, Peix J, Newell P, Minguez B, LeBlanc AC, Donovan DJ, Thung SN, Solé M, Tovar V, Alsinet C, Ramos AH, Barretina J, Roayaie S, Schwartz M, Waxman S, Bruix J, Mazzaferro V, Ligon AH, Najfeld V, Friedman SL, Sellers WR, Meyerson M, Llovet JM

Abstract

Hepatocellular carcinomas represent the third leading cause of cancer-related deaths worldwide. The vast majority of cases arise in the context of chronic liver injury due to hepatitis B virus or hepatitis C virus infection. To identify genetic mechanisms of hepatocarcinogenesis, we characterized copy number alterations and gene expression profiles from the same set of tumors associated with hepatitis C virus. Most tumors harbored 1q gain, 8q gain, or 8p loss, with occasional alterations in 13 additional chromosome arms. In addition to amplifications at 11q13 in 6 of 103 tumors, 4 tumors harbored focal gains at 6p21 incorporating vascular endothelial growth factor A (VEGFA). Fluorescence in situ hybridization on an independent validation set of 210 tumors found 6p21 high-level gains in 14 tumors, as well as 2 tumors with 6p21 amplifications. Strikingly, this locus overlapped with copy gains in 4 of 371 lung adenocarcinomas. Overexpression of VEGFA via 6p21 gain in hepatocellular carcinomas suggested a novel, non-cell-autonomous mechanism of oncogene activation. Hierarchical clustering of gene expression among 91 of these tumors identified five classes, including "CTNNB1", "proliferation", "IFN-related", a novel class defined by polysomy of chromosome 7, and an unannotated class. These class labels were further supported by molecular data; mutations in CTNNB1 were enriched in the "CTNNB1" class, whereas insulin-like growth factor I receptor and RPS6 phosphorylation were enriched in the "proliferation" class. The enrichment of signaling pathway alterations in gene expression classes provides insights on hepatocellular carcinoma pathogenesis. Furthermore, the prevalence of VEGFA high-level gains in multiple tumor types suggests indications for clinical trials of antiangiogenic therapies.

MeSH Terms
Adenocarcinoma/genetics,pathology Biomarkers, Tumor/genetics,metabolism Carcinoma, Hepatocellular/classification,genetics,virology Chromosome Aberrations Chromosomes, Human, Pair 6/genetics Chromosomes, Human, Pair 7/genetics Gene Dosage Gene Expression Profiling Hepatitis B, Chronic/complications,genetics Hepatitis C, Chronic/complications,genetics Humans Immunoenzyme Techniques In Situ Hybridization, Fluorescence Karyotyping Liver Neoplasms/classification,genetics,virology Lung Neoplasms/genetics,secondary Neoplasm Staging Nucleic Acid Hybridization Oligonucleotide Array Sequence Analysis Prognosis Signal Transduction Survival Rate Tissue Array Analysis Vascular Endothelial Growth Factor A/genetics,metabolism
Chemicals
Biomarkers, Tumor VEGFA protein, human Vascular Endothelial Growth Factor A
Authors & Affiliations
25 authors, click to expand affiliations / ORCID
Chiang Derek Y
Department of Medical Oncology and Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, MA 02115, USA.
Villanueva Augusto
Hoshida Yujin
Peix Judit
Newell Philippa
Minguez Beatriz
LeBlanc Amanda C
Donovan Diana J
Thung Swan N
Solé Manel
Tovar Victoria
Alsinet Clara
Ramos Alex H
Barretina Jordi
Roayaie Sasan
Schwartz Myron
Waxman Samuel
Bruix Jordi
Mazzaferro Vincenzo
Ligon Azra H
Najfeld Vesna
Friedman Scott L
Sellers William R
Meyerson Matthew
Llovet Josep M
References (48)
48 references, click to expand
  1. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling.
    Hepatology. 2004 Sep;40(3):667-76 PMID: 15349906
  2. Chromosome alterations in human hepatocellular carcinomas correlate with aetiology and histological grade--results of an explorative CGH meta-analysis.
    Br J Cancer. 2005 Mar 14;92(5):935-41 PMID: 15756261
  3. Genome-wide detection of human copy number variations using high-density DNA oligonucleotide arrays.
    Genome Res. 2006 Dec;16(12):1575-84 PMID: 17122084
  4. Molecular karyotyping of human hepatocellular carcinoma using single-nucleotide polymorphism arrays.
    Oncogene. 2006 Sep 7;25(40):5581-90 PMID: 16785998
  5. AceView: a comprehensive cDNA-supported gene and transcripts annotation.
    Genome Biol. 2006;7 Suppl 1:S12.1-14 PMID: 16925834
  6. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma.
    Cancer Res. 2008 Mar 1;68(5):1451-61 PMID: 18316609
  7. Amplification and overexpression of the cyclin D1 gene in aggressive human hepatocellular carcinoma.
    Cancer Res. 1994 Jun 15;54(12):3107-10 PMID: 8205525
  8. Clinical significance of vascular endothelial growth factor and basic fibroblast growth factor gene expression in liver tumor.
    Hepatology. 1996 Mar;23(3):455-64 PMID: 8617424
  9. New targets of beta-catenin signaling in the liver are involved in the glutamine metabolism.
    Oncogene. 2002 Nov 28;21(54):8293-301 PMID: 12447692
  10. Tbx3 is a downstream target of the Wnt/beta-catenin pathway and a critical mediator of beta-catenin survival functions in liver cancer.
    Cancer Res. 2007 Feb 1;67(3):901-10 PMID: 17283120
  11. Application of comparative functional genomics to identify best-fit mouse models to study human cancer.
    Nat Genet. 2004 Dec;36(12):1306-11 PMID: 15565109
  12. Chromosomal changes and clonality relationship between primary and recurrent hepatocellular carcinoma.
    Gastroenterology. 2000 Aug;119(2):431-40 PMID: 10930378
  13. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma.
    Hepatology. 2007 Apr;45(4):938-47 PMID: 17393520
  14. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells.
    Nat Med. 2006 Apr;12(4):410-6 PMID: 16532004
  15. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets.
    Hepatology. 2007 Jan;45(1):42-52 PMID: 17187432
  16. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1.
    Science. 2003 Feb 7;299(5608):890-3 PMID: 12574630
  17. GenePattern 2.0.
    Nat Genet. 2006 May;38(5):500-1 PMID: 16642009
  18. Inhibitory effect of antisense vascular endothelial growth factor RNA on the profile of hepatocellular carcinoma cell line in vitro and in vivo.
    World J Gastroenterol. 2006 Feb 21;12(7):1140-3 PMID: 16534861
  19. Liver gene expression signature to predict response to pegylated interferon plus ribavirin combination therapy in patients with chronic hepatitis C.
    Gut. 2008 Apr;57(4):516-24 PMID: 17895355
  20. Correlation between genomic DNA copy number alterations and transcriptional expression in hepatitis B virus-associated hepatocellular carcinoma.
    FEBS Lett. 2006 Jun 26;580(15):3571-81 PMID: 16750200
  21. Hepatocellular carcinoma pathogenesis: from genes to environment.
    Nat Rev Cancer. 2006 Sep;6(9):674-87 PMID: 16929323
  22. Summaries of Affymetrix GeneChip probe level data.
    Nucleic Acids Res. 2003 Feb 15;31(4):e15 PMID: 12582260
  23. Molecular profiling of human hepatocellular carcinoma defines mutually exclusive interferon regulation and insulin-like growth factor II overexpression.
    Cancer Res. 2004 Sep 1;64(17):6058-64 PMID: 15342387
  24. Molecular targeted therapies in hepatocellular carcinoma.
    Hepatology. 2008 Oct;48(4):1312-27 PMID: 18821591
  25. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma.
    J Clin Invest. 2007 Sep;117(9):2713-22 PMID: 17717605
  26. Functional correlates of mutation of the Asp32 and Gly34 residues of beta-catenin.
    Oncogene. 2005 Apr 14;24(16):2667-76 PMID: 15829978
  27. Gene expression patterns in human liver cancers.
    Mol Biol Cell. 2002 Jun;13(6):1929-39 PMID: 12058060
  28. Diagnosis of multiple cancer types by shrunken centroids of gene expression.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6567-72 PMID: 12011421
  29. Molecular pathogenesis of human hepatocellular carcinoma.
    Nat Genet. 2002 Aug;31(4):339-46 PMID: 12149612
  30. A tumor progression model for hepatocellular carcinoma: bioinformatic analysis of genomic data.
    Gastroenterology. 2006 Oct;131(4):1262-70 PMID: 17030195
  31. Changes in gene expression during pegylated interferon and ribavirin therapy of chronic hepatitis C virus distinguish responders from nonresponders to antiviral therapy.
    J Virol. 2007 Apr;81(7):3391-401 PMID: 17267482
  32. A molecular signature to discriminate dysplastic nodules from early hepatocellular carcinoma in HCV cirrhosis.
    Gastroenterology. 2006 Dec;131(6):1758-67 PMID: 17087938
  33. Array-based comparative genomic hybridization reveals recurrent chromosomal aberrations and Jab1 as a potential target for 8q gain in hepatocellular carcinoma.
    Carcinogenesis. 2005 Dec;26(12):2050-7 PMID: 16000397
  34. Overexpression of regenerating islet-derived 1 alpha and 3 alpha genes in human primary liver tumors with beta-catenin mutations.
    Oncogene. 2006 Jan 26;25(4):599-608 PMID: 16314847
  35. Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis.
    Gastroenterology. 2001 Jun;120(7):1763-73 PMID: 11375957
  36. Prediction of venous metastases, recurrence, and prognosis in hepatocellular carcinoma based on a unique immune response signature of the liver microenvironment.
    Cancer Cell. 2006 Aug;10(2):99-111 PMID: 16904609
  37. Genetically distinct and clinically relevant classification of hepatocellular carcinoma: putative therapeutic targets.
    Gastroenterology. 2007 Nov;133(5):1475-86 PMID: 17983802
  38. Redefinition of Affymetrix probe sets by sequence overlap with cDNA microarray probes reduces cross-platform inconsistencies in cancer-associated gene expression measurements.
    BMC Bioinformatics. 2005 Apr 25;6:107 PMID: 15850491
  39. PTK2 and EIF3S3 genes may be amplification targets at 8q23-q24 and are associated with large hepatocellular carcinomas.
    Hepatology. 2003 Nov;38(5):1242-9 PMID: 14578863
  40. Characterizing the cancer genome in lung adenocarcinoma.
    Nature. 2007 Dec 6;450(7171):893-8 PMID: 17982442
  41. Common markers of proliferation.
    Nat Rev Cancer. 2006 Feb;6(2):99-106 PMID: 16491069
  42. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach.
    Cell. 2006 Jun 30;125(7):1253-67 PMID: 16814713
  43. Disruption of beta-catenin pathway or genomic instability define two distinct categories of liver cancer in transgenic mice.
    Gastroenterology. 2004 May;126(5):1374-86 PMID: 15131798
  44. Vascular endothelial growth factor secreted by replicating hepatocytes induces sinusoidal endothelial cell proliferation during regeneration after partial hepatectomy in rats.
    J Hepatol. 2001 May;34(5):683-9 PMID: 11434614
  45. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis.
    Cancer Res. 2004 Oct 1;64(19):7099-109 PMID: 15466206
  46. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):20007-12 PMID: 18077431
  47. Prognostic significance of serum vascular endothelial growth factor and endostatin in patients with hepatocellular carcinoma.
    Br J Surg. 2004 Oct;91(10):1354-60 PMID: 15376182
  48. Hepatocellular carcinoma.
    Lancet. 2003 Dec 6;362(9399):1907-17 PMID: 14667750
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2008-08-15
Pages
6779-88
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC2587454
Subset
IM
Grants
NIDDK NIH HHS · DK076986 · United States
NIDDK NIH HHS · R01 DK076986 · United States
NIDDK NIH HHS · DK037340 · United States
NCI NIH HHS · R01 CA109038 · United States
NIDDK NIH HHS · R01 DK076986-01 · United States
NCI NIH HHS · CA109038 · United States
NIDDK NIH HHS · R01 DK037340 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com