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PMID: 23723997 Published · epublish English Journal Article Research Support, N.I.H., Extramural

Epigenetic upregulation of HGF and c-Met drives metastasis in hepatocellular carcinoma.

PloS one ·Vol. 8 ·No. 5 ·2013-00-00 ·Pages e63765

Ogunwobi OO, Puszyk W, Dong HJ, Liu C

Abstract

Hepatocyte growth factor (HGF) and its receptor, c-Met, are important regulators of growth and differentiation of healthy hepatocytes. However, upregulation of HGF and c-Met have been associated with tumor progression and metastasis in hepatocellular carcinoma (HCC). Hematogenous dissemination is the most common route for cancer metastasis, but the role of HGF and c-Met in circulating tumor cells (CTCs) is unknown. We have isolated and established a circulating tumor cell line from the peripheral blood of a mouse HCC model. Our studies show that these CTCs have increased expression of HGF and c-Met in comparison to the primary tumor cells. The CTCs display phenotypic evidence of epithelial-mesenchymal transition (EMT) and the EMT appears to be inducible by HGF. Epigenetic analysis of the c-Met promoter identified significant loss of DNA methylation in CTCs which correlated with overexpression of c-Met and increased expression of HGF. Six specific CpG sites of c-Met promoter demethylation were identified. CTCs show significantly increased tumorigenicity and metastatic potential in a novel orthotopic syngeneic model of metastatic HCC. We conclude that during hematogenous dissemination in HCC, CTCs undergo EMT under the influence of increased HGF. This process also involves up regulation of c-Met via promoter demethylation at 6 CpG sites. Consequently, targeting HGF and c-Met expression by CTCs may be a novel non-invasive approach with potential clinical applications in HCC management.

MeSH Terms
Animals Base Sequence Carcinogenesis/genetics,pathology Carcinoma, Hepatocellular/genetics,pathology Cell Line, Tumor DNA Methylation/genetics Epigenesis, Genetic Epithelial-Mesenchymal Transition/genetics Gene Expression Regulation, Neoplastic Hepatocyte Growth Factor/genetics Humans Liver Neoplasms/genetics,pathology Mesoderm/pathology Mice Mice, Inbred BALB C Models, Biological Molecular Sequence Data Neoplastic Cells, Circulating/metabolism,pathology Promoter Regions, Genetic/genetics Proto-Oncogene Proteins c-met/genetics,metabolism Up-Regulation/genetics
Chemicals
Hepatocyte Growth Factor Proto-Oncogene Proteins c-met
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ogunwobi Olorunseun O
Department of Pathology, Immunology and Laboratory Medicine, University of Florida, Gainesville, Florida, United States of America.
Puszyk William
Dong Hui-Jia
Liu Chen
References (44)
44 references, click to expand
  1. Methylation-sensitive high resolution melting (MS-HRM): a new approach for sensitive and high-throughput assessment of methylation.
    Nucleic Acids Res. 2007;35(6):e41 PMID: 17289753
  2. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling.
    Hepatology. 2004 Sep;40(3):667-76 PMID: 15349906
  3. Regulation of c-met expression by transcription repressor Daxx.
    Oncogene. 2008 Apr 3;27(15):2177-86 PMID: 17952115
  4. The basics of epithelial-mesenchymal transition.
    J Clin Invest. 2009 Jun;119(6):1420-8 PMID: 19487818
  5. Breast cancer-derived bone metastasis can be effectively reduced through specific c-MET inhibitor tivantinib (ARQ 197) and shRNA c-MET knockdown.
    Mol Cancer Ther. 2012 Jan;11(1):214-23 PMID: 22027690
  6. HGF/c-Met overexpressions, but not met mutation, correlates with progression of non-small cell lung cancer.
    Pathol Oncol Res. 2012 Apr;18(2):209-18 PMID: 21779788
  7. Characterization of metastatic breast cancer patients with nondetectable circulating tumor cells.
    Int J Cancer. 2011 Jul 15;129(2):417-23 PMID: 20857493
  8. Role of overexpression of CD151 and/or c-Met in predicting prognosis of hepatocellular carcinoma.
    Hepatology. 2009 Feb;49(2):491-503 PMID: 19065669
  9. Circulating tumor cells: advances in detection methods, biological issues, and clinical relevance.
    J Cancer Res Clin Oncol. 2011 Aug;137(8):1151-73 PMID: 21681690
  10. Epithelial-mesenchymal transitions in development and disease.
    Cell. 2009 Nov 25;139(5):871-90 PMID: 19945376
  11. The physics of cancer: the role of physical interactions and mechanical forces in metastasis.
    Nat Rev Cancer. 2011 Jun 24;11(7):512-22 PMID: 21701513
  12. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers.
    Mol Cancer Res. 2011 Aug;9(8):997-1007 PMID: 21665936
  13. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis.
    Nature. 2012 Jul 26;487(7408):510-3 PMID: 22763454
  14. Effect of c-Met inhibitor SU11274 on hepatocellular carcinoma cell growth.
    Biosci Trends. 2011;5(2):52-6 PMID: 21572247
  15. Genetic and expression analysis of MET, MACC1, and HGF in metastatic colorectal cancer: response to met inhibition in patient xenografts and pathologic correlations.
    Clin Cancer Res. 2011 May 15;17(10):3146-56 PMID: 21447729
  16. Blockage of HGF/c-Met system by gene therapy (adenovirus-mediated NK4 gene) suppresses hepatocellular carcinoma in mice.
    J Hepatol. 2006 Nov;45(5):688-95 PMID: 16839638
  17. Mechanisms of disease: epithelial-mesenchymal transition--does cellular plasticity fuel neoplastic progression?
    Nat Clin Pract Oncol. 2008 May;5(5):280-90 PMID: 18349857
  18. Tumor self-seeding by circulating cancer cells.
    Cell. 2009 Dec 24;139(7):1315-26 PMID: 20064377
  19. Detection of TIMP3 promoter hypermethylation in salivary rinse as an independent predictor of local recurrence-free survival in head and neck cancer.
    Clin Cancer Res. 2012 Feb 15;18(4):1082-91 PMID: 22228635
  20. Kinase inhibitor Sorafenib modulates immunosuppressive cell populations in a murine liver cancer model.
    Lab Invest. 2011 Apr;91(4):598-608 PMID: 21321535
  21. Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype.
    J Clin Invest. 2006 Jun;116(6):1582-95 PMID: 16710476
  22. Hepatocellular carcinoma displays distinct DNA methylation signatures with potential as clinical predictors.
    PLoS One. 2010 Mar 17;5(3):e9749 PMID: 20305825
  23. DNA methylation suppresses expression of the urea cycle enzyme carbamoyl phosphate synthetase 1 (CPS1) in human hepatocellular carcinoma.
    Am J Pathol. 2011 Feb;178(2):652-61 PMID: 21281797
  24. DNA methylation profiles of primary colorectal carcinoma and matched liver metastasis.
    PLoS One. 2011;6(11):e27889 PMID: 22132162
  25. Regulation of the c-met proto-oncogene promoter by p53.
    J Biol Chem. 1999 Feb 5;274(6):3565-72 PMID: 9920903
  26. Prognostic role and HER2 expression of circulating tumor cells in peripheral blood of patients prior to radical cystectomy: a prospective study.
    Eur Urol. 2012 Apr;61(4):810-7 PMID: 22277196
  27. Hepatocyte growth factor upregulation promotes carcinogenesis and epithelial-mesenchymal transition in hepatocellular carcinoma via Akt and COX-2 pathways.
    Clin Exp Metastasis. 2011 Dec;28(8):721-31 PMID: 21744257
  28. Candidate epigenetic biomarkers for non-invasive prenatal diagnosis of Down syndrome.
    Reprod Biomed Online. 2007 Aug;15(2):227-35 PMID: 17697502
  29. Phase I trial of a selective c-MET inhibitor ARQ 197 incorporating proof of mechanism pharmacodynamic studies.
    J Clin Oncol. 2011 Apr 1;29(10):1271-9 PMID: 21383285
  30. Identification and verification of rodent cell lines by polymerase chain reaction.
    Cytotechnology. 2008 Jan;56(1):49-56 PMID: 19002841
  31. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma.
    Hepatology. 2011 Sep 2;54(3):879-89 PMID: 21618573
  32. SF/HGF-c-Met autocrine and paracrine promote metastasis of hepatocellular carcinoma.
    World J Gastroenterol. 2001 Dec;7(6):816-20 PMID: 11854908
  33. Cyclooxygenase-2 and Akt mediate multiple growth-factor-induced epithelial-mesenchymal transition in human hepatocellular carcinoma.
    J Gastroenterol Hepatol. 2012 Mar;27(3):566-78 PMID: 22097969
  34. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  35. Dissemination and growth of cancer cells in metastatic sites.
    Nat Rev Cancer. 2002 Aug;2(8):563-72 PMID: 12154349
  36. The current role of circulating tumor cells in the diagnosis and management of bone metastases in advanced prostate cancer.
    Future Oncol. 2012 Mar;8(3):321-31 PMID: 22409467
  37. Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis.
    Cancer Res. 2012 May 15;72(10):2683-91 PMID: 22454286
  38. MEK1 signaling mediates transformation and metastasis of EpH4 mammary epithelial cells independent of an epithelial to mesenchymal transition.
    Cancer Res. 2002 Aug 15;62(16):4781-90 PMID: 12183438
  39. Leptin stimulates proliferation and inhibits apoptosis in Barrett's esophageal adenocarcinoma cells by cyclooxygenase-2-dependent, prostaglandin-E2-mediated transactivation of the epidermal growth factor receptor and c-Jun NH2-terminal kinase activation.
    Endocrinology. 2006 Sep;147(9):4505-16 PMID: 16740977
  40. Detection and characterization of carcinoma cells in the blood.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4589-94 PMID: 9539782
  41. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits.
    Nat Rev Cancer. 2009 Apr;9(4):265-73 PMID: 19262571
  42. Epithelial-to-mesenchymal transition of murine liver tumor cells promotes invasion.
    Hepatology. 2010 Sep;52(3):945-53 PMID: 20564331
  43. Circulating tumor cell isolation and diagnostics: toward routine clinical use.
    Cancer Res. 2011 Sep 15;71(18):5955-60 PMID: 21896640
  44. Single-molecule polymerase chain reaction reduces bias: application to DNA methylation analysis by bisulfite sequencing.
    Anal Biochem. 2008 Jun 1;377(1):46-54 PMID: 18358818
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2013-00-00
Epub
2013-00-28
Pages
e63765
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3665785
Subset
IM
Grants
NCRR NIH HHS · K26RR023976 · United States
NCI NIH HHS · 5T32CA009126-35 · United States
NCRR NIH HHS · K26 RR023976 · United States
NIAAA NIH HHS · R01 AA019976 · United States
NCI NIH HHS · R01 CA133086 · United States
NCI NIH HHS · R01CA133086 · United States
NCI NIH HHS · T32 CA009126 · United States
NIAAA NIH HHS · R01AA019976 · United States
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