Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells

Hepatology

Volumn 53, Issue 4, 2011, Pages 1192-1205

  Schrader, Jörg ^a,b   Gordon Walker, Timothy T ^a   Aucott, Rebecca L ^a   van Deemter, Mariëlle ^a   Quaas, Alexander ^b   Walsh, Shaun ^c   Benten, Daniel ^b   Forbes, Stuart J ^a   Wells, Rebecca G ^d   Iredale, John P ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c NINEWELLS HOSPITAL   (United Kingdom)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; BETA1 INTEGRIN; CD44V ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CISPLATIN; FLUOROURACIL; FOCAL ADHESION KINASE; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; POLYACRYLAMIDE; PROTEIN KINASE B; SCATTER FACTOR; TRANSCRIPTION FACTOR NANOG; TUMOR MARKER;

APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CARCINOMA CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL STRAIN HEPG2; CELL SURVIVAL; CLUSTER ANALYSIS; DIAGNOSTIC KIT; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIVER CELL CARCINOMA; LIVER FIBROSIS; MICROENVIRONMENT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; STAINING; STEM CELL; TUMOR GROWTH;

CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; STAT3 TRANSCRIPTION FACTOR;

EID: 79953736762     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24108     Document Type: Article

References (38)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001; 94: 153-156.
2. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004; 127( 5 Suppl 1): S35-S50.
3. Masuzaki R, Tateishi R, Yoshida H, Goto E, Sato T, Ohki T, et al. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. HEPATOLOGY 2009; 49: 1954-1961.
4. Masuzaki R, Tateishi R, Yoshida H, Sato T, Ohki T, Goto T, et al. Assessing liver tumor stiffness by transient elastography. Hepatol Int 2007; 1: 394-397.
5. Ingber DE. Can cancer be reversed by engineering the tumor microenvironment? Semin Cancer Biol 2008; 18: 356-364.
6. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005; 8: 241-254.
7. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009; 139: 891-906.
8. Nowak AK, Chow PK, Findlay M. Systemic therapy for advanced hepatocellular carcinoma: a review. Eur J Cancer 2004; 40: 1474-1484.
9. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001; 35: 421-430.
10. Mathurin P, Raynard B, Dharancy S, Kirzin S, Fallik D, Pruvot FR, et al. Meta-analysis: evaluation of adjuvant therapy after curative liver resection for hepatocellular carcinoma. Aliment Pharmacol Ther 2003; 17: 1247-1261.
11. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, Choo C, et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 1999; 5: 662-668.
12. Conti JA, Kendall TJ, Bateman A, Armstrong TA, Papa-Adams A, Xu Q, et al. The desmoplastic reaction surrounding hepatic colorectal adenocarcinoma metastases aids tumor growth and survival via alpha(v) integrin ligation. Clin Cancer Res 2008; 14: 6405-6413.
13. Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D. Substrate compliance versus ligand density in cell on gel responses. Biophys J 2004; 86( 1 Pt 1): 617-628.
14. Pelham RJ Jr, Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A 1997; 94: 13661-13665.
15. Kendall TJ, Hennedige S, Aucott RL, Hartland SN, Vernon MA, Benyon RC, et al. p75 Neurotrophin receptor signaling regulates hepatic myofibroblast proliferation and apoptosis in recovery from rodent liver fibrosis. HEPATOLOGY 2009; 49: 901-910.
16. Georges PC, Hui JJ, Gombos Z, McCormick ME, Wang AY, Uemura M, et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 2007; 293: G1147-G1154.
17. Patriarca C, Roncalli M, Gambacorta M, Cominotti M, Coggi G, Viale G. Patterns of integrin common chain beta 1 and collagen IV immunoreactivity in hepatocellular carcinoma. Correlations with tumour growth rate, grade and size. J Pathol 1993; 171: 5-11.
18. Fujii T, Koshikawa K, Nomoto S, Okochi O, Kaneko T, Inoue S, et al. Focal adhesion kinase is overexpressed in hepatocellular carcinoma and can be served as an independent prognostic factor. J Hepatol 2004; 41: 104-111.
19. Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005; 128: 343-350.
20. Kornek M, Raskopf E, Tolba R, Becker U, Klockner M, Sauerbruch T, et al. Accelerated orthotopic hepatocellular carcinomas growth is linked to increased expression of pro-angiogenic and prometastatic factors in murine liver fibrosis. Liver Int 2008; 28: 509-518.
21. Kuriyama S, Yamazaki M, Mitoro A, Tsujimoto T, Kikukawa M, Tsujinoue H, et al. Hepatocellular carcinoma in an orthotopic mouse model metastasizes intrahepatically in cirrhotic but not in normal liver. Int J Cancer 1999; 80: 471-476.
22. Osada S, Kanematsu M, Imai H, Goshima S, Sugiyama Y. Hepatic fibrosis influences the growth of hepatocellular carcinoma. Hepatogastroenterology 2008; 55: 184-187.
23. Ulrich TA, de Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 2009; 69: 4167-4174.
24. Klein EA, Campbell LE, Kothapalli D, Fournier AK, Assoian RK. Joint requirement for Rac and ERK activities underlies the mid-G1 phase induction of cyclin D1 and S phase entry in both epithelial and mesenchymal cells. J Biol Chem 2008; 283: 30911-30918.
25. Aguirre Ghiso JA, Kovalski K, Ossowski L. Tumor dormancy induced by downregulation of urokinase receptor in human carcinoma involves integrin and MAPK signaling. J Cell Biol 1999; 147: 89-104.
26. Hedvat M, Huszar D, Herrmann A, Gozgit JM, Schroeder A, Sheehy A, et al. The JAK2 inhibitor AZD1480 potently blocks Stat3 signaling and oncogenesis in solid tumors. Cancer Cell 2009; 16: 487-497.
27. Barkan D, Green JE, Chambers AF. Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur J Cancer 2010; 46: 1181-1188.
28. Levental I, Georges PC, Janmey PA. Soft biological materials and their influence on cell function. Soft Matter 2007; 3: 299-306.
29. Fisher B, Fisher ER. Experimental evidence in support of the dormant tumor cell. Science 1959; 130: 918-919.
30. Agostino D, Cliffton EE. Organ localization and the effect of trauma on the fate of circulating cancer cells. Cancer Res 1965; 25: 1728-1732.
31. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010; 70: 5706-5716.
32. Vessella RL, Pantel K, Mohla S. Tumor cell dormancy: an NCI workshop report. Cancer Biol Ther 2007; 6: 1496-1504.
33. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009; 28: 15-33.
34. Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007; 39: 305-318.
35. Godoy P, Hengstler JG, Ilkavets I, Meyer C, Bachmann A, Muller A, et al. Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis. HEPATOLOGY 2009; 49: 2031-2043.
36. Cicchini C, Laudadio I, Citarella F, Corazzari M, Steindler C, Conigliaro A, et al. TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp Cell Res 2008; 314: 143-152.
37. Naumov GN, Townson JL, MacDonald IC, Wilson SM, Bramwell VH, Groom AC, et al. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast Cancer Res Treat 2003; 82: 199-206.
38. Lee TK, Castilho A, Ma S, Ng IO. Liver cancer stem cells: implications for a new therapeutic target. Liver Int 2009; 29: 955-965.