Moving towards personalised therapy in patients with hepatocellular carcinoma: The role of the microenvironment

Gut

Volumn 63, Issue 10, 2014, Pages 1668-1676

  Giannelli, Gianluigi ^a   Rani, Bhavna ^a   Dituri, Francesco ^a   Cao, Yuan ^a   Palasciano, Giuseppe ^a  

^a UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRIVANIB; CONNECTIVE TISSUE GROWTH FACTOR; ERLOTINIB; EVEROLIMUS; GALUNISERTIB; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; KALININ; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLACEBO; RAMUCIRUMAB; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SCLEROPROTEIN; SORAFENIB; STAT3 PROTEIN; SUNITINIB; TAMOXIFEN; TIVANTINIB; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

BLEEDING; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER GROWTH; CELL HETEROGENEITY; CIRCULATING TUMOR CELL; DRUG EFFICACY; DRUG SAFETY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; LIVER CELL CARCINOMA; MULTICENTER STUDY (TOPIC); NEUTROPENIA; NONHUMAN; OVERALL SURVIVAL; PERSONALIZED MEDICINE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; UNSPECIFIED SIDE EFFECT; DISEASE COURSE; LIVER TUMOR; METHODOLOGY; TGF-BETA;

HEPATOCELLULAR CARCINOMA; TGF-BETA;

CARCINOMA, HEPATOCELLULAR; DISEASE PROGRESSION; HUMANS; INDIVIDUALIZED MEDICINE; LIVER NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84908551404     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2014-307323     Document Type: Review

References (92)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
3. El-Serag HB. Epidemiology of hepatocellular carcinoma in USA. Hepatol Res 2007;37(Suppl 2):S88-94.
4. Bosetti C, Levi F, Boffetta P, et al. Trends in mortality from hepatocellular carcinoma in Europe, 1980-2004. Hepatology 2008;48:137-45.
5. Chang MH, You SL, Chen CJ, et al. Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: a 20-year follow-up study. J Natl Cancer Inst 2009;101:1348-55.
6. Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
7. Schlaeger C, Longerich T, Schiller C, et al. Etiology-dependent molecular mechanisms in human hepatocarcinogenesis. Hepatology 2008;47:511-20.
8. Liotta LA, Tryggvason K, Garbisa S, et al. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980;284:67-8.
9. Itoh Y, Binner S, Nagase H. Steps involved in activation of the complex of pro-matrix metalloproteinase 2 (progelatinase A) and tissue inhibitor of metalloproteinases (TIMP)-2 by 4-aminophenylmercuric acetate. Biochem J 1995;3082):645-51.
10. Kinoshita T, Sato H, Okada A, et al. TIMP-2 promotes activation of progelatinase A by membrane-type 1 matrix metalloproteinase immobilized on agarose beads. J Biol Chem 1998;273:16098-103.
11. Galateau-Salle FB, Luna RE, Horiba K, et al. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in bronchial squamous preinvasive lesions. Hum Pathol 2000;31:296-305.
12. Sparano JA, Bernardo P, Stephenson P, et al. Randomized phase III trial of marimastat versus placebo in patients with metastatic breast cancer who have responding or stable disease after first-line chemotherapy: Eastern Cooperative Oncology Group trial E2196. J Clin Oncol 2004;22:4683-90.
13. Kohn EC, Liotta LA. Molecular insights into cancer invasion: strategies for prevention and intervention. Cancer Res 1995;55:1856-62.
14. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature 2001;411:375-9.
15. Burgeson RE, Chiquet M, Deutzmann R, et al. A new nomenclature for the laminins. Matrix Biol 1994;14:209-11.
16. Baker SE, Hopkinson SB, Fitchmun M, et al. Laminin-5 and hemidesmosomes: role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 1996;109 (Pt 10):2509-20.
17. Santamato A, Fransvea E, Dituri F, et al. Hepatic stellate cells stimulate HCC cell migration via laminin-5 production. Clin Sci (Lond) 2011;121:159-68.
18. Giannelli G, Falk-Marzillier J, Schiraldi O, et al. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997;277:225-8.
19. Koshikawa N, Giannelli G, Cirulli V, et al. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 2000;148:615-24.
20. Seftor RE, Seftor EA, Koshikawa N, et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 2001;61:6322-7.
21. Giannelli G, Antonaci S. Biological and clinical relevance of Laminin-5 in cancer. In: Clin. Exp. Metastasis, 2001.
22. Schenk S, Hintermann E, Bilban M, et al. Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution. J Cell Biol 2003;161:197-209.
23. Bergamini C, Sgarra C, Trerotoli P, et al. Laminin-5 stimulates hepatocellular carcinoma growth through a different function of alpha6beta4 and alpha3beta1 integrins. Hepatology 2007;46:1801-9.
24. Hlubek F, Jung A, Kotzor N, et al. Expression of the invasion factor laminin gamma2 in colorectal carcinomas is regulated by beta-catenin. Cancer Res 2001;61:8089-93.
25. Giannelli G, Bergamini C, Fransvea E, et al. Laminin-5 with transforming growth factor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma. Gastroenterology 2005;129:1375-83.
26. Giannelli G, Fransvea E, Bergamini C, et al. Laminin-5 chains are expressed differentially in metastatic and nonmetastatic hepatocellular carcinoma. Clin Cancer Res 2003;9:3684-91.
27. Govaere O, Komuta M, Berkers J, et al. Keratin 19: a key role player in the invasion of human hepatocellular carcinomas. Gut 2014;63:674-85.
28. Sulpice L, Rayar M, Desille M, et al. Molecular profiling of stroma identifies osteopontin as an independent predictor of poor prognosis in intrahepatic cholangiocarcinoma. Hepatology 2013;58:1992-2000.
29. Giannelli G, Astigiano S, Antonaci S, et al. Role of the alpha3beta1 and alpha6beta4 integrins in tumor invasion. Clin Exp Metastasis 2002;19:217-23.
30. Lampe PD, Nguyen BP, Gil S, et al. Cellular interaction of integrin alpha3beta1 with laminin 5 promotes gap junctional communication. J Cell Biol 1998;143:1735-47.
31. Plopper GE, Domanico SZ, Cirulli V, et al. Migration of breast epithelial cells on Laminin-5: differential role of integrins in normal and transformed cell types. Breast Cancer Res Treat 1998;51:57-69.
32. Liu L, Cao Y, Chen C, et al. Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 2006;66:11851-8.
33. Abou-Alfa GK, Schwartz L, Ricci S, et al. Phase II study of sorafenib in patients with advanced hepatocellular carcinoma. J Clin Oncol 2006;24:4293-300.
34. Cheng AL, Kang YK, Chen Z, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009;10:25-34.
35. Iavarone M, Cabibbo G, Piscaglia F, et al. Field-practice study of sorafenib therapy for hepatocellular carcinoma: a prospective multicenter study in Italy. Hepatology 2011;54:2055-63.
36. Finn RS, Kang YK, Mulcahy M, et al. Phase II, open-label study of brivanib as second-line therapy in patients with advanced hepatocellular carcinoma. Clin Cancer Res 2012;18:2090-8.
37. Llovet JM, Decaens T, Raoul JL, et al. Brivanib in patients with advanced hepatocellular carcinoma who were intolerant to sorafenib or for whom sorafenib failed: results from the randomized phase III BRISK-PS study. J Clin Oncol 2013;31:3509-16.
38. Johnson PJ, Qin S, Park JW, et al. Brivanib versus sorafenib as first-line therapy in patients with unresectable, advanced hepatocellular carcinoma: results from the randomized phase III BRISK-FL study. J Clin Oncol 2013;31:3517-24.
39. Santoro A, Rimassa L, Borbath I, et al. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomised, placebo-controlled phase 2 study. Lancet Oncol 2013;14:55-63.
40. Zhu AX, Finn RS, Mulcahy M, et al. A phase II and biomarker study of ramucirumab, a human monoclonal antibody targeting the VEGF receptor-2, as first-line monotherapy in patients with advanced hepatocellular cancer. Clin Cancer Res 2013;19:6614-23.
41. Sieghart W, Pinter M, Dauser B, et al. Erlotinib and sorafenib in an orthotopic rat model of hepatocellular carcinoma. J Hepatol 2012;57:592-9.
42. Llovet JM, Pena CE, Lathia CD, et al. Plasma biomarkers as predictors of outcome in patients with advanced hepatocellular carcinoma. Clin Cancer Res 2012;18:2290-300.
43. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002;296:1655-7.
44. Samuels Y, Velculescu VE. Oncogenic mutations of PIK3CA in human cancers. Cell Cycle 2004;3:1221-4.
45. Kang S, Bader AG, Zhao L, et al. Mutated PI 3-kinases: cancer targets on a silver platter. Cell Cycle 2005;4:578-81.
46. Fabregat I. Dysregulation of apoptosis in hepatocellular carcinoma cells. World J Gastroenterol 2009;15:513-20.
47. Dituri F, Mazzocca A, Lupo L, et al. PI3K class IB controls the cell cycle checkpoint promoting cell proliferation in hepatocellular carcinoma. Int J Cancer 2012;130:2505-13.
48. Erstad DJ, Cusack JC Jr. Targeting the NF-kappaB pathway in cancer therapy. Surg Oncol Clin N Am 2013;22:705-46.
49. Koehler BC, Urbanik T, Vick B, et al. TRAIL-induced apoptosis of hepatocellular carcinoma cells is augmented by targeted therapies. World J Gastroenterol 2009;15:5924-35.
50. Chen KF, Tai WT, Liu TH, et al. Sorafenib overcomes TRAIL resistance of hepatocellular carcinoma cells through the inhibition of STAT3. Clin Cancer Res 2010;16:5189-99.
51. Nojiri K, Sugimoto K, Shiraki K, et al. Sorafenib and TRAIL have synergistic effect on hepatocellular carcinoma. Int J Oncol 2013;42:101-8.
52. Pickup M, Novitskiy S, Moses HL. The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 2013;13:788-99.
53. Massague J. G1 cell-cycle control and cancer. Nature 2004;432:298-306.
54. Gorsch SM, Memoli VA, Stukel TA, et al. Immunohistochemical staining for transforming growth factor beta 1 associates with disease progression in human breast cancer. Cancer Res 1992;52:6949-52.
55. Hasegawa Y, Takanashi S, Kanehira Y, et al. Transforming growth factor-beta1 level correlates with angiogenesis, tumor progression, and prognosis in patients with nonsmall cell lung carcinoma. Cancer 2001;91:964-71.
56. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
57. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 2002;3:155-66.
58. Coulouarn C, Factor VM, Thorgeirsson SS. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology 2008;47:2059-67.
59. Huang GT, Lee HS, Chen CH, et al. Correlation of E-cadherin expression and recurrence of hepatocellular carcinoma. Hepatogastroenterology 1999;46:1923-7.
60. Matsumura T, Makino R, Mitamura K. Frequent down-regulation of E-cadherin by genetic and epigenetic changes in the malignant progression of hepatocellular carcinomas. Clin Cancer Res 2001;7:594-9.
61. Inayoshi J, Ichida T, Sugitani S, et al. Gross appearance of hepatocellular carcinoma reflects E-cadherin expression and risk of early recurrence after surgical treatment. J Gastroenterol Hepatol 2003;18:673-7.
62. Fiorentino M, Altimari A, Ravaioli M, et al. Predictive value of biological markers for hepatocellular carcinoma patients treated with orthotopic liver transplantation. Clin Cancer Res 2004;10:1789-95.
63. Palumbo JS, Kombrinck KW, Drew AF, et al. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 2000;96:3302-9.
64. Suehiro K, Gailit J, Plow EF. Fibrinogen is a ligand for integrin alpha5beta1 on endothelial cells. J Biol Chem 1997;272:5360-6.
65. Vogel BE, Tarone G, Giancotti FG, et al. A novel fibronectin receptor with an unexpected subunit composition (alpha v beta 1). J Biol Chem 1990;265:5934-7.
66. Giannelli G, Pierri F, Trerotoli P, et al. Occurrence of portal vein tumor thrombus in hepatocellular carcinoma affects prognosis and survival. A retrospective clinical study of 150 cases. Hepatol Res 2002;24:50-9.
67. Poon RT, Ng IO, Lau C, et al. Serum vascular endothelial growth factor predicts venous invasion in hepatocellular carcinoma: a prospective study. Ann Surg 2001;233:227-35.
68. Jonas S, Bechstein WO, Steinmuller T, et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis. Hepatology 2001;33:1080-6.
69. Sumie S, Kuromatsu R, Okuda K, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol 2008;15:1375-82.
70. Mise M, Arii S, Higashituji H, et al. Clinical significance of vascular endothelial growth factor and basic fibroblast growth factor gene expression in liver tumor. Hepatology 1996;23:455-64.
71. Semela D, Dufour JF. Angiogenesis and hepatocellular carcinoma. J Hepatol 2004;41:864-80.
72. Yamaguchi R, Yano H, Iemura A, et al. Expression of vascular endothelial growth factor in human hepatocellular carcinoma. Hepatology 1998;28:68-77.
73. Poon RT, Lau CP, Cheung ST, et al. Quantitative correlation of serum levels and tumor expression of vascular endothelial growth factor in patients with hepatocellular carcinoma. Cancer Res 2003;63:3121-6.
74. Liu S, Umezu-Goto M, Murph M, et al. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 2009;15:539-50.
75. Abreu JG, Ketpura NI, Reversade B, et al. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 2002;4:599-604.
76. Liu Y, Liu H, Meyer C, et al. Transforming growth factor-beta (TGF-beta)-mediated connective tissue growth factor (CTGF) expression in hepatic stellate cells requires Stat3 signaling activation. J Biol Chem 2013;288:30708-19.
77. Gressner OA, Gressner AM. Connective tissue growth factor: a fibrogenic master switch in fibrotic liver diseases. Liver Int 2008;28:1065-79.
78. Chu CY, Chang CC, Prakash E, et al. Connective tissue growth factor (CTGF) and cancer progression. J Biomed Sci 2008;15:675-85.
79. Rani B, Cao Y, Malfettone A, et al. Role of the tissue microenvironment as a therapeutic target in hepatocellular carcinoma. World J Gastroenterol 2014;20:4128-40.
80. Fransvea E, Mazzocca A, Santamato A, et al. Kinase activation profile associated with TGF-beta-dependent migration of HCC cells: a preclinical study. Cancer Chemother Pharmacol 2011;68:79-86.
81. Hoshida Y, Villanueva A, Kobayashi M, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 2008;359:1995-2004.
82. Nault JC, De Reynies A, Villanueva A, et al. A hepatocellular carcinoma 5-gene score associated with survival of patients after liver resection. Gastroenterology 2013;145:176-87.
83. Hoshida Y, Nijman SM, Kobayashi M, et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res 2009;69:7385-92.
84. Morton CL, Houghton PJ. Establishment of human tumor xenografts in immunodeficient mice. Nat Protoc 2007;2:247-50.
85. Jin K, Teng L, Shen Y, et al. Patient-derived human tumour tissue xenografts in immunodeficient mice: a systematic review. Clin Transl Oncol 2010;12:473-80.
86. Tentler JJ, Tan AC, Weekes CD, et al. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 2012;9:338-50.
87. Siolas D, Hannon GJ. Patient-derived tumor xenografts: transforming clinical samples into mouse models. Cancer Res 2013;73:5315-19.
88. Rubio-Viqueira B, Hidalgo M. Direct in vivo xenograft tumor model for predicting chemotherapeutic drug response in cancer patients. Clin Pharmacol Ther 2009;85:217-21.
89. Boyault S, Rickman DS, de Reynies A, et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 2007;45:42-52.
90. Toffanin S, Hoshida Y, Lachenmayer A, et al. MicroRNA-based classification of hepatocellular carcinoma and oncogenic role of miR-517a. Gastroenterology 2011;140:1618-28, e16.
91. Breuhahn K, Vreden S, Haddad R, et al. Molecular profiling of human hepatocellular carcinoma defines mutually exclusive interferon regulation and insulin-like growth factor II overexpression. Cancer Research 2004;64:6058-64.
92. Chiang DY, Villanueva A, Hoshida Y, et al. Focal gains of VEGFA and molecular classification of hepatocellular carcinoma. Cancer Research 2008;68:6779-88.