Mechanism-related circulating proteins as biomarkers for clinical outcome in patients with unresectable hepatocellular carcinoma receiving sunitinib

Journal of Translational Medicine

Volumn 9, Issue 1, 2011, Pages

  Harmon, Charles S ^a   DePrimo, Samuel E ^a,h   Raymond, Eric ^b   Cheng, Ann Lii ^c   Boucher, Eveline ^d   Douillard, Jean Yves ^e   Lim, Ho Y ^f   Kim, Jun S ^g   Lechuga, Maria J ^a   Lanzalone, Silvana ^a   Lin, Xun ^a   Faivre, Sandrine ^b  

^a PFIZER INC   (United States)

^b BEAUJON HOSPITAL   (France)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d RENNES UNIVERSITY HOSPITAL   (France)

^e CENTRE RENÉ GAUDUCHEAU   (France)

^f Samsung Medical Center   (South Korea)

^g Korea University College of Medicine   (South Korea)

^h EXELIXIS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL FACTOR; SUNITINIB; TUMOR MARKER; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; ANGIOGENESIS INHIBITOR; INDOLE DERIVATIVE; PYRROLE DERIVATIVE; TUMOR PROTEIN; VEGFC PROTEIN, HUMAN;

ADULT; ADVANCED CANCER; ARTICLE; CANCER CONTROL; CANCER SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG MECHANISM; FEMALE; HUMAN; LIVER CELL CARCINOMA; MALE; MULTICENTER STUDY; MULTIPLE CYCLE TREATMENT; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL; PREDICTION; PREDICTIVE VALUE; PROTEIN FUNCTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SEX DIFFERENCE; TUMOR GROWTH; BLOOD; CLINICAL TRIAL; DISEASE COURSE; KAPLAN MEIER METHOD; LIVER TUMOR; MULTIVARIATE ANALYSIS; TIME; TREATMENT OUTCOME;

ANGIOGENESIS INHIBITORS; CARCINOMA, HEPATOCELLULAR; DISEASE PROGRESSION; FEMALE; HUMANS; INDOLES; KAPLAN-MEIER ESTIMATE; LIVER NEOPLASMS; MALE; MULTIVARIATE ANALYSIS; NEOPLASM PROTEINS; PYRROLES; ROC CURVE; TIME FACTORS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 79960590467     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-9-120     Document Type: Article

References (47)

1. Yao DF, Wu XH, Zhu Y, Shi GS, Dong ZZ, Yao DB, Wu W, Qiu LW, Meng XY. Quantitative analysis of vascular endothelial growth factor, microvascular density and their clinicopathologic features in human hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2005, 4:220-226.
2. Zhang ZL, Liu ZS, Sun Q. Expression of angiopoietins, Tie2 and vascular endothelial growth factor in angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 2006, 12:4241-4245.
3. Amaoka N, Saio M, Nonaka K, Imai H, Tomita H, Sakashita F, Takahashi T, Sugiyama Y, Takami T, Adachi Y. Expression of vascular endothelial growth factor receptors is closely related to the histological grade of hepatocellular carcinoma. Oncol Rep 2006, 16:3-10.
4. Thelen A, Scholz A, Benckert C, von Marschall Z, Schröder M, Wiedenmann B, Neuhaus P, Rosewicz S, Jonas S. VEGF-D promotes tumor growth and lymphatic spread in a mouse model of hepatocellular carcinoma. Int J Cancer 2008, 122:2471-2481. 10.1002/ijc.23439, 18338756.
5. Semela D, Dufour JF. Angiogenesis and hepatocellular carcinoma. J Hepatol 2004, 41:864-880. 10.1016/j.jhep.2004.09.006, 15519663.
6. Park YN, Kim YB, Yang KM, Park C. Increased expression of vascular endothelial growth factor and angiogenesis in the early stage of multistep hepatocarcinogenesis. Arch Pathol Lab Med 2000, 124:1061-1065.
7. Kim SJ, Choi IK, Park KH, Yoon SY, Oh SC, Seo JH, Choi CW, Kim BS, Shin SW, Kim YH, Kim JS. Serum vascular endothelial growth factor per platelet count in hepatocellular carcinoma: correlations with clinical parameters and survival. Jpn J Clin Oncol 2004, 34:184-190. 10.1093/jjco/hyh039, 15121753.
8. Poon RT, Ng IO, Lau C, Yu WC, Fan ST, Wong J. Correlation of serum basic fibroblast growth factor levels with clinicopathologic features and postoperative recurrence in hepatocellular carcinoma. Am J Surg 2001, 182:298-304. 10.1016/S0002-9610(01)00708-5, 11587697.
9. Kong SY, Park JW, Lee JA, Park JE, Park KW, Hong EK, Kim CM. Association between vascular endothelial growth factor gene polymorphisms and survival in hepatocellular carcinoma patients. Hepatology 2007, 46:446-455. 10.1002/hep.21720, 17659575.
10. Moon EJ, Jeong CH, Jeong JW, Kim KR, Yu DY, Murakami S, Kim CW, Kim KW. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1alpha. FASEB J 2004, 18:382-384.
11. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, Luo R, Feng J, Ye S, Yang TS, Xu J, Sun Y, Liang H, Liu J, Wang J, Tak WY, Pan H, Burock K, Zou J, Voliotis D, Guan Z. 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. 10.1016/S1470-2045(08)70285-7, 19095497.
12. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Häussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J, . the SHARP Investigators Study Group Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008, 359:378-390. 10.1056/NEJMoa0708857, 18650514, the SHARP Investigators Study Group.
13. Zhu AX, Sahani DV, Duda DG, di Tomaso E, Ancukiewicz M, Catalano OA, Sindhwani V, Blaszkowsky LS, Yoon SS, Lahdenranta J, Bhargava P, Meyerhardt J, Clark JW, Kwak EL, Hezel AF, Miksad R, Abrams TA, Enzinger PC, Fuchs CS, Ryan DP, Jain RK. Efficacy, safety, and potential biomarkers of sunitinib monotherapy in advanced hepatocellular carcinoma: a phase II study. J Clin Oncol 2009, 27:3027-3035. 10.1200/JCO.2008.20.9908, 2702235, 19470923.
14. Faivre S, Raymond E, Boucher E, Douillard J, Lim HY, Kim JS, Zappa M, Lanzalone S, Lin X, Deprimo S, Harmon C, Ruiz-Garcia A, Lechuga MJ, Cheng AL. Safety and efficacy of sunitinib in patients with advanced hepatocellular carcinoma: an open-label, multicentre, phase II study. Lancet Oncol 2009, 10:794-800. 10.1016/S1470-2045(09)70171-8, 19586800.
15. Koeberle D, Montemurro M, Samaras P, Majno P, Simcock M, Limacher A, Lerch S, Kovàcs K, Inauen R, Hess V, Saletti P, Borner M, Roth A, Bodoky G. Continuous sunitinib treatment in patients with advanced hepatocellular carcinoma: a Swiss Group for Clinical Cancer Research (SAKK) and Swiss Association for the Study of the Liver (SASL) multicenter phase II trial (SAKK 77/06). Oncologist 2010, 15:285-292. 10.1634/theoncologist.2009-0316, 20203173.
16. Abrams TJ, Lee LB, Murray LJ, Pryer NK, Cherrington JM. SU11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther 2003, 2:471-478.
17. Kim DW, Jo YS, Jung HS, Chung HK, Song JH, Park KC, Park SH, Hwang JH, Rha SY, Kweon GR, Lee SJ, Jo KW, Shong M. An orally administered multitarget tyrosine kinase inhibitor, SU11248, is a novel potent inhibitor of thyroid oncogenic RET/papillary thyroid cancer kinases. J Clin Endocrinol Metab 2006, 91:4070-4076. 10.1210/jc.2005-2845, 16849418.
18. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G, Schreck RE, Abrams TJ, Ngai TJ, Lee LB, Murray LJ, Carver J, Chan E, Moss KG, Haznedar JO, Sukbuntherng J, Blake RA, Sun L, Tang C, Miller T, Shirazian S, McMahon G, Cherrington JM. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 2003, 9:327-337.
19. Murray LJ, Abrams TJ, Long KR, Ngai TJ, Olson LM, Hong W, Keast PK, Brassard JA, O'Farrell AM, Cherrington JM, Pryer NK. SU11248 inhibits tumor growth and CSF-1R-dependent osteolysis in an experimental breast cancer bone metastasis model. Clin Exp Metastasis 2003, 20:757-766.
20. O'Farrell AM, Abrams TJ, Yuen HA, Ngai TJ, Louie SG, Yee KW, Wong LM, Hong W, Lee LB, Town A, Smolich BD, Manning WC, Murray LJ, Heinrich MC, Cherrington JM. SU11248 is a novel FLT3 tyrosine kinase inhibitor with potent activity in vitro and in vivo. Blood 2003, 101:3597-3605. 10.1182/blood-2002-07-2307, 12531805.
21. Kodera Y, Katanasaka Y, Kitamura Y, Hitoshi T, Nishio K, Tamura T, Koizumi F. Sunitinib inhibits lymphatic endothelial cell functions and lymph node metastasis in a breast cancer model through inhibition of vascular endothelial growth factor receptor 3. Breast Cancer Res 2011,
22. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG. New guidelines to evaluate the response to treatment in solid tumors. J Natl Cancer Inst 2000, 92:205-216. 10.1093/jnci/92.3.205, 10655437.
23. Faivre S, Zappa M, Vilgrain V, Boucher E, Douillard JY, Lim HY, Kim JS, Im SA, Kang YK, Bouattour M, Dokmak S, Dreyer C, Sablin MP, Serrate C, Cheng AL, Lanzalone S, Lin X, Lechuga MJ, Raymond E. Changes in Tumor Density in Patients with Advanced Hepatocellular Carcinoma Treated with Sunitinib. Clin Cancer Res 2011, 17:4504-4512. 10.1158/1078-0432.CCR-10-1708, 21531821.
24. DePrimo SE, Bello CL, Smeraglia J, Baum CM, Spinella D, Rini BI, Michaelson MD, Motzer RJ. Circulating protein biomarkers of pharmacodynamic activity of sunitinib in patients with metastatic renal cell carcinoma: modulation of VEGF and VEGF-related proteins. J Transl Med 2007, 5:32. 10.1186/1479-5876-5-32, 1939830, 17605814.
25. Bello CL, DePrimo SE, Friece C, Smeraglia J, Sherman L, Tye L, Baum CM, Meropol NJ, Lenz H, Kulke MH. Analysis of circulating biomarkers of sunitinib malate in patients with unresectable neuroendocrine tumors (NET): VEGF, IL-8, and soluble VEGF receptors 2 and 3. J Clin Oncol 2006, 24(Suppl 18S). Abstract 4045.
26. Burstein HJ, Elias AD, Rugo HS, Cobleigh MA, Wolff AC, Eisenberg PD, Lehman M, Adams BJ, Bello CL, DePrimo SE, Baum CM, Miller KD. Phase II study of sunitinib malate, an oral multitargeted tyrosine kinase inhibitor, in patients with metastatic breast cancer previously treated with an anthracycline and a taxane. J Clin Oncol 2008, 26:1810-1816. 10.1200/JCO.2007.14.5375, 18347007.
27. Faivre S, Delbaldo C, Vera K, Robert C, Lozahic S, Lassau N, Bello C, Deprimo S, Brega N, Massimini G, Armand JP, Scigalla P, Raymond E. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol 2006, 24:25-35. 10.1200/JCO.2005.02.2194, 16314617.
28. Motzer RJ, Michaelson MD, Redman BG, Hudes GR, Wilding G, Figlin RA, Ginsberg MS, Kim ST, Baum CM, DePrimo SE, Li JZ, Bello CL, Theuer CP, George DJ, Rini BI. Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J Clin Oncol 2006, 24:16-24. 10.1200/JCO.2005.02.2574, 16330672.
29. Norden-Zfoni A, Desai J, Manola J, Beaudry P, Force J, Maki R, Folkman J, Bello C, Baum C, DePrimo SE, Shalinsky DR, Demetri GD, Heymach JV. Blood-based biomarkers of SU11248 activity and clinical outcome in patients with metastatic imatinib-resistant gastrointestinal stromal tumor. Clin Cancer Res 2007, 13:2643-2650. 10.1158/1078-0432.CCR-06-0919, 17473195.
30. George S, Blay JY, Casali PG, Le Cesne A, Stephenson P, DePrimo SE, Harmon CS, Law CN, Morgan JA, Ray-Coquard I, Tassell V, Cohen DP, Demetri GD. Clinical evaluation of continuous daily dosing of sunitinib malate in patients with advanced gastrointestinal stromal tumor after imatinib failure. Eur J Cancer 2009, 45:1959-1968. 10.1016/j.ejca.2009.02.011, 19282169.
31. DePrimo SE, Huang X, Blackstein ME, Garrett CR, Harmon CS, Schöffski P, Shah MH, Verweij J, Baum CM, Demetri GD. Circulating levels of soluble KIT serve as a biomarker for clinical outcome in gastrointestinal stromal tumor patients receiving sunitinib following imatinib failure. Clin Cancer Res 2009, 15:5869-5877. 10.1158/1078-0432.CCR-08-2480, 19737953.
32. Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR, Chen LL, Podoloff DA, Benjamin RS. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol 2007, 25:1753-1759. 10.1200/JCO.2006.07.3049, 17470865.
33. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 2009, 21:154-165. 10.1016/j.ceb.2008.12.012, 19230644.
34. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, Alitalo K. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 1998, 95:14389-14394. 10.1073/pnas.95.24.14389, 24383, 9826710.
35. Clarijs R, Schalkwijk L, Hofmann UB, Ruiter DJ, de Waal RM. Induction of vascular endothelial growth factor receptor-3 expression on tumor microvasculature as a new progression marker in human cutaneous melanoma. Cancer Res 2002, 62:7059-7065.
36. Grau SJ, Trillsch F, Herms J, Thon N, Nelson PJ, Tonn JC, Goldbrunner R. Expression of VEGFR3 in glioma endothelium correlates with tumor grade. J Neurooncol 2007, 82:141-150. 10.1007/s11060-006-9272-4, 17115285.
37. Valtola R, Salven P, Heikkilä P, Taipale J, Joensuu H, Rehn M, Pihlajaniemi T, Weich H, deWaal R, Alitalo K. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 1999, 154:1381-1390. 10.1016/S0002-9440(10)65392-8, 1866582, 10329591.
38. Achen MG, Williams RA, Baldwin ME, Lai P, Roufail S, Alitalo K, Stacker SA. The angiogenic and lymphangiogenic factor vascular endothelial growth factor-D exhibits a paracrine mode of action in cancer. Growth Factors 2002, 20:99-107. 10.1080/08977190290031969, 12148568.
39. Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, Hutson TE, Margolin K, Harmon CS, DePrimo SE, Kim ST, Chen I, George DJ. Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. J Clin Oncol 2008, 26:3743-3748. 10.1200/JCO.2007.15.5416, 18669461.
40. Motzer RJ, Hudes GR, Ginsberg MS, Baum MS, Harmon CS, Kim ST, Chen I, Redman BG. Phase I/II trial of sunitinib plus gefitinib in patients with metastatic renal cell carcinoma. Am J Clin Oncol 2010, 33:614-618. 10.1097/COC.0b013e3181c4454d, 20142724.
41. Becker G, Schmitt-Graeff A, Ertelt V, Blum HE, Allgaier HP. CD117 (c-kit) expression in human hepatocellular carcinoma. Clin Oncol (R Coll Radiol) 2007, 19:204-208.
42. Knight B, Tirnitz-Parker JE, Olynyk JK. C-kit inhibition by imatinib mesylate attenuates progenitor cell expansion and inhibits liver tumor formation in mice. Gastroenterology 2008, 135:969-979. 979.e1, 10.1053/j.gastro.2008.05.077, 18602920.
43. Tandon P, Garcia-Tsao G. Prognostic indicators in hepatocellular carcinoma: a systematic review of 72 studies. Liver Int 2009, 29:502-510. 10.1111/j.1478-3231.2008.01957.x, 2711257, 19141028.
44. Ogawa E, Takenaka K, Yanagihara K, Kurozumi M, Manabe T, Wada H, Tanaka F. Clinical significance of VEGF-C status in tumour cells and stromal macrophages in non-small cell lung cancer patients. Br J Cancer 2004, 91:498-503. 10.1038/sj.bjc.6601992, 2409842, 15226767.
45. Liu P, Chen W, Zhu H, Liu B, Song S, Shen W, Wang F, Tucker S, Zhong B, Wang D. Expression of VEGF-C correlates with a poor prognosis based on analysis of prognostic factors in 73 patients with esophageal squamous cell carcinomas. Jpn J Clin Oncol 2009, 39:644-650. 10.1093/jjco/hyp079, 19648590.
46. Tsutsumi S, Kuwano H, Shimura T, Morinaga N, Mochiki E, Asao T. Vascular endothelial growth factor C (VEGF-C) expression in pT2 gastric cancer. Hepatogastroenterology 2005, 52:629-632.
47. Miyazaki T, Okada N, Ishibashi K, Ogata K, Ohsawa T, Ishiguro T, Nakada H, Yokoyama M, Matsuki M, Kato H, Kuwano H, Ishida H. Clinical significance of plasma level of vascular endothelial growth factor-C in patients with colorectal cancer. Jpn J Clin Oncol 2008, 38:839-843. 10.1093/jjco/hyn106, 18923001.