Tumor and circulating biomarkers in patients with second-line hepatocellular carcinoma from the randomized phase II study with tivantinib

Oncotarget

Volumn 7, Issue 45, 2016, Pages 72622-72633

  Rimassa, Lorenza ^a   Abbadessa, Giovanni ^b   Personeni, Nicola ^a,c   Porta, Camillo ^d   Borbath, Ivan ^e   Daniele, Bruno ^f   Salvagni, Stefania ^g   Van Laethem, Jean Luc ^h   Van Vlierberghe, Hans ⁱ   Trojan, Jörg ^j   De Toni, Enrico N ^k   Weiss, Alan ^l   Miles, Steven ^m   Gasbarrini, Antonio ⁿ   Lencioni, Monica ^o   Lamar, Maria E ^b   Wang, Yunxia ^b   Shuster, Dale ^p   Schwartz, Brian E ^b   Santoro, Armando ^a,q  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b ARQULE INC   (United States)

^c UNIVERSITY OF MILAN   (Italy)

^d FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^e CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^f G RUMMO HOSPITAL   (Italy)

^g UNIVERSITY OF BOLOGNA   (Italy)

^h ERASME HOSPITAL   (Belgium)

ⁱ GHENT UNIVERSITY HOSPITAL   (Belgium)

^j UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^k LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^l VANCOUVER GENERAL HOSPITAL   (Canada)

^m Cedars Sinai Hospital   (United States)

ⁿ FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

^o UNIVERSITY HOSPITAL OF PISA   (Italy)

^p DAIICHI SANKYO INC   (United States)

^q HUMANITAS UNIVERSITY   (Italy)

more..

Author keywords

AFP; HCC; HGF; MET; Sorafenib

Indexed keywords

ALPHA FETOPROTEIN; BIOLOGICAL MARKER; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SORAFENIB; TIVANTINIB; VASCULOTROPIN; 2 PYRROLIDONE DERIVATIVE; QUINOLINE DERIVATIVE; TUMOR MARKER;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CANCER MORTALITY; CANCER PROGNOSIS; CANCER SURVIVAL; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL; PREDICTIVE VALUE; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL; SECONDARY HEALTH CARE; VERY ELDERLY; CLINICAL TRIAL; LIVER TUMOR; MIDDLE AGED; MORTALITY; PATHOLOGY; SURVIVAL ANALYSIS;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; FEMALE; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; PROTO-ONCOGENE PROTEINS C-MET; PYRROLIDINONES; QUINOLINES; SURVIVAL ANALYSIS;

EID: 84995743844     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.11621     Document Type: Article

References (48)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65: 87-108.
2. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, Cosme de Oliveira A, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008; 359: 378-90.
3. 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, 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.
4. Finn, Richard S. Survival after sorafenib: Expect the unexpected. J Hepatol. 2014; 60: 243-4.
5. Fornaro L, Vivaldi C, Caparello C, Sacco R, Rotella V, Musettini G, Luchi S, Baldini EE, Falcone A, Masi G. Dissecting signaling pathways in hepatocellular carcinoma: new perspectives in medical therapy. Future Oncol. 2014; 10: 285-304.
6. You H, Ding W, Dang H, Jiang Y, Rountree CB. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma. Hepatology. 2011; 54: 879-89.
7. Chau GY, Lui WY, Chi CW, Chau YP, Li AF, Kao HL, Wu CW. Significance of serum hepatocyte growth factor levels in patients with hepatocellular carcinoma undergoing hepatic resection. Eur J Surg Oncol. 2008; 34: 333-8.
8. Santoro A, Rimassa L, Borbath I, Daniele B, Salvagni S, Van Leathem JL, Van Vlierberghe H, Trojan J, Kolligs FT, Weiss A, Miles S, Gasbarrini A, Lencioni M. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomized, placebo controlled phase 2 study. Lancet Oncol. 2013; 14: 55-63.
9. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003; 3: 347-61.
10. Jahangiri A, De Lay M, Miller LM, Carbonell WS, Hu YL, Lu K, Tom MW, Paquette J, Tokuyasu TA, Tsao S, Marshall R, Perry A, Bjorgan KM. Gene expression profile identifies tyrosine kinase c-Met as a targetable mediator of antiangiogenic therapy resistance. Clin Cancer Res. 2013; 19: 1773-83.
11. Piscaglia AC, Saulnier N, Barba M, Castellini L, Tesori V, Campanale M, Purchiaroni F, Zocco MA, Galeotti T, Pani G, Gasbarrini A. Transcriptome analysis and sorafenib effects on HGF/cMET pathway in liver cancer cell lines. Hepatology 2009; 50: 290A.
12. Firtina Karagonlar Z, Koc D, Iscan E, Erdal E, Atabey N. Elevated HGF Expression as an Autocrine c-Met Activation Mechanism in Acquired Resistance to Sorafenib in HCC Cells. Cancer Sci. 2016; 107: 407-16.
13. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer. 2012; 12: 89-103.
14. Tesio M, Golan K, Corso S, Giordano S, Schajnovitz A, Vagima Y, Shivtiel S, Kalinkovich A, Caione L, Gammaitoni L, Laurenti E, Buss EC, Shezen E, et al. Enhanced c-Met activity promotes G-CSF-induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood. 2011; 117: 419-28.
15. Gordin M, Tesio M, Cohen S, Gore Y, Lantner F, Leng L, Bucala R, Shachar I. c-Met and its ligand hepatocyte growth factor/scatter factor regulate mature B cell survival in a pathway induced by CD74. J Immunol. 2010; 185: 2020-31.
16. Eathiraj S, Palma R, Hirschi M, Volckova E, Nakuci E, Castro J, Chen CR, Chan TC, France DS, Ashwell MA. A novel mode of protein kinase inhibition exploiting hydrophobic motifs of autoinhibited kinases: discovery of ATP-independent inhibitors of fibroblast growth factor receptor. J Biol Chem. 2011; 286: 20677-87.
17. Munshi N, Jeay S, Li Y, Chen CR, France DS, Ashwell MA, Hill J, Moussa MM, Leggett DS, Li CJ. ARQ 197, a novel and selective inhibitor of the human c-Met receptor tyrosine kinase with antitumor activity. Mol Cancer Ther. 2010; 9: 1544-53.
18. Kanome T, Kadofuku T, Yamaoka T, Hirose H, Akinaga S, Adachi M, Saijo N, Ohmori T. The novel c-MET inhibitor, ARQ 197, shows additive growth-inhibitory effect with erlotinib through enhanced degradation of c-MET protein via ubiquitin/proteasome pathway. Cancer Res. 2010; 70(suppl 8): abstr 1639.
19. Remsing Rix LL, Kuenzi BM, Luo Y, Remily-Wood E, Kinose F, Wright G, Li J, Koomen JM, Haura EB, Lawrence HR, Rixet U. GSK3 alpha and beta are new functionally relevant targets of tivantinib in lung cancer cells. ACS Chem Biol. 2014; 9: 353-8.
20. Kanteti R, Dhanasingh I, Kawada I, Lennon FE, Arif Q, Bueno R, Hasina R, Husain AN, Vigneswaran W, Seiwert T, Kindler HL, Salgia R. MET and PI3K/mTOR as a Potential Combinatorial Therapeutic Target in Malignant Pleural Mesothelioma. PLoS ONE. 2014; 9: e105919.
21. Basilico C, Pennacchietti S, Vigna E, Chiriaco C, Arena S, Bardelli A, Valdembri D, Serini G, Michieli P. Tivantinib (ARQ197) displays cytotoxic activity that is independent of its ability to bind MET. Clin Cancer Res. 2013; 19: 2381-92.
22. Katayama R, Aoyama A, Yamori T, Qi J, Oh-hara T, Song Y, Engelman JA, Fujita N. Cytotoxic Activity of Tivantinib (ARQ 197) Is Not Due Solely to MET Inhibition. Cancer Res. 2013; 73: 3087-96.
23. Porta C, Giglione P, Ferrari A, Reversi F, Liguigli W, Imarisio I, Ganini C. Tivantinib (ARQ197) in hepatocellular carcinoma. Expert Rev Anticancer Ther. 2015; 15: 615-22.
24. Rimassa L, Bruix J, Broggini M, Santoro A. Tivantinib (ARQ197) Displays Cytotoxic Activity That Is Independent of Its Ability to Bind MET-Letter. Clin Cancer Res. 2013; 19: 4290.
25. Rosen LS, Senzer N, Mekhail T, Ganapathi R, Chai F, Savage RE, Waghorne C, Abbadessa G, Schwartz B, Dreicer R. A phase I dose-escalation study of Tivantinib (ARQ 197) in adult patients with metastatic solid tumors. Clin Cancer Res. 2011; 17: 7754-64.
26. Santoro A, Simonelli M, Rodriguez-Lope C, Zucali P, Camacho LH, Granito A, Senzer N, Rimassa L, Abbadessa G, Schwartz B, Lamar M, Savage RE, Bruix J. A Phase-1b study of tivantinib (ARQ 197) in adult patients with hepatocellular carcinoma and cirrhosis. Br J Cancer. 2013; 108: 21-4.
27. Scagliotti G, von Pawel J, Novello S, Ramlau R, Favaretto A, Barlesi F, Akerley W, Orlov S, Santoro A, Spigel D, Hirsh V, Shepherd F, Sequist L, et al. Phase III Multinational, Randomized, Double-Blind, Placebo-Controlled Study of Tivantinib (ARQ 197) Plus Erlotinib Versus Erlotinib Alone in Previously Treated Patients With Locally Advanced or Metastatic Nonsquamous Non-Small-Cell Lung Cancer. J Clin Oncol. 2015; 33: 2667-74.
28. Eng C, Bessudo A, Hart LL, Severtsev A, Gladkov O, Müller L, Kopp MV, Vladimirov V, Langdon R, Kotiv B, Barni S, Hsu C, Bolotin E, et al. A randomized, placebocontrolled, phase 1/2 study of tivantinib (ARQ 197) in combination with irinotecan and cetuximab in patients with metastatic colorectal cancer with wild-type KRAS who have received first-line systemic therapy. Int J Cancer. 2016: 139: 177-86.
29. Yap TA, Olmos D, Brunetto AT, Tunariu N, Barriuso J, Riisnaes R, Pope L, Clark J, Futreal A, Germuska M, Collins D, deSouza NM, Leach MO, et al. Phase I trial of a selective c-MET inhibitor ARQ 197 incorporating proof of mechanism pharmacodynamic studies. J Clin Oncol. 2011; 29: 1271-9.
30. Monk P, Liu G, Stadler WM, Geyer SM, Sexton JL, Wright JJ, Miguel Angel Villalona-Calero, James Lloyd Wade, Russell Zelig Szmulewitz, Shilpa Gupta, Amir Mortazavi, Robert Dreicer, Roberto Pili, et al. Phase II randomized, double-blind, placebo-controlled study of tivantinib in men with asymptomatic or minimally symptomatic metastatic castrate-resistant prostate cancer (mCRPC). J Clin Oncol. 2015; 33(suppl 7): abstr 146.
31. Knudsen BS, Gmyrek GA, Inra J, Scherr DS, Vaughan ED, Nanus DM, Kattan MW, Gerald WL, Vande Woude GF. High expression of the Met receptor in prostate cancer metastasis to bone. Urology. 2002; 60: 1113-7.
32. Tolaney SM, Tan S, Guo H, Barry W, Van Allen E, Wagle N, Brock J, Larrabee K, Paweletz C, Ivanova E, Janne P, Overmoyer B, Wright JJ, et al. Phase II study of tivantinib (ARQ 197) in patients with metastatic triple-negative breast cancer. Invest New Drugs. 2015; 33: 1108-14.
33. Puzanov I, Sosman J, Santoro A, Saif MW, Goff L, Dy GK, Zucali P, Means-Powell JA, Ma WW, Simonelli M, Martell R, Chai F, Lamar M, et al. Phase 1 trial of tivantinib in combination with sorafenib in adult patients with advanced solid tumors. Invest New Drugs. 2015; 33: 159-68.
34. Hollebecque A, Malka D, Ferté C, Ducreux M, Boige V. Systemic treatment of advanced hepatocellular carcinoma: from disillusions to new horizons. Eur J Cancer. 2015; 51: 327-39.
35. Tsao, M-S. c-MET as a potential therapeutic target and biomarker in cancer. Ther Adv Med Oncol. 2011; 3: S21-S35.
36. Rimassa L, Abbadessa G, Personeni N, Porta C, Borbath I, Daniele B, Van Laethem JL, Van Vlieberghe H, Trojan J, de Toni E, Peck-Radosavljevic M, Finn RS, Raoul JL, et al. Tumor and plasma biomarker analysis from the randomized controlled phase II trial (RCT) of tivantinib in second-line hepatocellular carcinoma (HCC). J Clin Oncol. 2016; 34(suppl 4S): abstr 197.
37. Iveson T, Donehower RC, Davidenko I, Tjulandin S, Deptala A, Harrison M, Nirni, S, Lakshmaiah K, Thomas A, Jiang Y, Zhu M, Tang R, Anderson A, et al. Rilotumumab in combination with epirubicin, cisplatin, and capecitabine as first-line treatment for gastric or oesophagogastric junction adenocarcinoma: an open-label, dose de-escalation phase 1b study and a double-blind, randomised phase 2 study. Lancet Oncol. 2014; 9: 1007-18.
38. Zhu AX, Park JO, Ryoo B-Y, Yen C-J, Poon R, Pastorelli D, Blanc JF, Chung HC, Baron AD, Flesch Pfiffer TE, Okusaka T, Kubackova K, Trojan J, et al. Ramucirumab versus placebo as second-line treatment in patients with advanced hepatocellular carcinoma following first-line therapy with sorafenib (REACH): a randomised, doubleblind, multicentre, phase 3 trial. Lancet Oncol. 2015; 16: 859-70.
39. Zhu AX, Chen D, He W, Kanai M, Voi M, Chen LT. Integrative Biomarker Analyses Indicate Etiological Variations in Hepatocellular Carcinoma. J Hepatol. 2016; 65: 296-304.
40. Llovet JM, Peña CE, Lathia CD, Shan M, Meinhardt G, Bruix J. SHARP Investigators Study Group. Plasma biomarkers as predictors of outcome in patients with advanced hepatocellular carcinoma. Clin Cancer Res. 2012; 18: 2290-300.
41. Llovet JM, Decaens T, Raoul J-L, Boucher E, Kudo M, Chang C, Kang YK, Assenat E, Lim HY, Boige V, Mathurin P, Fartoux L, Lin DY, 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.
42. European Association For The Study Of The Liver; European Organisation For Research And Treatment Of Cancer. EASL-EORTC Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol. 2012; 56: 908-43.
43. Malaguarnera G, Giordano M, I Paladina I, Berretta M, Cappellani A, Malaguarnera M. Serum Markers of Hepatocellular Carcinoma. Dig Dis Sci. 2010; 10: 1184-7.
44. Gomes DA, Rodrigues MA, Leite MF, Gomez MV, Varnai P, Balla T, Bennett AM, Nathanson MH. c-Met must translocate to the nucleus to initiate Ca2+ signals. J Biol Chem. 2008; 283: 4344-51.
45. Bruix J, Merle P, Granito A, Huang Y.-H., Bodoky G, Yokosuka O, Rosmorduc O, Breder V, Gerolami R, Masi G, Paul JR, Qin S, Song T, et al. Efficacy and safety of regorafenib versus placebo in patients with hepatocellular carcinoma (HCC) progressing on sorafenib: results of the international, randomized phase 3 RESORCE trial. Ann Oncol. 2016; 27(suppl 2; abstr LBA-03): ii1-ii3.
46. Shi B, Abrams M, Sepp-Lorenzino L. Expression of Asialoglycoprotein Receptor 1 in Human Hepatocellular Carcinoma. J Histochem and Cytochem. 2013; 61: 901-9.
47. Anderson JR, Cain KC, Gelber RD. Analysis of survival by tumor response. J Clin Oncol. 1983; 1: 710-9.
48. Personeni N, Bozzarelli S, Pressiani T, Rimassa L, Tronconi MC, Sclafani F, Carnaghi C, Pedicini V, Giordano L, Santoro A. Usefulness of alpha-fetoprotein response in patients treated with sorafenib for advanced hepatocellular carcinoma. J Hepatol. 2012; 57: 101-7.