Systemic therapy of advanced/metastatic gastrointestinal stromal tumors: an update on progress beyond imatinib, sunitinib, and regorafenib

References

• Verschoor AJ, Bovee J, Overbeek LIH, et al. The incidence, mutational status, risk classification and referral pattern of gastro-intestinal stromal tumours in the Netherlands: a nationwide pathology registry (PALGA) study. Virchows Arch. 2018;472(2):221–229.
   PubMed Web of Science ®Google Scholar
• Soreide K, Sandvik OM, Soreide JA, et al. Global epidemiology of gastrointestinal stromal tumours (GIST): a systematic review of population-based cohort studies. Cancer Epidemiol. 2016;40:39–46.
   PubMed Web of Science ®Google Scholar
• Hirota S, Isozaki K, Moriyama Y, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science. 1998;279(5350):577–580.
   PubMed Web of Science ®Google Scholar
• Heinrich MC, Corless CL, Duensing A, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science. 2003;299(5607):708–710.
   PubMed Web of Science ®Google Scholar
• DeMatteo RP, Lewis JJ, Leung D, et al. Two hundred gastrointestinal stromal tumors: recurrence patterns and prognostic factors for survival. Ann Surg. 2000;231(1):51–58.
   PubMed Web of Science ®Google Scholar
• Joensuu H, Roberts PJ, Sarlomo-Rikala M, et al. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N Engl J Med. 2001;344(14):1052–1056.
   PubMed Web of Science ®Google Scholar
• van Oosterom AT, Judson I, Verweij J, et al. Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumours: a phase I study. Lancet. 2001;358(9291):1421–1423.
   PubMed Web of Science ®Google Scholar
• Demetri GD, von Mehren M, Blanke CD, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med. 2002;347(7):472–480.
   PubMed Web of Science ®Google Scholar
• Verweij J, van Oosterom A, Blay JY, et al. Imatinib mesylate (STI-571 Glivec, Gleevec) is an active agent for gastrointestinal stromal tumours, but does not yield responses in other soft-tissue sarcomas that are unselected for a molecular target. Results from an EORTC soft tissue and bone sarcoma group phase II study. Eur J Cancer. 2003;39(14):2006–2011.
   PubMed Web of Science ®Google Scholar
• Verweij J, Casali PG, Zalcberg J, et al. Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: randomised trial. Lancet. 2004;364(9440):1127–1134.
   PubMed Web of Science ®Google Scholar
• Blanke CD, Rankin C, Demetri GD, et al. Phase III randomized, intergroup trial assessing imatinib mesylate at two dose levels in patients with unresectable or metastatic gastrointestinal stromal tumors expressing the kit receptor tyrosine kinase: S0033. J Clin Oncol. 2008;26(4):626–632.
   PubMed Web of Science ®Google Scholar
• Gastrointestinal Stromal Tumor Meta-Analysis G. Comparison of two doses of imatinib for the treatment of unresectable or metastatic gastrointestinal stromal tumors: a meta-analysis of 1,640 patients. J Clin Oncol. 2010;28(7):1247–1253.
   PubMed Web of Science ®Google Scholar
• Casali PG, Zalcberg J, Le Cesne A, et al. Ten-year progression-free and overall survival in patients with unresectable or metastatic GI stromal tumors: long-term analysis of the european organisation for research and treatment of cancer, Italian Sarcoma Group, and Australasian gastrointestinal trials group intergroup phase III randomized trial on imatinib at two dose levels. J Clin Oncol. 2017;35(15):1713–1720.
   PubMed Web of Science ®Google Scholar
• Antonescu CR, Besmer P, Guo T, et al. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res. 2005;11(11):4182–4190.
   PubMed Web of Science ®Google Scholar
• Liegl B, Kepten I, Le C, et al. Heterogeneity of kinase inhibitor resistance mechanisms in GIST. J Pathol. 2008;216(1):64–74.
   PubMed Web of Science ®Google Scholar
• Gramza AW, Corless CL, Heinrich MC. Resistance to tyrosine kinase inhibitors in gastrointestinal stromal tumors. Clin Cancer Res. 2009;15(24):7510–7518.
   PubMed Web of Science ®Google Scholar
• Demetri GD, van Oosterom AT, Garrett CR, et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet. 2006;368(9544):1329–1338.
   PubMed Web of Science ®Google Scholar
• George S, Blay JY, Casali PG, et al. Clinical evaluation of continuous daily dosing of sunitinib malate in patients with advanced gastrointestinal stromal tumour after imatinib failure. Eur J Cancer. 2009;45(11):1959–1968.
   PubMed Web of Science ®Google Scholar
• Demetri GD, Reichardt P, Kang YK, et al. Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet. 2013;381(9863):295–302.
   PubMed Web of Science ®Google Scholar
• Montemurro M, Schoffski P, Reichardt P, et al. Nilotinib in the treatment of advanced gastrointestinal stromal tumours resistant to both imatinib and sunitinib. Eur J Cancer. 2009;45(13):2293–2297.
   PubMed Web of Science ®Google Scholar
• Sawaki A, Nishida T, Doi T, et al. Phase 2 study of nilotinib as third-line therapy for patients with gastrointestinal stromal tumor. Cancer. 2011;117(20):4633–4641.
   PubMed Web of Science ®Google Scholar
• Reichardt P, Blay JY, Gelderblom H, et al. Phase III study of nilotinib versus best supportive care with or without a TKI in patients with gastrointestinal stromal tumors resistant to or intolerant of imatinib and sunitinib. Ann Oncol. 2012;23(7):1680–1687.
   PubMed Web of Science ®Google Scholar
• Heinrich MC, Marino-Enriquez A, Presnell A, et al. Sorafenib inhibits many kinase mutations associated with drug-resistant gastrointestinal stromal tumors. Mol Cancer Ther. 2012;11(8):1770–1780.
   PubMed Web of Science ®Google Scholar
• Wilhelm SM, Carter C, Tang L, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 2004;64(19):7099–7109.
   PubMed Web of Science ®Google Scholar
• Montemurro M, Gelderblom H, Bitz U, et al. Sorafenib as third- or fourth-line treatment of advanced gastrointestinal stromal tumour and pretreatment including both imatinib and sunitinib, and nilotinib: a retrospective analysis. Eur J Cancer. 2013;49(5):1027–1031.
   PubMed Web of Science ®Google Scholar
• Park SH, Ryu MH, Ryoo BY, et al. Sorafenib in patients with metastatic gastrointestinal stromal tumors who failed two or more prior tyrosine kinase inhibitors: a phase II study of Korean gastrointestinal stromal tumors study group. Invest New Drugs. 2012;30(6):2377–2383.
   PubMed Web of Science ®Google Scholar
• Kindler HL, Campbell NP, Wroblewski K, et al. Sorafenib (SOR) in patients (pts) with imatinib (IM) and sunitinib (SU)-resistant (RES) gastrointestinal stromal tumors (GIST): final results of a University of Chicago Phase II Consortium trial. J clin oncol. 2011;29(15). DOI:10.1200/jco.2011.29.15_suppl.10009
   PubMed Web of Science ®Google Scholar
• Ganjoo KN, Villalobos VM, Kamaya A, et al. A multicenter phase II study of pazopanib in patients with advanced gastrointestinal stromal tumors (GIST) following failure of at least imatinib and sunitinib. Ann Oncol. 2014;25(1):236–240.
   PubMed Web of Science ®Google Scholar
• Mir O, Cropet C, Toulmonde M, et al. Pazopanib plus best supportive care versus best supportive care alone in advanced gastrointestinal stromal tumours resistant to imatinib and sunitinib (PAZOGIST): a randomised, multicentre, open-label phase 2 trial. Lancet Oncol. 2016;17(5):632–641.
   PubMed Web of Science ®Google Scholar
• Schoffski P, Mir O, Kasper B, et al. Activity and safety of the multi-target tyrosine kinase inhibitor cabozantinib in patients with metastatic gastrointestinal stromal tumour after treatment with imatinib and sunitinib: European Organisation for Research and Treatment of Cancer phase II trial 1317 ‘CaboGIST’. Eur J Cancer. 2020;134:62–74.
   PubMed Web of Science ®Google Scholar
• Duensing A, Heinrich MC, Fletcher CD, et al. Biology of gastrointestinal stromal tumors: KIT mutations and beyond. Cancer Invest. 2004;22(1):106–116.
   PubMed Web of Science ®Google Scholar
• Wozniak A, Gebreyohannes YK, Debiec-Rychter M, et al. New targets and therapies for gastrointestinal stromal tumors. Expert Rev Anticancer Ther. 2017;17(12):1117–1129.
   PubMed Web of Science ®Google Scholar
• Van Looy T, Wozniak A, Floris G, et al. Phosphoinositide 3-kinase inhibitors combined with imatinib in patient-derived xenograft models of gastrointestinal stromal tumors: rationale and efficacy. Clin Cancer Res. 2014;20(23):6071–6082.
   PubMed Web of Science ®Google Scholar
• Gelderblom H, Jones RL, George S, et al. Imatinib in combination with phosphoinositol kinase inhibitor buparlisib in patients with gastrointestinal stromal tumour who failed prior therapy with imatinib and sunitinib: a Phase 1b, multicentre study. Br J Cancer. 2020;122(8):1158–1165.
   PubMed Web of Science ®Google Scholar
• O’Hare T, Walters DK, Stoffregen EP, et al. In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 against clinically relevant imatinib-resistant Abl kinase domain mutants. Cancer Res. 2005;65(11):4500–4505.
   PubMed Web of Science ®Google Scholar
• Shah NP, Tran C, Lee FY, et al. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004;305(5682):399–401.
   PubMed Web of Science ®Google Scholar
• Jabbour E, Kantarjian HM, Saglio G, et al. Early response with dasatinib or imatinib in chronic myeloid leukemia: 3-year follow-up from a randomized phase 3 trial (DASISION). Blood. 2014;123(4):494–500.
   PubMed Web of Science ®Google Scholar
• Shah NP, Guilhot F, Cortes JE, et al. Long-term outcome with dasatinib after imatinib failure in chronic-phase chronic myeloid leukemia: follow-up of a phase 3 study. Blood. 2014;123(15):2317–2324.
   PubMed Web of Science ®Google Scholar
• Montemurro M, Cioffi A, Domont J, et al. Long-term outcome of dasatinib first-line treatment in gastrointestinal stromal tumor: a multicenter, 2-stage phase 2 trial (Swiss Group for Clinical Cancer Research 56/07). Cancer. 2018;124(7):1449–1454.
   PubMed Web of Science ®Google Scholar
• Li J, Zhou Y, Zhang X, et al. Safety and efficacy of dasatinib in patients with advanced gastrointestinal stromal tumors refractory to imatinib and sunitinib: a single arm, multicenters, phase 2 trial. J clin oncol. 2019;37(4_suppl):138.
   Web of Science ®Google Scholar
• Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005;5(10):761–772.
   PubMed Web of Science ®Google Scholar
• Bauer S, Yu LK, Demetri GD, et al. Heat shock protein 90 inhibition in imatinib-resistant gastrointestinal stromal tumor. Cancer Res. 2006;66(18):9153–9161.
   PubMed Web of Science ®Google Scholar
• Smyth T, Van Looy T, Curry JE, et al. The HSP90 inhibitor, AT13387, is effective against imatinib-sensitive and -resistant gastrointestinal stromal tumor models. Mol Cancer Ther. 2012;11(8):1799–1808.
   PubMed Web of Science ®Google Scholar
• Doi T, Kurokawa Y, Sawaki A, et al. Efficacy and safety of TAS-116, an oral inhibitor of heat shock protein 90, in patients with metastatic or unresectable gastrointestinal stromal tumour refractory to imatinib, sunitinib and regorafenib: a phase II, single-arm trial. Eur J Cancer. 2019;121:29–39.
   PubMed Web of Science ®Google Scholar
• Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem. 2011;149(2):121–130.
   PubMed Web of Science ®Google Scholar
• Tanner Y, Grose RP. Dysregulated FGF signalling in neoplastic disorders. Semin Cell Dev Biol. 2016;53:126–135.
   PubMed Web of Science ®Google Scholar
• Shi E, Chmielecki J, Tang CM, et al. FGFR1 and NTRK3 actionable alterations in “Wild-Type” gastrointestinal stromal tumors. J Transl Med. 2016;14(1):339.
   PubMedGoogle Scholar
• Urbini M, Indio V, Tarantino G, et al. Gain of FGF4 is a frequent event in KIT/PDGFRA/SDH/RAS-P WT GIST. Genes Chromosomes Cancer. 2019;58(9):636–642.
   PubMed Web of Science ®Google Scholar
• Kelly CM, Shoushtari AN, Qin LX, et al. A phase Ib study of BGJ398, a pan-FGFR kinase inhibitor in combination with imatinib in patients with advanced gastrointestinal stromal tumor. Invest New Drugs. 2019;37(2):282–290.
   PubMed Web of Science ®Google Scholar
• Vaishnavi A, Capelletti M, Le AT, et al. Oncogenic and drug-sensitive NTRK1 rearrangements in lung cancer. Nat Med. 2013;19(11):1469–1472.
   PubMed Web of Science ®Google Scholar
• Tognon C, Knezevich SR, Huntsman D, et al. Expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell. 2002;2(5):367–376.
   PubMed Web of Science ®Google Scholar
• Drilon A, Laetsch TW, Kummar S, et al. Efficacy of Larotrectinib in TRK Fusion-Positive Cancers in Adults and Children. N Engl J Med. 2018;378(8):731–739
   Google Scholar
• Balachandran VP, Cavnar MJ, Zeng S, et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat Med. 2011;17(9):1094–U1099.
   PubMed Web of Science ®Google Scholar
• Ksienski D. Imatinib mesylate: past successes and future challenges in the treatment of gastrointestinal stromal tumors. Clin Med Insights Oncol. 2011;5:365–379.
   PubMedGoogle Scholar
• Gajiwala KS, Wu JC, Christensen J, et al. KIT kinase mutants show unique mechanisms of drug resistance to imatinib and sunitinib in gastrointestinal stromal tumor patients. Proc Natl Acad Sci U S A. 2009;106(5):1542–1547.
   PubMed Web of Science ®Google Scholar
• Smith BD, Kaufman MD, Lu WP, et al. Ripretinib (DCC-2618) is a switch control kinase inhibitor of a broad spectrum of oncogenic and drug-resistant KIT and PDGFRA variants. Cancer Cell. 2019;35(5):738–751 e739.
   PubMed Web of Science ®Google Scholar
• Schneeweiss M, Peter B, Bibi S, et al. The KIT and PDGFRA switch-control inhibitor DCC-2618 blocks growth and survival of multiple neoplastic cell types in advanced mastocytosis. Haematologica. 2018;103(5):799–809.
   PubMed Web of Science ®Google Scholar
• Schneeweiss MA, Peter B, Blatt K, et al. The multi-kinase inhibitor DCC-2618 inhibits proliferation and survival of neoplastic mast cells and other cell types involved in systemic mastocytosis. Blood. 2016;128(22):1965.
   Web of Science ®Google Scholar
• Janku F, Abdul Razak AR, Chi P, et al. Switch control inhibition of KIT and PDGFRA in patients with advanced gastrointestinal stromal tumor: a phase I study of ripretinib. J Clin Oncol. 2020;38(28):3294–3303.
   PubMed Web of Science ®Google Scholar
• Blay JY, Serrano C, Heinrich MC, et al. Ripretinib in patients with advanced gastrointestinal stromal tumours (INVICTUS): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol. 2020;21(7):923–934.
   PubMed Web of Science ®Google Scholar
• Evans EK, Gardino AK, Kim JL, et al. A precision therapy against cancers driven by KIT/PDGFRA mutations. Sci Transl Med. 2017;9:414.
   Web of Science ®Google Scholar
• Gebreyohannes YK, Wozniak A, Zhai ME, et al. Robust activity of avapritinib, potent and highly selective inhibitor of mutated KIT, in patient-derived xenograft models of gastrointestinal stromal tumors. Clin Cancer Res. 2019;25(2):609–618.
   PubMed Web of Science ®Google Scholar
• Corless CL, Barnett CM, Heinrich MC. Gastrointestinal stromal tumours: origin and molecular oncology. Nat Rev Cancer. 2011;11(12):865–878.
   PubMed Web of Science ®Google Scholar
• Heinrich MC, Jones RL, von Mehren M, et al. Avapritinib in advanced PDGFRA D842V-mutant gastrointestinal stromal tumour (NAVIGATOR): a multicentre, open-label, phase 1 trial. Lancet Oncol. 2020;21(7):935–946.
   PubMed Web of Science ®Google Scholar
• Corporation BM. Blueprint medicines announces top-line results from phase 3 VOYAGER trial of avapritinib versus regorafenib in patients with advanced gastrointestinal stromal tumor. 2020.
   Google Scholar
• Patrikidou A, Chabaud S, Ray-Coquard I, et al. Influence of imatinib interruption and rechallenge on the residual disease in patients with advanced GIST: results of the BFR14 prospective French Sarcoma Group randomised, phase III trial. Ann Oncol. 2013;24(4):1087–1093.
   PubMed Web of Science ®Google Scholar
• Ray-Coquard I, Bui N, Adenis A. Risk of relapse with imatinib (IM) discontinuation at 5 years in advanced GIST patients: results of the prospective BFR14 randomized phase III study comparing interruption versus continuation of IM at 5 years of treatment: a French Sarcoma Group Study. J clin oncol. 2010;28:10032.
   PubMed Web of Science ®Google Scholar
• Yop D, Zalcberg JR, Blay JY, et al. ALT-GIST: randomised phase II trial of imatinib alternating with regorafenib vs imatinib alone for the first line treatment of metastatic gastrointestinal stromal tumor (GIST). ASCO. 2019;Chicago:2019.
   Google Scholar
• Serrano C, Marino-Enriquez A, Tao DL, et al. Complementary activity of tyrosine kinase inhibitors against secondary kit mutations in imatinib-resistant gastrointestinal stromal tumours. Br J Cancer. 2019;120(6):612–620.
   PubMed Web of Science ®Google Scholar
• Serrano C, Leal A, Kuang Y, et al. Phase I study of rapid alternation of sunitinib and regorafenib for the treatment of tyrosine kinase inhibitor refractory gastrointestinal stromal tumors. Clin Cancer Res. 2019;25(24):7287–7293.
   PubMed Web of Science ®Google Scholar