Increased KIT inhibition enhances therapeutic efficacy in gastrointestinal stromal tumor

Clinical Cancer Research

Volumn 20, Issue 9, 2014, Pages 2350-2362

  Kim, Teresa S ^a   Cavnar, Michael J ^a   Cohen, Noah A ^a   Sorenson, Eric C ^a   Greer, Jonathan B ^a   Seifert, Adrian M ^a   Crawley, Megan H ^a   Green, Benjamin L ^a   Popow, Rachel ^a   Pillarsetty, Nagavarakishore ^a   Veach, Darren R ^a   Ku, Anson T ^a   Rossi, Ferdinand ^a   Besmer, Peter ^a   Antonescu, Cristina R ^a   Zeng, Shan ^a   De Matteo, Ronald P ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR; IMATINIB; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLX 3397; PROTEIN TYROSINE KINASE INHIBITOR; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; 5-((5-CHLORO-1H-PYRROLO(2,3-B)PYRIDIN-3-YL)METHYL)-N-((6-(TRIFLUOROMETHYL)PYRIDIN-3-YL)METHYL)PYRIDIN-2-AMINE; AMINOPYRIDINE DERIVATIVE; BENZAMIDE DERIVATIVE; PIPERAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE; STEM CELL FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; FIBROSIS; GASTROINTESTINAL STROMAL TUMOR; HISTOLOGY; HUMAN; IN VITRO STUDY; MACROPHAGE; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOPSY; CELL SURVIVAL; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; GASTROINTESTINAL STROMAL TUMORS; IC50; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TUMOR VOLUME;

AMINOPYRIDINES; ANIMALS; ANTINEOPLASTIC AGENTS; BENZAMIDES; BIOPSY; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; GASTROINTESTINAL STROMAL TUMORS; HUMANS; IMATINIB MESYLATE; INHIBITORY CONCENTRATION 50; MICE, KNOCKOUT; MOLECULAR TARGETED THERAPY; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-KIT; PYRIMIDINES; PYRROLES; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; TUMOR BURDEN;

EID: 84899708388     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-3033     Document Type: Article

References (45)

1. Ducimetiere F, Lurkin A, Ranchere-Vince D, Decouvelaere AV, Peoc'h M, Istier L, et al. Incidence of sarcoma histotypes and molecular subtypes in a prospective epidemiological study with central pathology review and molecular testing. PLoS ONE 2011;6: e20294.
2. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998;279:577-80.
3. Heinrich MC, Corless CL, Duensing A, McGreevey L, Chen CJ, Joseph N, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 2003;299:708-10.
4. DeMatteo RP, Lewis JJ, Leung D, Mudan SS, Woodruff JM, Brennan MF. Two hundred gastrointestinal stromal tumors: recurrence patterns and prognostic factors for survival. Ann Surg 2000;231:51-8.
5. Buchdunger E, Cioffi CL, Law N, Stover D, Ohno-Jones S, Druker BJ, et al. Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 2000;295:139-45.
6. Heinrich MC, Griffith DJ, Druker BJ, Wait CL, Ott KA, Zigler AJ. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 2000;96:925-32.
7. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002;347: 472-80.
8. Verweij J, Casali PG, Zalcberg J, LeCesne A, Reichardt P, Blay JY, et al. Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: randomised trial. Lancet 2004;364:1127-34.
9. Blanke CD, Rankin C, Demetri GD, Ryan CW, von Mehren M, Benjamin RS, 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;26:626-32.
10. Antonescu CR, Besmer P, Guo T, Arkun K, Hom G, Koryotowski B, et al. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 2005;11: 4182-90.
11. Demetri GD, van Oosterom AT, Garrett CR, Blackstein ME, Shah MH, Verweij J, et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 2006;368:1329-38.
12. Demetri GD, Reichardt P, Kang YK, Blay JY, Rutkowski P, Gelderblom H, 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;381:295-302.
13. Rossi F, Yozgat Y, de Stanchina E, Veach D, Clarkson B, Manova K, et al. Imatinib upregulates compensatory integrin signaling in a mouse model of gastrointestinal stromal tumor and is more effective when combined with dasatinib. Mol Cancer Res 2010;8: 1271-83.
14. Balachandran VP, Cavnar MJ, Zeng S, Bamboat ZM, Ocuin LM, Obaid H, et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat Med 2011; 17:1094-100.
15. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1:54-67.
16. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 2013;73:1128-41.
17. van Dongen M, Savage ND, Jordanova ES, Briaire-de Bruijn IH, Walburg KV, Ottenhoff TH, et al. Anti-inflammatory M2 type macrophages characterize metastasized and tyrosine kinase inhibitor-treated gastrointestinal stromal tumors. Int J Cancer 2010;127:899-909.
18. Qian B, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
19. Prada CE, Jousma E, Rizvi TA, Wu J, Dunn RS, Mayes DA, et al. Neurofibroma-associated macrophages play roles in tumor growth and response to pharmacological inhibition. Acta Neuropathol 2013; 125:159-68.
20. Xu J, Escamilla J, Mok S, David J, Priceman S, West B, et al. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res 2013;73:2782-94.
21. Sommer G, Agosti V, Ehlers I, Rossi F, Corbacioglu S, Farkas J, et al. Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci U S A 2003;100:6706-11.
22. Yu W, Chen J, Xiong Y, Pixley FJ, Yeung YG, Stanley ER. Macrophage proliferation is regulated through CSF-1 receptor tyrosines 544, 559, and 807. J Biol Chem 2012;287:13694-704.
23. Zeng S, Feirt N, Goldstein M, Guarrera J, Ippagunta N, Ekong U, et al. Blockade of receptor for advanced glycation end product (RAGE) attenuates ischemia and reperfusion injury to the liver in mice. Hepatology 2004;39:422-32.
24. Taguchi T, Sonobe H, Toyonaga S, Yamasaki I, Shuin T, Takano A, et al. Conventional and molecular cytogenetic characterization of a new human cell line, GIST-T1, established from gastrointestinal stromal tumor. Lab Invest 2002;82:663-5.
25. Rossi F, Ehlers I, Agosti V, Socci ND, Viale A, Sommer G, et al. Oncogenic Kit signaling and therapeutic intervention in a mouse model of gastrointestinal stromal tumor. Proc Natl Acad Sci U S A 2006; 103:12843-8.
26. Deininger M, Buchdunger E, Druker BJ. The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 2005; 105:2640-53.
27. Dewar AL, Cambareri AC, Zannettino AC, Miller BL, Doherty KV, Hughes TP, et al. Macrophage colony-stimulating factor receptor cfms is a novel target of imatinib. Blood 2005;105:3127-32.
28. Logue JS, Morrison DK. Complexity in the signaling network: insights from the use of targeted inhibitors in cancer therapy. Genes Dev 2012;26:641-50.
29. Gupta A, Roy S, Lazar AJ, Wang WL, McAuliffe JC, Reynoso D, et al. Autophagy inhibition and antimalarials promote cell death in gastrointestinal stromal tumor (GIST). Proc Natl Acad Sci U S A 2010;107: 14333-8.
30. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6:392-401.
31. Joensuu H, Roberts PJ, Sarlomo-Rikala M, Andersson LC, Tervahartiala P, Tuveson D, et al. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor.NEngl JMed 2001;344:1052-6.
32. Weinstein IB. Cancer. Addiction to oncogenes-the Achilles heal of cancer. Science 2002;297:63-4.
33. Felsher DW, Bishop JM. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 1999;4:199-207.
34. Jain M, Arvanitis C, Chu K, Dewey W, Leonhardt E, Trinh M, et al. Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 2002;297:102-4.
35. Hoeflich KP, Gray DC, Eby MT, Tien JY, Wong L, Bower J, et al. Oncogenic BRAF is required for tumor growth and maintenance in melanoma models. Cancer Res 2006;66:999-1006.
36. Botchkareva NV, Khlgatian M, Longley BJ, Botchkarev VA, Gilchrest BA. SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit. FASEB J 2001;15:645-58.
37. Nocka K, Majumder S, Chabot B, Ray P, Cervone M, Bernstein A, et al. Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice-evidence for an impaired c-kit kinase in mutant mice. Genes Dev 1989;3:816-26.
38. Anthony SP, Puzanov I, Lin PS, Nolop KB, West B, Von Hoff DD. Pharmacodynamic activity demonstrated in phase I for PLX3397, a selective inhibitor of FMS and Kit. J Clin Oncol 2011;29:suppl; abstr 3093.
39. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer 2006;6:583-92.
40. Agaram NP, Besmer P, Wong GC, Guo T, Socci ND, Maki RG, et al. Pathologic and molecular heterogeneity in imatinib-stable or imatinibresponsive gastrointestinal stromal tumors. Clin Cancer Res 2007; 13:170-81.
41. Chaplin DJ, Durand RE, Olive PL. Cell selection from a murine tumour using the fluorescent probe Hoechst 33342. Br J Cancer 1985;51: 569-72.
42. Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, Jones JO, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010;330:827-30.
43. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012; 21:418-29.
44. Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut 2013;62:112-20.
45. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000;60:2497-503.