Targeting the tumor-promoting microenvironment in METamplified NSCLC cells with a novel inhibitor of pro-HGF activation

Oncotarget

Volumn 8, Issue 38, 2017, Pages 63014-63025

  Owusu, Benjamin Y ^a   Thomas, Shantasia ^a   Venukadasula, Phanindra ^a   Han, Zhenfu ^b   Janetka, James W ^b   Galemmo, Robert A ^a   Klampfer, Lidija ^a  

^a SOUTHERN RESEARCH INSTITUTE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HGF; MET; NSCLC

Indexed keywords

ANTINEOPLASTIC AGENT; HEPSIN; JNJ 38877605; MATRIPTASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE INHIBITOR; SCATTER FACTOR RECEPTOR; SRI 31215; UNCLASSIFIED DRUG;

A-549 CELL LINE; AKT SIGNALING; ARTICLE; BIOLOGICAL ACTIVITY; CELL DEATH; CELL INTERACTION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; EBC-1 CELL LINE; ENZYME ACTIVATION; ENZYME INHIBITION; FIBROBLAST; LUNG NON-SMALL CELL CARCINOMA CELL LINE; MAPK SIGNALING; NCI-H1993 CELL LINE; PROTEIN TARGETING; TUMOR CELL; TUMOR MICROENVIRONMENT;

EID: 85029804762     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.18260     Document Type: Article

References (64)

1. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, Fujii Y, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004; 304:1497-1500
2. Sordella R, Bell DW, Haber DA, Settleman J. Gefitinibsensitizing EGFR mutations in lung cancer activate antiapoptotic pathways. Science. 2004; 305:1163-1167
3. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J, Haber DA. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004; 350:2129-2139
4. Rosell R, Bivona TG, Karachaliou N. Genetics and biomarkers in personalisation of lung cancer treatment. Lancet. 2013; 382:720-731
5. Ayoola A, Barochia A, Belani K, Belani CP. Primary and acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer: an update. Cancer Invest. 2012; 30:433-446
6. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, Johnson BE, Eck MJ, Tenen DG, Halmos B. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005; 352:786-792
7. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, Kris MG, Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005; 2:e73
8. Bean J, Brennan C, Shih JY, Riely G, Viale A, Wang L, Chitale D, Motoi N, Szoke J, Broderick S, Balak M, Chang WC, Yu CJ, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Natl Acad Sci U S A. 2007; 104:20932-20937
9. Camidge DR, Pao W, Sequist LV. Acquired resistance to TKIs in solid tumours: learning from lung cancer. Nat Rev Clin Oncol. 2014; 11:473-481
10. Scagliotti G, von Pawel J, Novello S, Ramlau R, Favaretto A, Barlesi F, Akerley W, Orlov S, Santoro A, Spigel D, Hirsh V, Shepherd FA, Sequist LV, 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; 33:2667-2674
11. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E, Toschi L, Rogers A, Mok T, Sequist L, Lindeman NI, Murphy C, Akhavanfard S, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell. 2010; 17:77-88
12. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007; 316:1039-1043
13. Smolen GA, Sordella R, Muir B, Mohapatra G, Barmettler A, Archibald H, Kim WJ, Okimoto RA, Bell DW, Sgroi DC, Christensen JG, Settleman J, Haber DA. Amplification of MET may identify a subset of cancers with extreme sensitivity to the selective tyrosine kinase inhibitor PHA-665752 Proc Natl Acad Sci U S A. 2006; 103:2316-2321
14. Lutterbach B, Zeng Q, Davis LJ, Hatch H, Hang G, Kohl NE, Gibbs JB, Pan BS. Lung cancer cell lines harboring MET gene amplification are dependent on MET for growth and survival. Cancer Res. 2007; 67:2081-2088
15. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer. 2012; 12:89-103
16. McDermott U, Pusapati RV, Christensen JG, Gray NS, Settleman J. Acquired resistance of non-small cell lung cancer cells to MET kinase inhibition is mediated by a switch to epidermal growth factor receptor dependency. Cancer Res. 2010; 70:1625-1634
17. Zhang YW, Staal B, Essenburg C, Lewis S, Kaufman D, Vande Woude GF. Strengthening context-dependent anticancer effects on non-small cell lung carcinoma by inhibition of both MET and EGFR. Mol Cancer Ther. 2013; 12:1429-1441
18. Presutti D, Santini S, Cardinali B, Papoff G, Lalli C, Samperna S, Fustaino V, Giannini G, Ruberti G. MET gene amplification and MET receptor activation are not sufficient to predict efficacy of combined MET and EGFR inhibitors in EGFR TKI-resistant NSCLC cells. PLoS One. 2015; 10:e0143333
19. Klemm F, Joyce JA. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 2015; 25:198-213
20. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, Davis A, Mongare MM, Gould J, Frederick DT, Cooper ZA, Chapman PB, Solit DB, et al. Tumour microenvironment elicits innate resistance to RAF inhibitors through HGF secretion. Nature. 2012; 487:500-504
21. Junttila MR, de Sauvage FJ. Influence of tumour microenvironment heterogeneity on therapeutic response. Nature. 2013; 501:346-354
22. Donev IS, Wang W, Yamada T, Li Q, Takeuchi S, Matsumoto K, Yamori T, Nishioka Y, Sone S, Yano S. Transient PI3K inhibition induces apoptosis and overcomes HGF-mediated resistance to EGFR-TKIs in EGFR mutant lung cancer. Clin Cancer Res. 2011; 17:2260-2269
23. Wang W, Li Q, Yamada T, Matsumoto K, Matsumoto I, Oda M, Watanabe G, Kayano Y, Nishioka Y, Sone S, Yano S. Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clin Cancer Res. 2009; 15:6630-6638
24. Arrieta O, Cruz-Rico G, Soto-Perez-de-Celis E, Ramirez-Tirado LA, Caballe-Perez E, Martinez-Hernandez JN, Martinez-Alvarez I, Soca-Chafre G, Macedo-Perez EO, Astudillo-de la Vega H. Reduction in hepatocyte growth factor serum levels is associated with improved prognosis in advanced lung adenocarcinoma patients treated with afatinib: a phase II trial. Targeted Oncol. 2016; 11:619-629
25. Kasahara K, Arao T, Sakai K, Matsumoto K, Sakai A, Kimura H, Sone T, Horiike A, Nishio M, Ohira T, Ikeda N, Yamanaka T, Saijo N, Nishio K. Impact of serum hepatocyte growth factor on treatment response to epidermal growth factor receptor tyrosine kinase inhibitors in patients with non-small cell lung adenocarcinoma. Clin Cancer Res. 2010; 16:4616-4624
26. Pennacchietti S, Cazzanti M, Bertotti A, Rideout WM 3rd, Han M, Gyuris J, Perera T, Comoglio PM, Trusolino L, Michieli P. Microenvironment-derived HGF overcomes genetically determined sensitivity to anti-MET drugs. Cancer Res. 2014; 74:6598-6609
27. Patnaik A, Weiss GJ, Papadopoulos KP, Hofmeister CC, Tibes R, Tolcher A, Isaacs R, Jac J, Han M, Payumo FC, Cotreau MM, Ramanathan RK. Phase I ficlatuzumab monotherapy or with erlotinib for refractory advanced solid tumours and multiple myeloma. Br J Cancer. 2014; 111:272-280
28. Tabernero J, Elez ME, Herranz M, Rico I, Prudkin L, Andreu J, Mateos J, Carreras MJ, Han M, Gifford J, Credi M, Yin W, Agarwal S, et al. A pharmacodynamic/ pharmacokinetic study of ficlatuzumab in patients with advanced solid tumors and liver metastases. Clin Cancer Res. 2014; 20:2793-2804
29. Han Z, Harris PK, Karmakar P, Kim T, Owusu BY, Wildman SA, Klampfer L, Janetka JW. a-Ketobenzothiazole serine protease inhibitors of aberrant HGF/c-MET and MSP/RON kinase pathway signaling in cancer. ChemMedChem. 2016; 11:585-599
30. Venukadasula PK, Owusu BY, Bansal N, Ross LJ, Hobrath JV, Bao D, Truss JW, Stackhouse M, Messick TE, Klampfer L, Galemmo RA Jr. Design and synthesis of nonpeptide inhibitors of hepatocyte growth factor activation. ACS Med Chem Lett. 2016; 7:177-181
31. Kawaguchi M, Kataoka H. Mechanisms of hepatocyte growth factor activation in cancer tissues. Cancers (Basel). 2014; 6:1890-1904
32. Mazzone M, Basilico C, Cavassa S, Pennacchietti S, Risio M, Naldini L, Comoglio PM, Michieli P. An uncleavable form of pro-scatter factor suppresses tumor growth and dissemination in mice. J Clin Invest. 2004; 114:1418-1432
33. Michieli P, Mazzone M, Basilico C, Cavassa S, Sottile A, Naldini L, Comoglio PM. Targeting the tumor and its microenvironment by a dual-function decoy Met receptor. Cancer Cell. 2004; 6:61-73
34. Matsumoto K, Nakamura T. Mechanisms and significance of bifunctional NK4 in cancer treatment. Biochem Biophys Res Commun. 2005; 333:316-327
35. Murakami M, Nagai E, Mizumoto K, Saimura M, Ohuchida K, Inadome N, Matsumoto K, Nakamura T, Maemondo M, Nukiwa T, Tanaka M. Suppression of metastasis of human pancreatic cancer to the liver by transportal injection of recombinant adenoviral NK4 in nude mice. Int J Cancer. 2005; 117:160-165
36. Owusu BY, Bansal N, Venukadasula PK, Ross LJ, Messick TE, Goel S, Galemmo RA, Klampfer L. Inhibition of pro-HGF activation by SRI31215, a novel approach to block oncogenic HGF/MET signaling. Oncotarget. 2016; 7:29492-29506. doi: 10.18632/oncotarget.8785
37. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, Peng J, Lin E, Wang Y, Sosman J, Ribas A, Li J, Moffat J, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature. 2012; 487:505-509
38. Graveel CR, Tolbert D, Vande Woude GF. MET: a critical player in tumorigenesis and therapeutic target. Cold Spring Harb Perspect Biol. 2013; 5:a009209
39. Tanizaki J, Okamoto I, Sakai K, Nakagawa K. Differential roles of trans-phosphorylated EGFR, HER2, HER3, and RET as heterodimerisation partners of MET in lung cancer with MET amplification. Br J Cancer. 2011; 105:807-813
40. Moniz S, Jordan P. Emerging roles for WNK kinases in cancer. Cell Mol Life Sci. 2010; 67:1265-1276
41. Russo A, Franchina T, Ricciardi GR, Picone A, Ferraro G, Zanghi M, Toscano G, Giordano A, Adamo V. A decade of EGFR inhibition in EGFR-mutated non small cell lung cancer (NSCLC): Old successes and future perspectives. Oncotarget. 2015; 6:26814-26825. doi: 10.18632/ oncotarget.4254
42. Boolell V, Alamgeer M, Watkins DN, Ganju V. The evolution of therapies in non-small cell lung cancer. Cancers (Basel). 2015; 7:1815-1846
43. Tan CS, Gilligan D, Pacey S. Treatment approaches for EGFR-inhibitor-resistant patients with non-small-cell lung cancer. Lancet Oncol. 2015; 16:e447-e459
44. Yamaoka T, Ohmori T, Ohba M, Arata S, Kishino Y, Murata Y, Kusumoto S, Ishida H, Shirai T, Hirose T, Ohnishi T, Sasaki Y. Acquired resistance mechanisms to combination Met-TKI/EGFR-TKI exposure in Met-amplified EGFR-TKI resistant lung adenocarcinoma harboring an activating egfr mutation. Mol Cancer Ther. 2016; 15:3040-3054
45. Bahcall M, Sim T, Paweletz CP, Patel JD, Alden RS, Kuang Y, Sacher AG, Kim ND, Lydon C, Awad MM, Jaklitsch MT, Sholl LM, Janne PA, Oxnard GR. Acquired MET D1228V mutation and resistance to MET inhibition in lung cancer. Cancer Discov. 2016; 6:1334-1341
46. Tanaka H, Kimura T, Kudoh S, Mitsuoka S, Watanabe T, Suzumura T, Tachibana K, Noguchi M, Yano S, Hirata K. Reaction of plasma hepatocyte growth factor levels in nonsmall cell lung cancer patients treated with EGFR-TKIs. Int J Cancer. 2011; 129:1410-1416
47. Chen JT, Lin TS, Chow KC, Huang HH, Chiou SH, Chiang SF, Chen HC, Chuang TL, Lin TY, Chen CY. Cigarette smoking induces overexpression of hepatocyte growth factor in type II pneumocytes and lung cancer cells. Am J Respir Cell Mol Biol. 2006; 34:264-273
48. Van Cutsem E, Eng C, Nowara E, Swieboda-Sadlej A, Tebbutt NC, Mitchell E, Davidenko I, Stephenson J, Elez E, Prenen H, Deng H, Tang R, McCaffery I, et al. Randomized phase Ib/II trial of rilotumumab or ganitumab with panitumumab versus panitumumab alone in patients with wild-type KRAS metastatic colorectal cancer. Clinical Cancer Res. 2014; 20:4240-4250
49. Martin LP, Sill M, Shahin MS, Powell M, DiSilvestro P, Landrum LM, Gaillard SL, Goodheart MJ, Hoffman J, Schilder RJ. A phase II evaluation of AMG 102 (rilotumumab) in the treatment of persistent or recurrent epithelial ovarian, fallopian tube or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol. 2014; 132:526-530
50. Gordon MS, Sweeney CS, Mendelson DS, Eckhardt SG, Anderson A, Beaupre DM, Branstetter D, Burgess TL, Coxon A, Deng H, Kaplan-Lefko P, Leitch IM, Oliner KS, et al. Safety, pharmacokinetics, and pharmacodynamics of AMG 102, a fully human hepatocyte growth factorneutralizing monoclonal antibody, in a first-in-human study of patients with advanced solid tumors. Clinical Cancer Res. 2010; 16:699-710
51. Rosen PJ, Sweeney CJ, Park DJ, Beaupre DM, Deng H, Leitch IM, Shubhakar P, Zhu M, Oliner KS, Anderson A, Yee LK. A phase Ib study of AMG 102 in combination with bevacizumab or motesanib in patients with advanced solid tumors. Clin Cancer Res. 2010; 16:2677-2687
52. Imai K, Takaoka A. Comparing antibody and smallmolecule therapies for cancer. Nat Rev Cancer. 2006; 6:714-727
53. Kawaguchi M, Takeda N, Hoshiko S, Yorita K, Baba T, Sawaguchi A, Nezu Y, Yoshikawa T, Fukushima T, Kataoka H. Membrane-bound serine protease inhibitor HAI-1 is required for maintenance of intestinal epithelial integrity. Am J Pathol. 2011; 179:1815-1826
54. Hoshiko S, Kawaguchi M, Fukushima T, Haruyama Y, Yorita K, Tanaka H, Seiki M, Inatsu H, Kitamura K, Kataoka H. Hepatocyte growth factor activator inhibitor type 1 is a suppressor of intestinal tumorigenesis. Cancer Res. 2013; 73:2659-2670
55. Saleem M, Adhami VM, Zhong W, Longley BJ, Lin CY, Dickson RB, Reagan-Shaw S, Jarrard DF, Mukhtar H. A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol Biomarkers Prev. 2006; 15:217-227
56. Oberst MD, Johnson MD, Dickson RB, Lin CY, Singh B, Stewart M, Williams A, al-Nafussi A, Smyth JF, Gabra H, Sellar GC. Expression of the serine protease matriptase and its inhibitor HAI-1 in epithelial ovarian cancer: correlation with clinical outcome and tumor clinicopathological parameters. Clinical Cancer Res. 2002; 8:1101-1107
57. Zeng L, Cao J, Zhang X. Expression of serine protease SNC19/matriptase and its inhibitor hepatocyte growth factor activator inhibitor type 1 in normal and malignant tissues of gastrointestinal tract. World J Gastroenterol. 2005; 11:6202-6207
58. Nakamura K, Abarzua F, Kodama J, Hongo A, Nasu Y, Kumon H, Hiramatsu Y. Expression of hepatocyte growth factor activator inhibitors (HAI-1 and HAI-2) in ovarian cancer. Int J Oncol. 2009; 34:345-353
59. Hamasuna R, Kataoka H, Meng JY, Itoh H, Moriyama T, Wakisaka S, Koono M. Reduced expression of hepatocyte growth factor activator inhibitor type-2/placental bikunin (HAI-2/PB) in human glioblastomas: implication for antiinvasive role of HAI-2/PB in glioblastoma cells. Int J Cancer. 2001; 93:339-345
60. Morris MR, Gentle D, Abdulrahman M, Maina EN, Gupta K, Banks RE, Wiesener MS, Kishida T, Yao M, Teh B, Latif F, Maher ER. Tumor suppressor activity and epigenetic inactivation of hepatocyte growth factor activator inhibitor type 2/SPINT2 in papillary and clear cell renal cell carcinoma. Cancer Res. 2005; 65:4598-4606
61. Pupo E, Ducano N, Lupo B, Vigna E, Avanzato D, Perera T, Trusolino L, Lanzetti L, Comoglio PM. Rebound effects caused by withdrawal of MET kinase inhibitor are quenched by a MET therapeutic antibody. Cancer Res. 2016; 76:5019-5029
62. Finisguerra V, Prenen H, Mazzone M. Preclinical and clinical evaluation of MET functions in cancer cells and in the tumor stroma. Oncogene. 2016; 35:5457-5467
63. Landi MT, Dracheva T, Rotunno M, Figueroa JD, Liu H, Dasgupta A, Mann FE, Fukuoka J, Hames M, Bergen AW, Murphy SE, Yang P, Pesatori AC, et al. Gene expression signature of cigarette smoking and its role in lung adenocarcinoma development and survival. PLoS One. 2008; 3:e1651
64. Beer DG, Kardia SL, Huang CC, Giordano TJ, Levin AM, Misek DE, Lin L, Chen G, Gharib TG, Thomas DG, Lizyness ML, Kuick R, Hayasaka S, et al. Geneexpression profiles predict survival of patients with lung adenocarcinoma. Nat Med. 2002; 8:816-824