Epidermal growth factor-receptor activation modulates Src-dependent resistance to lapatinib in breast cancer models

Breast Cancer Research

Volumn 16, Issue 3, 2014, Pages

  Formisano, Luigi ^a   Nappi, Lucia ^a   Rosa, Roberta ^a   Marciano, Roberta ^a   D'Amato, Claudia ^a   D'Amato, Valentina ^a   Damiano, Vincenzo ^a   Raimondo, Lucia ^a   Iommelli, Francesca ^b   Scorziello, Antonella ^a   Troncone, Giancarlo ^a   Veneziani, Bianca M ^a   Parsons, Sarah J ^c   De Placido, Sabino ^a   Bianco, Roberto ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; LAPATINIB; PROTEIN TYROSINE KINASE; SARACATINIB; TRASTUZUMAB; 1,3 BENZODIOXOLE DERIVATIVE; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER RESISTANCE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TREATMENT DURATION; TUMOR INVASION; WESTERN BLOTTING; WOUND HEALING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CANCER TRANSPLANTATION; CELL MOTION; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SECONDARY; TUMOR CELL LINE; XENOGRAFT; CANCER COMBINATION CHEMOTHERAPY; CHEMOSENSITIVITY; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GROWTH INHIBITION; IC50; LUNG METASTASIS; METASTASIS; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BENZODIOXOLES; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSPLANTATION, HETEROLOGOUS;

EID: 84902116278     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3650     Document Type: Article

References (47)

1. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001, 2:127-137. 10.1038/35052073, 11252954.
2. Moasser MM. The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene 2007, 26:6469-6487. 10.1038/sj.onc.1210477, 3021475, 17471238.
3. Moasser MM. Targeting the function of the HER2 oncogene in human cancer therapeutics. Oncogene 2007, 26:6577-6592. 10.1038/sj.onc.1210478, 3071580, 17486079.
4. Burris HA. Overcoming acquired resistance to anticancer therapy: focus on the PI3K/AKT/mTOR pathway. Cancer Chemother Pharmacol 2013, Epub ahead of print.
5. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh DY, Diéras V, Guardino E, Fang L, Lu MW, Olsen S, Blackwell K, EMILIA Study Group Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012, 367:1783-1791. 10.1056/NEJMoa1209124, 23020162, EMILIA Study Group.
6. Rusnak DW, Affleck K, Cockerill SG, Stubberfield C, Harris R, Page M, Smith KJ, Guntrip SB, Carter MC, Shaw RJ, Jowett A, Stables J, Topley P, Wood ER, Brignola PS, Kadwell SH, Reep BR, Mullin RJ, Alligood KJ, Keith BR, Crosby RM, Murray DM, Knight WB, Gilmer TM, Lackey K. The characterization of novel, dual ErbB-2/EGFR, tyrosine kinase inhibitors: potential therapy for cancer. Cancer Res 2001, 61:7196-7203.
7. Rusnak DW, Lackey K, Affleck K, Wood ER, Alligood KJ, Rhodes N, Keith BR, Murray DM, Knight WB, Mullin RJ, Gilmer TM. The effects of the novel, reversible epidermal growth factor receptor/ErbB-2 tyrosine kinase inhibitor, GW2016, on the growth of human normal and tumor-derived cell lines in vitro and in vivo. Mol Cancer Ther 2001, 1:85-94.
8. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B, Skarlos D, Campone M, Davidson N, Berger M, Oliva C, Rubin SD, Stein S, Cameron D. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006, 355:2733-2743. 10.1056/NEJMoa064320, 17192538.
9. Scaltriti M, Chandarlapaty S, Prudkin L, Aura C, Jimenez J, Angelini PD, Sánchez G, Guzman M, Parra JL, Ellis C, Gagnon R, Koehler M, Gomez H, Geyer C, Cameron D, Arribas J, Rosen N, Baselga J. Clinical benefit of lapatinib-based therapy in patients with human epidermal growth factor receptor 2-positive breast tumors coexpressing the truncated p95HER2 receptor. Clin Cancer Res 2010, 16:2688-2695. 10.1158/1078-0432.CCR-09-3407, 3243489, 20406840.
10. Rexer BN, Arteaga CL. Intrinsic and acquired resistance to HER2-targeted therapies in HER2 gene-amplified breast cancer: mechanisms and clinical implications. Crit Rev Oncol 2012, 17:1-16.
11. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004, 4:470-480. 10.1038/nrc1366, 15170449.
12. Playford MP, Vadali K, Cai X. Focal adhesion kinase regulates cell-cell contact formation in epithelial cells via modulation of Rho. Exp Cell Res 2008, 314:3187-3197. 10.1016/j.yexcr.2008.08.010, 2613854, 18773890.
13. Nagaraj NS, Washington MK, Merchant NB. Combined blockade of Src kinase and epidermal growth factor receptor with gemcitabine overcomes STAT3-mediated resistance of inhibition of pancreatic tumor growth. Clin Cancer Res 2011, 17:483-493. 10.1158/1078-0432.CCR-10-1670, 3079196, 21266529.
14. Wheeler DL, Iida M, Kruser TJ, Nechrebecki MM, Dunn EF, Armstrong EA, Huang S, Harari PM. Epidermal growth factor receptor cooperates with Src family kinases in acquired resistance to cetuximab. Cancer Biol Ther 2009, 8:696-703. 10.4161/cbt.8.8.7903, 2895567, 19276677.
15. Dunn EF, Iida M, Myers RA, Campbell DA, Hintz KA, Armstrong EA, Li C, Wheeler DL. Dasatinib sensitizes KRAS mutant colorectal tumors to cetuximab. Oncogene 2011, 30:561-574. 10.1038/onc.2010.430, 3025039, 20956938.
16. Yoshida T, Zhang G, Haura EB. Targeting epidermal growth factor receptor: central signaling kinase in lung cancer. Biochem Pharmacol 2010, 80:613-623. 10.1016/j.bcp.2010.05.014, 20519133.
17. Zhang S, Huang WC, Li P, Guo H, Poh SB, Brady SW, Xiong Y, Tseng LM, Li SH, Ding Z, Sahin AA, Esteva FJ, Hortobagyi GN, Yu D. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 2011, 17:461-469. 10.1038/nm.2309, 3877934, 21399647.
18. Rexer BN, Ham AJ, Rinehart C, Hill S, Granja-Ingram M, González-Angulo AM, Mills GB, Dave B, Chang JC, Liebler DC, Arteaga CL. Phosphoproteomic mass spectrometry profiling links Src family kinases to escape from HER2 tyrosine kinase inhibition. Oncogene 2011, 30:4163-4174. 10.1038/onc.2011.130, 3204390, 21499296.
19. Sheffield LG. C-Src activation by ErbB2 leads to attachment-independent growth of human breast epithelial cells. Biochem Biophys Res Commun 1998, 250:27-31. 10.1006/bbrc.1998.9214, 9735325.
20. Belsches-Jablonski AP, Biscardi JS, Peavy DR, Tice DA, Romney DA, Parsons SJ. Src family kinases and HER2 interactions in human breast cancer cell growth and survival. Oncogene 2001, 20:1465-1475. 10.1038/sj.onc.1204205, 11313890.
21. Tan M, Li P, Klos KS. ErbB2 promotes Src synthesis and stability: novel mechanisms of Src activation that confer breast cancer metastasis. Cancer Res 2005, 65:1858-1867. 10.1158/0008-5472.CAN-04-2353, 15753384.
22. Kurebayashi J, Otsuki T, Tang CK, Kurosumi M, Yamamoto S, Tanaka K, Mochizuki M, Nakamura H, Sonoo H. Isolation and characterization of a new human breast cancer cell line, KPL-4, expressing the Erb B family receptors and interleukin-6. Br J Cancer 1999, 79:707-717. 10.1038/sj.bjc.6690114, 2362677, 10070858.
23. Tanner M, Kapanen AI, Junttila T, Raheem O, Grenman S, Elo J, Elenius K, Isola J. Characterization of a novel cell line established from a patient with Herceptin-resistant breast cancer. Mol Cancer Ther 2004, 3:1585-1592.
24. Bianco R, Rosa R, Damiano V, Daniele G, Gelardi T, Garofalo S, Tarallo V, De Falco S, Melisi D, Benelli R, Albini A, Ryan A, Ciardiello F, Tortora G. Vascular endothelial growth factor receptor-1 contributes to resistance to anti-epidermal growth factor receptor drugs in human cancer cells. Clin Cancer Res 2008, 14:5069-5080. 10.1158/1078-0432.CCR-07-4905, 18694994.
25. Melisi D, Ishiyama S, Sclabas GM, Fleming JB, Xia Q, Tortora G, Abbruzzese JL, Chiao PJ. LY2109761, a novel transforming growth factor beta receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis. Mol Cancer Ther 2008, 7:829-840. 10.1158/1535-7163.MCT-07-0337, 3088432, 18413796.
26. Rosa R, Marciano R, Malapelle U, Formisano L, Nappi L, D'Amato C, D'Amato V, Damiano V, Marfè G, Del Vecchio S, Zannetti A, Greco A, De Stefano A, Carlomagno C, Veneziani BM, Troncone G, De Placido S, Bianco R. Sphingosine kinase 1 overexpression contributes to cetuximab resistance in human colorectal cancer models. Clin Cancer Res 2013, 19:138-147. 10.1158/1078-0432.CCR-12-1050, 23166225.
27. Liu Z, Zhang B, Liu K, Ding Z, Hu X. Schisandrin B attenuates cancer invasion and metastasis via inhibiting epithelial-mesenchymal transition. PLoS One 2012, 7:e40480. 10.1371/journal.pone.0040480, 3405072, 22848381.
28. Schneider T, Osl F, Friess T, Stockinger H, Scheuer WV. Quantification of human Alu sequences by real-time PCR-an improved method to measure therapeutic efficacy of anti-metastatic drugs in human xenotransplants. Clin Exp Metastasis 2002, 19:571-582. 10.1023/A:1020992411420, 12498386.
29. García-García C, Ibrahim YH, Serra V, Calvo MT, Guzmán M, Grueso J, Aura C, Pérez J, Jessen K, Liu Y, Rommel C, Tabernero J, Baselga J, Scaltriti M. Dual mTORC1/2 and HER2 blockade results in antitumor activity in preclinical models of breast cancer resistant to anti-HER2 therapy. Clin Cancer Res 2012, 18:2603-2612. 10.1158/1078-0432.CCR-11-2750, 22407832.
30. O'Brien NA, Browne BC, Chow L, Wang Y, Ginther C, Arboleda J, Duffy MJ, Crown J, O'Donovan N, Slamon DJ. Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib. Mol Cancer Ther 2010, 9:1489-1502. 10.1158/1535-7163.MCT-09-1171, 20501798.
31. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
32. Donepudi M, Resh MD. c-Src trafficking and co-localization with the EGF receptor promotes EGF ligand-independent EGF receptor activation and signaling. Cell Signal 2008, 20:1359-1367. 10.1016/j.cellsig.2008.03.007, 2459337, 18448311.
33. Biscardi JS, Maa MC, Tice DA, Cox ME, Leu TH, Parsons SJ. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem 1999, 274:8335-8343. 10.1074/jbc.274.12.8335, 10075741.
34. Tice DA, Biscardi JS, Nickles AL, Parsons SJ. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci U S A 1999, 96:1415-1420. 10.1073/pnas.96.4.1415, 15477, 9990038.
35. Wu W, Graves LM, Gill GN, Parsons SJ, Samet JM. Src-dependent phosphorylation of the epidermal growth factor receptor on tyrosine 845 is required for zinc-induced Ras activation. J Biol Chem 2002, 277:24252-24257. 10.1074/jbc.M200437200, 11983694.
36. Fan Z, Lu Y, Wu X, Mendelsohn J. Antibody-induced epidermal growth factor receptor dimerization mediates inhibition of autocrine proliferation of A431 squamous carcinoma cells. J Biol Chem 1994, 269:27595-27602.
37. Mueller KL, Powell K, Madden JM, Eblen ST, Boerner JL. EGFR tyrosine 845 phosphorylation-dependent proliferation and transformation of breast cancer cells require activation of p38 MAPK. Transl Oncol 2012, 5:327-334. 10.1593/tlo.12163, 3468924, 23066441.
38. Rexer BN, Ghosh R, Narasanna A, Estrada MV, Chakrabarty A, Song Y, Engelman JA, Arteaga CL. Human breast cancer cells harboring a gatekeeper T798M mutation in HER2 overexpress EGFR ligands and are sensitive to dual inhibition of EGFR and HER2. Clin Cancer Res 2013, 19:5390-5401. 10.1158/1078-0432.CCR-13-1038, 23948973.
39. Xia W, Petricoin EF, Zhao S, Liu L, Osada T, Cheng Q, Wulfkuhle JD, Gwin WR, Yang X, Gallagher RI, Bacus S, Lyerly HK, Spector NL. An heregulin-EGFR-HER3 autocrine signaling axis can mediate acquired lapatinib resistance in HER2+ breast cancer models. Breast Cancer Res 2013, 15:R85. 10.1186/bcr3480, 3978995, 24044505.
40. Duncan JS, Whittle MC, Nakamura K, Abell AN, Midland AA, Zawistowski JS, Johnson NL, Granger DA, Jordan NV, Darr DB, Usary J, Kuan PF, Smalley DM, Major B, He X, Hoadley KA, Zhou B, Sharpless NE, Perou CM, Kim WY, Gomez SM, Chen X, Jin J, Frye SV, Earp HS, Graves LM, Johnson GL. Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 2012, 149:307-321. 10.1016/j.cell.2012.02.053, 3328787, 22500798.
41. Mueller KL, Hunter LA, Ethier SP, Boerner JL. Met and c-Src cooperate to compensate for loss of epidermal growth factor receptor kinase activity in breast cancer cells. Cancer Res 2008, 68:3314-3322. 10.1158/0008-5472.CAN-08-0132, 3878202, 18451158.
42. De Luca A, D'Alessio A, Gallo M, Maiello MR, Bode AM, Normanno N. Src and CXCR4 are involved in the invasiveness of breast cancer cells with acquired resistance to lapatinib. Cell Cycle 2014, 13:148-156. 10.4161/cc.26899, 24200972.
43. Rexer BN, Chanthaphaychith S, Dahlman KB, Arteaga CL. Direct inhibition of PI3K in combination with dual HER2 inhibitors is required for optimal antitumor activity in HER2+ breast cancer cells. Breast Cancer Res 2014, 16:R9. 10.1186/bcr3601, 3978602, 24451154.
44. Zhang D, Pal A, Bornmann WG, Yamasaki F, Esteva FJ, Hortobagyi GN, Bartholomeusz C, Ueno NT. Activity of lapatinib is independent of EGFR expression level in HER2-overexpressing breast cancer cells. Mol Cancer Ther 2008, 7:1846-1850. 10.1158/1535-7163.MCT-08-0168, 2525738, 18644997.
45. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, Arteaga CL. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res 2001, 61:8887-8895.
46. Normanno N, Campiglio M, De LA, Somenzi G, Maiello M, Ciardiello F, Gianni L, Salomon DS, Menard S. Cooperative inhibitory effect of ZD1839 (Iressa) in combination with trastuzumab (Herceptin) on human breast cancer cell growth. Ann Oncol 2002, 13:65-72.
47. Mayer EL, Baurain JF, Sparano J, Strauss L, Campone M, Fumoleau P, Rugo H, Awada A, Sy O, Llombart-Cussac A. A phase 2 trial of dasatinib in patients with advanced HER2-positive and/or hormone receptor-positive breast cancer. Clin Cancer Res 2011, 17:6897-6904. 10.1158/1078-0432.CCR-11-0070, 21903773.