Heregulin induces resistance to lapatinib-mediated growth inhibition of HER2-amplified cancer cells

Cancer Science

Volumn 104, Issue 12, 2013, Pages 1618-1625

  Sato, Yuji ^a,b   Yashiro, Masakazu ^c   Takakura, Nobuyuki ^a,d  

^a OSAKA UNIVERSITY   (Japan)

^b SHIONOGI AND CO LTD   (Japan)

^c OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AFATINIB; ANTINEOPLASTIC AGENT; CRIZOTINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; EVEROLIMUS; LAPATINIB; NEU DIFFERENTIATION FACTOR; NVP BGJ 398; PF 562271; PROTEIN KINASE B; SARACATINIB; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE ARREST; CONTROLLED STUDY; DOWN REGULATION; DRUG RESISTANCE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LOWER ESOPHAGUS SPHINCTER CANCER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH CANCER; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; ESOPHAGEAL NEOPLASMS; HUMANS; NEUREGULIN-1; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TOR SERINE-THREONINE KINASES;

EID: 84889588956     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12290     Document Type: Article

References (42)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63: 11-30.
2. Cunningham D, Starling N, Rao S et al. Capecitabine and oxaliplatin for advanced esophagogastric cancer. New Engl J Med 2008; 358: 36-46.
3. Bang YJ, Van Cutsem E, Feyereislova A et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010; 376: 687-97.
4. Wainberg ZA, Anghel A, Desai AJ et al. Lapatinib, a dual EGFR and HER2 kinase inhibitor, selectively inhibits HER2-amplified human gastric cancer cells and is synergistic with trastuzumab in vitro and in vivo. Clin Cancer Res 2010; 16: 1509-19.
5. Park D, Yun JW, Park JH et al. HER-2/neu amplification is an independent prognostic factor in gastric cancer. Dig Dis Sci 2006; 51: 1371-9.
6. Zhang XL, Yang YS, Xu DP et al. Comparative study on overexpression of HER2/neu and HER3 in gastric cancer. World J Surg 2009; 33: 2112-8.
7. De Vita F, Giuliani F, Silvestris N, Catalano G, Ciardiello F, Orditura M. Human epidermal growth factor receptor 2 (HER2) in gastric cancer: a new therapeutic target. Cancer Treat Rev 2010; 36 (Suppl. 3): S11-5.
8. Xia W, Mullin RJ, Keith BR et al. Anti-tumor activity of GW572016: a dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene 2002; 21: 6255-63.
9. Kim JW, Kim HP, Im SA et al. The growth inhibitory effect of lapatinib, a dual inhibitor of EGFR and HER2 tyrosine kinase, in gastric cancer cell lines. Cancer Lett 2008; 272: 296-306.
10. Iqbal S, Goldman B, Fenoglio-Preiser CM et al. Southwest Oncology Group study S0413: a phase II trial of lapatinib (GW572016) as first-line therapy in patients with advanced or metastatic gastric cancer. Ann Oncol 2011; 22: 2610-5.
11. Jänne PA. Challenges of detecting EGFR T790M in gefitinib/erlotinib-resistant tumors. Lung Cancer 2008; 60 (Suppl. 2): s3-9.
12. Pao W, Miller VA, Politi KA et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2(3): e73.
13. Liu L, Greger J, Shi H et al. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res 2009; 69: 6871-8.
14. Engelman JA, Zejnullahu K, Mitsudomi T et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-43.
15. Garrett JT, Olivares MG, Rinehart C et al. Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc Natl Acad Sci USA 2011; 108: 5021-6.
16. Chen CT, Kim H, Liska D, Gao S, Christensen JG, Weiser MR. MET activation mediates resistance to lapatinib inhibition of HER2-amplified gastric cancer cells. Mol Cancer Ther 2012; 11: 660-9.
17. Wilson TR, Fridlyand J, Yan Y et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012; 487: 505-9.
18. Horan T, Wen J, Arakawa T et al. Binding of Neu differentiation factor with the extracellular domain of Her2 and Her3. J Biol Chem 1995; 270: 24604-8.
19. Hijazi MM, Thompson EW, Tang C et al. Heregulin regulates the actin cytoskeleton and promotes invasive properties in breast cancer cell lines. Int J Oncol 2000; 17: 629-41.
20. Li Q, Ahmed S, Loeb JA. Development of an autocrine neuregulin signaling loop with malignant transformation of human breast epithelial cells. Cancer Res 2004; 64: 7078-85.
21. Gollamudi M, Nethery D, Liu J, Kern JA. Autocrine activation of ErbB2/ErbB3 receptor complex by HRG1-1 in non-small cell lung cancer cell lines. Lung Cancer 2004; 43: 135-43.
22. Venkateswarlu S, Dawson DM, St Clair P, Gupta A, Willson JK, Brattain MG. Autocrine heregulin generates growth factor independence and blocks apoptosis in colon cancer cells. Oncogene 2002; 21: 78-86.
23. Wilson TR, Lee DY, Berry L, Shames DS, Settleman J. Neuregulin-1-mediated autocrine signaling underlies sensitivity to HER2 kinase inhibitors in a subset of human cancers. Cancer Cell 2011; 20: 158-72.
24. Srinivasan R, Benton E, McCormick F, Thomas H, Gullick WJ. Expression of the c-erbB-3/HER-3 and c-erbB-4/HER-4 growth factor receptors and their ligands, neuregulin-1 alpha, neuregulin-1 beta, and betacellulin, in normal endometrium and endometrial cancer. Clin Cancer Res 1999; 5: 2877-83.
25. Noguchi H, Sakamoto C, Wada K et al. Expression of heregulin alpha, erbB2, and erbB3 and their influences on proliferation of gastric epithelial cells. Gastroenterology 1997; 117: 1119-27.
26. Nagata K, Wada K, Tatsuguchi A et al. Heregulin-alpha and heregulin-beta expression is linked to a COX-2-PGE2 pathway in human gastric fibroblasts. Am J Physiol Gastrointest Liver Physiol 2006; 290: G1243-51.
27. Hutcheson IR, Knowlden JM, Hiscox SE et al. Heregulin beta1 drives gefitinib-resistant growth and invasion in tamoxifen-resistant MCF-7 breast cancer cells. Breast Cancer Res 2007; 9: R50.
28. Fuyuhiro Y, Yashiro M, Noda S et al. Upregulation of cancer-associated myofibroblasts by TGF-β from scirrhous gastric carcinoma cells. Br J Cancer 2011; 105: 996-1001.
29. Ishizawar RC, Miyake T, Parsons SJ. c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 2007; 26: 3503-10.
30. Guo A, Villén J, Kornhauser J et al. Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 2008; 105: 692-7.
31. Kunii K, Davis L, Gorenstein J et al. FGFR2-amplified gastric cancer cell lines require FGFR2 and Erbb3 signaling for growth and survival. Cancer Res 2008; 68: 2340-8.
32. Van der Horst EH, Weber I, Ullrich A. Tyrosine phosphorylation of PYK2 mediates heregulin-induced glioma invasion: novel heregulin/HER3-stimulated signaling pathway in glioma. Int J Cancer 2005; 113: 689-98.
33. Hecht JR, Bang YJ, Qin S et al. Lapatinib in combination with capecitabine plus oxaliplatin (CapeOx) in HER2-positive advanced or metastatic gastric, esophageal, or gastroesophageal adenocarcinoma (AC): the TRIO-013/LOGiC Trial. J Clin Oncol (Meeting abstracts) 2013; 31: Abstract LBA4001.
34. Hayashi M, Inokuchi M, Takagi Y et al. High expression of HER3 is associated with a decreased survival in gastric cancer. Clin Cancer Res 2008; 14: 7843-9.
35. Garrett JT, Sutton CR, Kuba MG, Cook RS, Arteaga CL. Dual blockade of HER2 in HER2-overexpressing tumor cells does not completely eliminate HER3 function. Clin Cancer Res 2013; 19: 610-9.
36. Chandarlapaty S, Sawai A, Scaltriti M et al. AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 2011; 19: 58-71.
37. Scaltriti M, Verma C, Guzman M et al. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene 2009; 28: 803-14.
38. Maruyama T, Mimura K, Izawa S et al. Lapatinib enhances herceptin-mediated antibody-dependent cellular cytotoxicity by up-regulation of cell surface HER2 expression. Anticancer Res 2011; 31: 2999-3005.
39. Schroeder B, Srivatsan S, Shaw A, Billadeau D, McNiven MA. CIN85 phosphorylation is essential for EGFR ubiquitination and sorting into multivesicular bodies. Mol Biol Cell 2012; 23: 3602-11.
40. Van Cutsem E, Yah KH, Bang YJ et al. Phase 3 trial of everolimus in previously treated patients with advanced gastric cancer: GRANITE-1. Gastrointestinal Cancers Symposium 2012; Abstract LBA3.
41. Shi F, Telesco SE, Liu Y, Radhakrishnan R, Lemmon MA. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci USA 2010; 107: 7692-7.
42. Wu Y, Zhang Y, Wang M et al. Downregulation of HER3 by a novel antisense oligonucleotide, EZN-3920, improves the antitumor activity of EGFR and HER2 tyrosine kinase inhibitors in animal models. Mol Cancer Ther 2013; 12: 427-37.