ErbB targeting inhibitors repress cell migration of esophageal squamous cell carcinoma and adenocarcinoma cells by distinct signaling pathways

Journal of Molecular Medicine

Volumn 92, Issue 11, 2014, Pages 1209-1223

  Fichter, Christiane D ^a,b   Gudernatsch, Verena ^a   Przypadlo, Camilla M ^a   Follo, Marie ^a   Schmidt, Gudula ^b   Werner, Martin ^a,c   Lassmann, Silke ^a,b,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

ErbB; Esophageal cancer; FAK; Migration; RhoA; STATs; TKI

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; FOCAL ADHESION KINASE; GEFITINIB; GUANOSINE TRIPHOSPHATASE; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; ANTINEOPLASTIC AGENT; PHALLOIDIN;

ACTIN FILAMENT; ARTICLE; CANCER CELL; CELL MIGRATION; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; DIMERIZATION; DRUG TARGETING; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL CANCER CELL LINE; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FOCAL ADHESION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRESS FIBER; WESTERN BLOTTING; ADENOCARCINOMA; ANTAGONISTS AND INHIBITORS; CELL MOTION; CHEMISTRY; ESOPHAGUS TUMOR; GENE EXPRESSION REGULATION; INDIRECT FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NEOPLASM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ACTIN CYTOSKELETON; ADENOCARCINOMA; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; ERBB RECEPTORS; ESOPHAGEAL NEOPLASMS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; PHALLOIDINE; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 84919838892     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-014-1187-5     Document Type: Article

References (35)

1. Yarden Y, Sliwkowski MX (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2:127–137
2. Walch A, Bink K, Hutzler P, Hofler H, Werner M (2000) HER-2/neu gene amplification by FISH predicts poor survival in Barrett’s esophagus-associated adenocarcinoma. Hum Pathol 31:1332–1334
3. Hanawa M, Suzuki S, Dobashi Y, Yamane T, Kono K, Enomoto N, Ooi A (2006) EGFR protein overexpression and gene amplification in squamous cell carcinomas of the esophagus. Int J Cancer 118:1173–1180
4. Okines A, Cunningham D, Chau I (2011) Targeting the human EGFR family in esophagogastric cancer. Nat Rev Clin Oncol 8:492–503
5. Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374
6. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev 11:633–643
7. Xie H, Pallero MA, Gupta K, Chang P, Ware MF, Witke W, Kwiatkowski DJ, Lauffenburger DA, Murphy-Ullrich JE, Wells A (1998) EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCgamma signaling pathway. J Cell Sci 111:615–624
8. Lu Z, Jiang G, Blume-Jensen P, Hunter T (2001) Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase. Mol Cell Biol 21:4016–4031
9. Han J, Li L, Hu J, Yu L, Zheng Y, Guo J, Zheng X, Yi P, Zhou Y (2010) Epidermal growth factor stimulates human trophoblast cell migration through Rho A and Rho C activation. Endocrinology 151:1732–1742
10. Pennathur A, Gibson MK, Jobe BA, Luketich JD (2013) Oesophageal carcinoma. Lancet 381:400–412
11. Yamamoto Y, Yamai H, Seike J, Yoshida T, Takechi H, Furukita Y, Kajiura K, Minato T, Bando Y, Tangoku A (2012) Prognosis of esophageal squamous cell carcinoma in patients positive for human epidermal growth factor receptor family can be improved by initial chemotherapy with docetaxel, fluorouracil, and cisplatin. Ann Surg Oncol 19:757–765
12. Yoon HH, Shi Q, Sukov WR, Wiktor AE, Khan M, Sattler CA, Grothey A, Wu TT, Diasio RB, Jenkins RB et al (2012) Association of HER2/ErbB2 expression and gene amplification with pathologic features and prognosis in esophageal adenocarcinomas. Clin Cancer Res 18:546–554
13. Fichter CD, Timme S, Braun JA, Gudernatsch V, Schopflin A, Bogatyreva L, Geddert H, Faller G, Klimstra D, Tang L et al (2014) EGFR, HER2 and HER3 dimerization patterns guide targeted inhibition in two histotypes of esophageal cancer. Int J Cancer. doi:10.1002/ijc28771
14. Sutter AP, Hopfner M, Huether A, Maaser K, Scherubl H (2006) Targeting the epidermal growth factor receptor by erlotinib (Tarceva) for the treatment of esophageal cancer. Int J Cancer 118:1814–1822
15. Hara F, Aoe M, Doihara H, Taira N, Shien T, Takahashi H, Yoshitomi S, Tsukuda K, Toyooka S, Ohta T et al (2005) Antitumor effect of gefitinib (‘Iressa’) on esophageal squamous cell carcinoma cell lines in vitro and in vivo. Cancer Lett 226:37–47
16. Mimura K, Kono K, Maruyama T, Watanabe M, Izawa S, Shiba S, Mizukami Y, Kawaguchi Y, Inoue M, Kono T et al (2011) Lapatinib inhibits receptor phosphorylation and cell growth and enhances antibody-dependent cellular cytotoxicity of EGFR- and HER2-overexpressing esophageal cancer cell lines. Int J Cancer 129:2408–2416
17. Ilson DH, Kelsen D, Shah M, Schwartz G, Levine DA, Boyd J, Capanu M, Miron B, Klimstra D (2011) A phase 2 trial of erlotinib in patients with previously treated squamous cell and adenocarcinoma of the esophagus. Cancer 117:1409–1414
18. Ku GY, Ilson DH (2013) Emerging tyrosine kinase inhibitors for esophageal cancer. Expert Opin Emerg Drugs 18:219–230
19. Haddad Y, Choi W, McConkey DJ (2009) Delta-crystallin enhancer binding factor 1 controls the epithelial to mesenchymal transition phenotype and resistance to the epidermal growth factor receptor inhibitor erlotinib in human head and neck squamous cell carcinoma lines. Clin Cancer Res 15:532–542
20. Nie F, Yang J, Wen S, An YL, Ding J, Ju SH, Zhao Z, Chen HJ, Peng XG, Wong ST et al (2012) Involvement of epidermal growth factor receptor overexpression in the promotion of breast cancer brain metastasis. Cancer 118:5198–5209
21. Ramis G, Thomas-Moya E, Fernandez de Mattos S, Rodriguez J, Villalonga P (2012) EGFR inhibition in glioma cells modulates Rho signaling to inhibit cell motility and invasion and cooperates with temozolomide to reduce cell growth. PLoS One 7:e38770
22. Miyazaki T, Kato H, Nakajima M, Sohda M, Fukai Y, Masuda N, Manda R, Fukuchi M, Tsukada K, Kuwano H (2003) FAK overexpression is correlated with tumour invasiveness and lymph node metastasis in oesophageal squamous cell carcinoma. Br J Cancer 89:140–145
23. Faried A, Nakajima M, Sohda M, Miyazaki T, Kato H, Kuwano H (2005) Correlation between RhoA overexpression and tumour progression in esophageal squamous cell carcinoma. Eur J Surg Oncol 31:410–414
24. Fichter CD, Herz C, Munch C, Opitz OG, Werner M, Lassmann S (2011) Occurrence of multipolar mitoses and association with Aurora-A/-B kinases and p53 mutations in aneuploid esophageal carcinoma cells. BMC Cell Biol 12:13
25. Reipschlager S, Kubatzky K, Taromi S, Burger M, Orth J, Aktories K, Schmidt G (2012) Toxin-induced RhoA activity mediates CCL1-triggered signal transducers and activators of transcription protein signaling. J Biol Chem 287:11183–11194
26. May M, Kolbe T, Wang T, Schmidt G, Genth H (2012) Increased cell-matrix adhesion upon constitutive activation of Rho proteins by cytotoxic necrotizing factors from E. coli and Y. pseudotuberculosis. J Signal Transduct 2012, 570183
27. Sun X, Gao L, Yu RK, Zeng G (2006) Down-regulation of WNK1 protein kinase in neural progenitor cells suppresses cell proliferation and migration. J Neurochem 99:1114–1121
28. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6:56–68
29. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–635
30. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471–484
31. Raptis L, Arulanandam R, Geletu M, Turkson J (2011) The R(h)oads to Stat3: Stat3 activation by the Rho GTPases. Exp Cell Res 317:1787–1795
32. Timme S, Ihde S, Fichter CD, Waehle V, Bogatyreva L, Atanasov K, Kohler I, Schopflin A, Geddert H, Faller G et al (2013) STAT3 expression, activity and functional consequences of STAT3 inhibition in esophageal squamous cell carcinomas and Barrett’s adenocarcinomas. Oncogene. doi:10.1038/onc2013298
33. Schaller MD (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123(Pt 7):1007–1013
34. Tomar A, Schlaepfer DD (2009) Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21:676–683
35. Hu T, Li C (2010) Convergence between Wnt-beta-catenin and EGFR signaling in cancer. Mol Cancer 9:236