Bypassing cellular EGF receptor dependence through epithelial-to- mesenchymal-like transitions

Clinical and Experimental Metastasis

Volumn 25, Issue 6, 2008, Pages 685-693

  Barr, Sharon ^a   Thomson, Stuart ^a   Buck, Elizabeth ^a   Russo, Suzanne ^a   Petti, Filippo ^a   Sujka Kwok, Izabela ^a   Eyzaguirre, Alexandra ^a   Rosenfeld Franklin, Maryland ^a   Gibson, Neil W ^a   Miglarese, Mark ^a   Epstein, David ^a   Iwata, Kenneth K ^a   Haley, John D ^a  

^a OSI PHARMACEUTICALS INC   (United States)

Author keywords

Cancer; E cadherin; EGFR; EMT; Epithelial to mesenchymal transition; Erlotinib; IGF 1R; Metastasis; PDGFR; Snail; Twist; Vimentin; Zeb 1

Indexed keywords

AMG 0479; ANTHRACYCLINE; AVE 1642; CAPECITABINE; CETUXIMAB; CP 753 871; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; GEMCITABINE; IMC A12; INSM 18; LAPATINIB; MK 0646; MONOCLONAL ANTIBODY; OSI 906; PANITUMUMAB; PLACEBO; R 1507; SCH 717454; SOMATOMEDIN; TRASTUZUMAB;

BLADDER CANCER; BREAST CANCER; BREAST CARCINOMA; CANCER SURVIVAL; CARCINOMA; CELL ADHESION; CELL MIGRATION; CELL SURVIVAL; CLINICAL TRIAL; COLORECTAL CANCER; EPITHELIUM CELL; HEAD AND NECK CANCER; HUMAN; LUNG NON SMALL CELL CANCER; MESENCHYME CELL; METASTASIS; MICROENVIRONMENT; NEOPLASM; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR CELL;

ANIMALS; CARCINOMA; EPITHELIUM; HUMANS; MESODERM; NEOPLASM INVASIVENESS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 47549092230     PISSN: 02620898     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10585-007-9121-7     Document Type: Review

References (105)

1. H Peinado D Olmeda A Cano 2007 Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7 6 415 428
2. M Maeda KR Johnson MJ Wheelock 2005 Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition J Cell Sci 118 Pt 5 873 887
3. T Brabletz A Jung S Reu 2001 Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment Proc Natl Acad Sci USA 98 18 10356 10361
4. B Willipinski-Stapelfeldt S Riethdorf V Assmann 2005 Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells Clin Cancer Res 11 22 8006 8014
5. E Buck A Eyzaguirre S Barr 2007 Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition Mol Cancer Ther 6 2 532 541
6. R Umbas JA Schalken TW Aalders 1992 Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer Cancer Res 52 18 5104 5109
7. T Yin C Wang T Liu T 2007 Expression of snail in pancreatic cancer promotes metastasis and chemoresistance J Surg Res 141 2 196 203
8. H Kajiyama K Shibata M Terauchi 2007 Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells Int J Oncol 31 2 277 283
9. GZ Cheng J Chan Q Wang 2007 Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel Cancer Res 67 5 1979 1987
10. Z Zhang D Xie X Li 2007 Significance of TWIST expression and its association with E-cadherin in bladder cancer Hum Pathol 38 4 598 606
11. S Hosono H Kajiyama M Terauchi 2007 Expression of Twist increases the risk for recurrence and for poor survival in epithelial ovarian carcinoma patients Br J Cancer 96 2 314 320
12. P Leroy KE Mostov 2007 Slug is required for cell survival during partial epithelial-mesenchymal transition of HGF-induced tubulogenesis Mol Biol Cell 18 5 1943 1952
13. HJ Cho KE Baek S Saika 2007 Snail is required for transforming growth factor-beta-induced epithelial-mesenchymal transition by activating PI3 kinase/Akt signal pathway Biochem Biophys Res Commun 353 2 337 343
14. H Laux R Tomer MT Mader 2004 Tumor-associated E-cadherin mutations do not induce Wnt target gene expression, but affect E-cadherin repressors Lab Invest 84 10 1372 1386
15. M Lombaerts T van Wezel K Philippo 2006 E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-to-mesenchymal transition in breast cancer cell lines Br J Cancer 94 5 661 671
16. AK Perl P Wilgenbus U Dahl 1998 A causal role for E-cadherin in the transition from adenoma to carcinoma Nature 392 6672 190 193
17. K Vleminckx L Vakaet Jr M Mareel 1991 Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role Cell 66 1 107 119
18. J Yang SA Mani JL Donaher 2004 Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis Cell 117 7 927 939
19. A Cano MA Perez-Moreno I Rodrigo 2000 The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat Cell Biol 2 2 76 83
20. E Batlle E Sancho C Franci 2000 The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells Nat Cell Biol 2 2 84 89
21. G Hennig O Lowrick W Birchmeier 1996 Mechanisms identified in the transcriptional control of epithelial gene expression J Biol Chem 271 1 595 602
22. G Hennig J Behrens M Truss 1995 Progression of carcinoma cells is associated with alterations in chromatin structure and factor binding at the E-cadherin promoter in vivo Oncogene 11 3 475 484
23. W Birchmeier J Behrens 1994 Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness Biochim Biophys Acta 1198 1 11 26
24. MA Nieto 2002 The snail superfamily of zinc-finger transcription factors Nat Rev Mol Cell Biol 3 3 155 166
25. K Aigner B Dampier Jr L Descovichl 2007 The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity Oncogene 26 49 6979 6988
26. A Eger K Aigner S Sonderegger 2005 DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells Oncogene 24 14 2375 2385
27. MA Perez-Moreno A Locascio I Rodrigo 2001 A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions J Biol Chem 276 29 27424 27431
28. S Guaita I Puig C Franci 2002 Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression J Biol Chem 277 42 39209 39216
29. L Tamagnone PM Comoglio 1997 Control of invasive growth by hepatocyte growth factor (HGF) and related scatter factors Cytokine Growth Factor Rev 8 2 129 142
30. R Montesano K Matsumoto T Nakamura 1991 Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor Cell 67 5 901 908
31. JP Thiery 2002 Epithelial-mesenchymal transitions in tumour progression Nat Rev Cancer 2 6 442 454
32. JP Thiery 2003 Epithelial-mesenchymal transitions in development and pathologies Curr Opin Cell Biol 15 6 740 746
33. A Vincent-Salomon JP Thiery 2003 Host microenvironment in breast cancer development: epithelial-mesenchymal transition in breast cancer development Breast Cancer Res 5 2 101 106
34. T Onoue D Uchida NM Begum 2006 Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells Int J Oncol 29 5 1133 1138
35. T Waerner M Alacakaptan I Tamir 2006 ILEI: a cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells Cancer Cell 10 3 227 239
36. OW Petersen HL Nielsen T Gudjonsson 2003 Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma Am J Pathol 162 2 391 402
37. R Derynck RJ Akhurst A Balmain 2001 TGF-beta signaling in tumor suppression and cancer progression Nat Genet 29 2 117 129
38. HL Moses EY Yang JA Pietenpol 1990 TGF-beta stimulation and inhibition of cell proliferation: new mechanistic insights Cell 63 2 245 247
39. F Valdes AM Alvarez A Locascio 2002 The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor Beta in fetal rat hepatocytes Mol Cancer Res 1 1 68 78
40. A Sanchez AM Alvarez JM Lopez Pedrosa 1999 Apoptotic response to TGF-beta in fetal hepatocytes depends upon their state of differentiation Exp Cell Res 252 2 281 291
41. EJ Robson WT Khaled K Abell 2006 Epithelial-to-mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines Differentiation; Res Biol Divers 74 5 254 264
42. Gal A, Sjoblom T, Fedorova L et al (2007) Sustained TGFbeta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene. doi: 10.1038/sj.onc.1210741
43. S Vega AV Morales OH Ocana 2004 Snail blocks the cell cycle and confers resistance to cell death Genes Dev 18 10 1131 1143
44. A Inoue MG Seidel W Wu 2002 Slug, a highly conserved zinc finger transcriptional repressor, protects hematopoietic progenitor cells from radiation-induced apoptosis in vivo Cancer Cell 2 4 279 288
45. WS Wu S Heinrichs D Xu 2005 Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma Cell 123 4 641 653
46. Y Fujita G Krause M Scheffner 2002 Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex Nat Cell Biol 4 3 222 231
47. HJ Kim BC Litzenburger X Cui 2007 Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-kappaB and snail Mol Cell Biol 27 8 3165 3175
48. T Lopez D Hanahan 2002 Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis Cancer Cell 1 4 339 353
49. ME Doerr JI Jones 1996 The roles of integrins and extracellular matrix proteins in the insulin-like growth factor I-stimulated chemotaxis of human breast cancer cells J Biol Chem 271 5 2443 2447
50. ML Stracke JD Engel LW Wilson 1989 The type I insulin-like growth factor receptor is a motility receptor in human melanoma cells J Biol Chem 264 36 21544 21549
51. KE Bornfeldt EW Raines T Nakano 1994 Insulin-like growth factor-I and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signaling pathways that are distinct from those of proliferation J Clin Invest 93 3 1266 1274
52. PS Leventhal EA Shelden B Kim 1997 Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance J Biol Chem 272 8 5214 5218
53. MP Playford D Bicknell WF Bodmer 2000 Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of beta-catenin Proc Natl Acad Sci USA 97 22 12103 12108
54. D Zhang P Brodt 2003 Type 1 insulin-like growth factor regulates MT1-MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling Oncogene 22 7 974 982
55. MR Shen YM Hsu KF Hsu 2006 Insulin-like growth factor 1 is a potent stimulator of cervical cancer cell invasiveness and proliferation that is modulated by alphavbeta3 integrin signaling Carcinogenesis 27 5 962 971
56. EA Bohula MP Playford VM Macaulay 2003 Targeting the type 1 insulin-like growth factor receptor as anti-cancer treatment Anticancer Drugs 14 9 669 682
57. JT Price HM Wilson NE Haites 1996 Epidermal growth factor (EGF) increases the in vitro invasion, motility and adhesion interactions of the primary renal carcinoma cell line, A704 Eur J Cancer 32A 11 1977 1982
58. T Shibata T Kawano H Nagayasu 1996 Enhancing effects of epidermal growth factor on human squamous cell carcinoma motility and matrix degradation but not growth Tumour Biol 17 3 168 175
59. Z Lu G Jiang P Blume-Jensen 2001 Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase Mol Cell Biol 21 12 4016 4031
60. CM Salamanca SL Maines-Bandiera PC Leung 2004 Effects of epidermal growth factor/hydrocortisone on the growth and differentiation of human ovarian surface epithelium J Soc Gynecol Invest 11 4 241 251
61. Z Lu S Ghosh Z Wang 2003 Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion Cancer Cell 4 6 499 515
62. GW Cole Jr AM Alleva RM Reddy 2005 The selective epidermal growth factor receptor tyrosine kinase inhibitor PD153035 suppresses expression of prometastasis phenotypes in malignant pleural mesothelioma cells in vitro J Thorac Cardiovasc Surg 129 5 1010 1017
63. A Lal CA Glazer HM Martinson 2002 Mutant epidermal growth factor receptor up-regulates molecular effectors of tumor invasion Cancer Res 62 12 3335 3339
64. SE Seton-Rogers Y Lu LM Hines 2004 Cooperation of the ErbB2 receptor and transforming growth factor beta in induction of migration and invasion in mammary epithelial cells Proc Natl Acad Sci USA 101 5 1257 1262
65. AR Mateus R Seruca JC Machado 2007 EGFR regulates RhoA-GTP dependent cell motility in E-cadherin mutant cells Hum Mol Genet 16 13 1639 1647
66. JH Lorch J Klessner JK Park 2004 Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens intercellular adhesion in squamous cell carcinoma cells J Biol Chem 279 35 37191 37200
67. A Wells 1999 EGF receptor Int J Biochem Cell Biol 31 6 637 643
68. JR Grandis JC Sok 2004 Signaling through the epidermal growth factor receptor during the development of malignancy Pharmacol Ther 102 1 37 46
69. FA Shepherd J Rodrigues Pereira T Ciuleanu 2005 Erlotinib in previously treated non-small-cell lung cancer N Engl J Med 353 2 123 132
70. S Thomson E Buck F Petti 2005 Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition Cancer Res 65 20 9455 9462
71. RL Yauch T Januario DA Eberhard 2005 Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients Clin Cancer Res 11 24 Pt 1 8686 8698
72. SE Witta RM Gemmill FR Hirsch 2006 Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines Cancer Res 66 2 944 950
73. BA Frederick BA Helfrich CD Coldren 2007 Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma Mol Cancer Ther 6 6 1683 1691
74. M Shrader MS Pino G Brown 2007 Molecular correlates of gefitinib responsiveness in human bladder cancer cells Mol Cancer Ther 6 1 277 285
75. Buck E, Eyzaguirre A, Franklin M et al (2007) The EGFR inhibitor erlotinib sensitizes tumor cells to IGF-1 receptor inhibition by promoting Akt signaling through the IGF-1R-IRS1-Akt axis. Proceedings of American Association for Cancer Research Annual Meeting, Los Angeles, CA
76. RS Herbst D Prager R Hermann 2005 TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer J Clin Oncol 23 25 5892 5899
77. M Ono A Hirata T Kometani 2004 Sensitivity to gefitinib (Iressa, ZD1839) in non-small cell lung cancer cell lines correlates with dependence on the epidermal growth factor (EGF) receptor/extracellular signal-regulated kinase 1/2 and EGF receptor/Akt pathway for proliferation Mol Cancer Ther 3 4 465 472
78. CL Arteaga 2002 Epidermal growth factor receptor dependence in human tumors: more than just expression? Oncologist 7 Suppl 4 31 39
79. SL Moulder FM Yakes SK Muthuswamy 2001 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 61 24 8887 8895
80. E Buck A Eyzaguirre JD Haley 2006 Inactivation of Akt by the epidermal growth factor receptor inhibitor erlotinib is mediated by HER-3 in pancreatic and colorectal tumor cell lines and contributes to erlotinib sensitivity Mol Cancer Ther 5 8 2051 2059
81. G Del Castillo MM Murillo A Alvarez-Barrientos 2006 Autocrine production of TGF-beta confers resistance to apoptosis after an epithelial-mesenchymal transition process in hepatocytes: role of EGF receptor ligands Exp Cell Res 312 15 2860 2871
82. MM Murillo G del Castillo A Sanchez 2005 Involvement of EGF receptor and c-Src in the survival signals induced by TGF-beta1 in hepatocytes Oncogene 24 28 4580 4587
83. JA Engelman PA Janne C Mermel 2005 ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines Proc Natl Acad Sci USA 102 10 3788 3793
84. C Desbois-Mouthon W Cacheux MJ Blivet-Van Eggelpoel 2006 Impact of IGF-1R/EGFR cross-talks on hepatoma cell sensitivity to gefitinib Int J Cancer 119 11 2557 2566
85. Barr SM, Buck EA, Thomson S et al (2007) The combination of small molecule inhibitors of EGFR and IGF-1R is synergistic in HNSCC and ovarian cancer cell lines. Proceedings of American Association of Cancer Research Annual Meeting. Los Angeles, CA
86. A Chakravarti JS Loeffler NJ Dyson 2002 Insulin-like growth factor receptor I mediates resistance to anti-epidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling Cancer Res 62 1 200 207
87. HE Jones L Goddard JM Gee 2004 Insulin-like growth factor-I receptor signalling and acquired resistance to gefitinib (ZD1839; Iressa) in human breast and prostate cancer cells Endocr Relat Cancer 11 4 793 814
88. AP Sutter M Hopfner A Huether 2006 Targeting the epidermal growth factor receptor by erlotinib (Tarceva) for the treatment of esophageal cancer Int J Cancer 118 7 1814 1822
89. MG Slomiany LA Black MM Kibbey 2007 Insulin-like growth factor-1 receptor and ligand targeting in head and neck squamous cell carcinoma Cancer Lett 248 2 269 279
90. C Desbois-Mouthon C Danan S Amselem 1996 Severe resistance to insulin and insulin-like growth factor-I in cells from a patient with leprechaunism as a result of two mutations in the tyrosine kinase domain of the insulin receptor Metabolism 45 12 1493 1500
91. F Morgillo JK Woo ES Kim 2006 Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib Cancer Res 66 20 10100 10111
92. SE Dunn M Ehrlich NJ Sharp 1998 A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer Cancer Res 58 15 3353 3361
93. AA Samani L Fallavollita DE Jaalouk 2001 Inhibition of carcinoma cell growth and metastasis by a vesicular stomatitis virus G-pseudotyped retrovector expressing type I insulin-like growth factor receptor antisense Hum Gene Ther 12 16 1969 1977
94. YJ Choi SJ Nam MJ Son 2006 Erlotinib prevents pulmonary metastasis in curatively resected breast carcinoma using a mouse model Oncol Rep 16 1 119 122
95. A Angelucci GL Gravina N Rucci 2006 Suppression of EGF-R signaling reduces the incidence of prostate cancer metastasis in nude mice Endocr Relat Cancer 13 1 197 210
96. S Shintani C Li M Mihara 2003 Gefitinib ('Iressa'), an epidermal growth factor receptor tyrosine kinase inhibitor, mediates the inhibition of lymph node metastasis in oral cancer cells Cancer Lett 201 2 149 155
97. Thomson S, Petti F, Haley J (2007) Multiple mechanisms of insensitivity to Erlotinib in mesenchymal-like NSCLC cell lines. Proceedings of the American Association for Cancer Research Anual Meeting, Los Angeles, CA; 48
98. CH Heldin B Westermark A Wasteson 1981 Specific receptors for platelet-derived growth factor on cells derived from connective tissue and glia Proc Natl Acad Sci USA 78 6 3664 3668
99. B Westermark CH Heldin M Nister 1995 Platelet-derived growth factor in human glioma Glia 15 3 257 263
100. C Dai JC Celestino Y Okada 2001 PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo Genes Dev 15 15 1913 1925
101. D Matei RE Emerson YC Lai 2006 Autocrine activation of PDGFRalpha promotes the progression of ovarian cancer Oncogene 25 14 2060 2069
102. YJ Ko EJ Small F Kabbinavar 2001 A multi-institutional phase ii study of SU101, a platelet-derived growth factor receptor inhibitor, for patients with hormone-refractory prostate cancer Clin Cancer Res 7 4 800 805
103. I Carvalho F Milanezi A Martins 2005 Overexpression of platelet-derived growth factor receptor alpha in breast cancer is associated with tumour progression Breast Cancer Res 7 5 R788 R795
104. M Jechlinger A Sommer R Moriggl 2006 Autocrine PDGFR signaling promotes mammary cancer metastasis J Clin Invest 116 6 1561 1570
105. R Kalluri M Zeisberg 2006 Fibroblasts in cancer Nat Rev Cancer 6 5 392 401