Hyperactivation of constitutively dimerized oncogenic EGF receptors by autocrine loops

Oncogene

Volumn 32, Issue 19, 2013, Pages 2403-2411

  Laisney, J A G C ^a   Mueller, T D ^b   Schartl, M ^a   Meierjohann, S ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

EGFR ligands; melanoma; receptor tyrosine kinase

Indexed keywords

AMPHIREGULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; LIGAND; PROTEIN VARIANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; CARCINOGENESIS; CONTROLLED STUDY; DIMERIZATION; FISH; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ORYZIAS; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADULT; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AUTOCRINE COMMUNICATION; CYPRINODONTIFORMES; ENZYME ACTIVATION; HUMANS; MELANOCYTES; MICE; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

ORYZIINAE; XIPHOPHORUS;

EID: 84877605179     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.267     Document Type: Article

References (70)

1. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR et al. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006; 366: 2-16.
2. Domingo G, Perez CA, Velez M, Cudris J, Raez LE, Santos ES. EGF receptor in lung cancer: a successful story of targeted therapy. Expert Rev Anticancer Ther 2010; 10: 1577-1587.
3. Berardi R, Onofri A, Pistelli M, Maccaroni E, Scartozzi M, Pierantoni C et al. Pani-tumumab: the evidence for its use in the treatment of metastatic colorectal cancer. Core Evid 2010; 5: 61-76.
4. Vivanco I, Mellinghoff IK. Epidermal growth factor receptor inhibitors in oncology. Curr Opin Oncol 2010; 22: 573-578.
5. Mitsudomi T, Yatabe Y. Epidermal growth factor receptor in relation to tumor development: EGFR gene and cancer. FEBS J 2010; 277: 301-308.
6. Modjtahedi H, Essapen S. Epidermal growth factor receptor inhibitors in cancer treatment: advances, challenges and opportunities. AntiCancer Drugs 2009; 20: 851-855.
7. Pines G, Kostler WJ, Yarden Y. Oncogenic mutant forms of EGFR: lessons in signal transduction and targets for cancer therapy. FEBS Lett 2010; 584: 2699-2706.
8. Bellone S, Frera G, Landolfi G, Romani C, Bandiera E, Tognon G et al. Over-expression of epidermal growth factor type-1 receptor (EGF-R1) in cervical cancer: implications for Cetuximab-mediated therapy in recurrent/metastatic disease. Gynecol Oncol 2007; 106: 513-520.
9. Huang PH, Cavenee WK, Furnari FB, White FM. Uncovering therapeutic targets for glioblastoma: a systems biology approach. Cell Cycle 2007; 6: 2750-2754.
10. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005; 97: 339-346.
11. Sihto H, Puputti M, Pulli L, Tynninen O, Koskinen W, Aaltonen LM et al. Epidermal growth factor receptor domain II, IV, and kinase domain mutations in human solid tumors. J Mol Med 2005; 83: 976-983.
12. Gomez A, Wellbrock C, Gutbrod H, Dimitrijevic N, Schartl M. Ligand-independent dimerization and activation of the oncogenic Xmrk receptor by two mutations in the extracellular domain. J Biol Chem 2001; 276: 3333-3340.
13. Bardeesy N, Kim M, Xu J, Kim RS, Shen Q, Bosenberg MW et al. Role of epidermal growth factor receptor signaling in RAS-driven melanoma. Mol Cell Biol 2005; 25: 4176-4188.
14. Djerf EA, Trinks C, Abdiu A, Thunell LK, Hallbeck AL, Walz TM. ErbB receptor tyrosine kinases contribute to proliferation of malignant melanoma cells: inhibition by gefitinib (ZD1839). Melanoma Res 2009; 19: 156-166.
15. Singh B, Schneider M, Knyazev P, Ullrich A, UV-induced EGFR. signal transacti-vation is dependent on proligand shedding by activated metalloproteases in skin cancer cell lines. Int J Cancer 2009; 124: 531-539.
16. Boone B, Jacobs K, Ferdinande L, Taildeman J, Lambert J, Peeters M et al. EGFR in melanoma: clinical significance and potential therapeutic target. J Cutan Pathol 2011; 38: 492-502.
17. Krasagakis K, Garbe C, Zouboulis CC, Orfanos CE. Growth control of melanoma cells and melanocytes by cytokines. Recent Results Cancer Res 1995; 139: 169-182.
18. Singh B, Schneider M, Knyazev P, Ullrich A. UV-induced EGFR signal transactiva-tion is dependent on proligand shedding by activated metalloproteases in skin cancer cell lines. Int J Cancer 2009; 124: 531-539.
19. Akslen LA, Puntervoll H, Bachmann IM, Straume O, Vuhahula E, Kumar R et al. Mutation analysis of the EGFR-NRAS-BRAF pathway in melanomas from black Africans and other subgroups of cutaneous melanoma. Melanoma Res 2008; 18: 29-35.
20. de Wit PE, Moretti S, Koenders PG, Weterman MA, van Muijen GN, Gianotti B et al. Increasing epidermal growth factor receptor expression in human melanocytic tumor progression. J Invest Dermatol 1992; 99: 168-173.
21. Mattei S, Colombo MP, Melani C, Silvani A, Parmiani G, Herlyn M. Expression of cytokine/growth factors and their receptors in human melanoma and melano-cytes. Int J Cancer 1994; 56: 853-857.
22. Sparrow LE, Heenan PJ. Differential expression of epidermal growth factor receptor in melanocytic tumours demonstrated by immunohistochemistry and mRNA in situ hybridization. Australas J Dermatol 1999; 40: 19-24.
23. Amin DN, Hida K, Bielenberg DR, Klagsbrun M. Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors. Cancer Res 2006; 66: 2173-2180.
24. Meierjohann S, Schartl M, Volff JN. Genetic, biochemical and evolutionary facets of Xmrk-induced melanoma formation in the fish Xiphophorus. Comp Biochem Physiol C Toxicol Pharmacol 2004; 138: 281-289.
25. Winnemoeller D, Wellbrock C, Schartl M. Activating mutations in the extracellular domain of the melanoma inducing receptor Xmrk are tumorigenic in vivo. Int J Cancer 2005; 117: 723-729.
26. Meierjohann S, Mueller T, Schartl M, Buehner M. A structural model of the extracellular domain of the oncogenic EGFR variant Xmrk. Zebrafish 2006; 3: 359-369.
27. Schartl M, Wilde B, Laisney JA, Taniguchi Y, Takeda S, Meierjohann S. A mutated EGFR is sufficient to induce malignant melanoma with genetic background-dependent histopathologies. J Invest Dermatol 2010; 130: 249-258.
28. Wittbrodt J, Shima A, Schartl M. Medaka-a model organism from the far East. Nat Rev Genet 2002; 3: 53-64.
29. Hong Y, Winkler C, Schartl M. Efficiency of cell culture derivation from blastula embryos and of chimera formation in the medaka (Oryzias latipes) depends on donor genotype and passage number. Dev Genes Evol 1998; 208: 595-602.
30. Hong Y, Liu T, Zhao H, Xu H, Wang W, Liu R et al. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci USA 2004; 101: 8011-8016.
31. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B et al. The medaka draft genome and insights into vertebrate genome evolution. Nature 2007; 447: 714-719.
32. Laisney JA, Braasch I, Walter RB, Meierjohann S, Schartl M. Lineage-specific co-evolution of the Egf receptor/ligand signaling system. BMC Evol Biol 2010; 10: 27.
33. Sihto H, Puputti M, Pulli L, Tynninen O, Koskinen W, Aaltonen LM et al. Epidermal growth factor receptor domain II, IV, and kinase domain mutations in human solid tumors. J Mol Med 2005; 83: 976-983.
34. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J et al. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004; 164: 769-779.
35. Meierjohann S, Wende E, Kraiss A, Wellbrock C, Schartl M. The oncogenic epidermal growth factor receptor variant Xiphophorus melanoma receptor kinase induces motility in melanocytes by modulation of focal adhesions. Cancer Res 2006; 66: 3145-3152.
36. Leikam C, Hufnagel A, Schartl M, Meierjohann S. Oncogene activation in mela-nocytes links reactive oxygen to multinucleated phenotype and senescence. Oncogene 2008; 27: 7070-7082.
37. Gomez A, Volff JN, Hornung U, Schartl M, Wellbrock C. Identification of a second egfr gene in Xiphophorus uncovers an expansion of the epidermal growth factor receptor family in fish. Mol Biol Evol 2004; 21: 266-275.
38. Nagy P, Arndt-Jovin DJ, Jovin TM. Small interfering RNAs suppress the expression of endogenous and GFP-fused epidermal growth factor receptor (erbB1) and induce apoptosis in erbB1-overexpressing cells. Exp Cell Res 2003; 285: 39-49.
39. Saxon ML, Lee DC. Mutagenesis reveals a role for epidermal growth factor receptor extracellular subdomain IV in ligand binding. J Biol Chem 1999; 274: 28356-28362.
40. Tao RH, Maruyama IN. All EGF (ErbB) receptors have preformed homo-and het-erodimeric structures in living cells. J Cell Sci 2008; 121(Part 19): 3207-3217.
41. Teutschbein J, Haydn JM, Samans B, Krause M, Eilers M, Schartl M et al. Gene expression analysis after receptor tyrosine kinase activation reveals new potential melanoma proteins. BMC Cancer 2010; 10: 386.
42. Joy AA, Butts CA. Extending outcomes: epidermal growth factor receptor-targeted monoclonal antibodies in non-small-cell lung cancer. Clin Lung Cancer 2009; 10(Suppl 1): S24-S29.
43. Gazdar AF. Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors. Oncogene 2009; 28(Suppl 1): S24-S31.
44. Astsaturov I, Cohen RB, Harari P. EGFR-targeting monoclonal antibodies in head and neck cancer. Curr Cancer Drug Targets 2007; 7: 650-665.
45. Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, Kerr D. Genetic prognostic and predictive markers in colorectal cancer. Nat Rev Cancer 2009; 9: 489-499.
46. Gan HK, Kaye AH, Luwor RB. The EGFRvIII variant in glioblastoma multiforme. J Clin Neurosci 2009; 16: 748-754.
47. Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V et al. Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol Cancer Res 2011; 9: 801-812.
48. Ramnarain DB, Park S, Lee DY, Hatanpaa KJ, Scoggin SO, Otu H et al. Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells. Cancer Res 2006; 66: 867-874.
49. Kansra S, Stoll SW, Johnson JL, Elder JT. Src family kinase inhibitors block amphiregulin-mediated autocrine ErbB signaling in normal human keratinocytes. Mol Pharmacol 2005; 67: 1145-1157.
50. Zhuang S, Kinsey GR, Rasbach K, Schnellmann RG. Heparin-binding epidermal growth factor and Src family kinases in proliferation of renal epithelial cells. Am J Physiol Renal Physiol 2008; 294: F459-F468.
51. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007; 26: 3291-3310.
52. McCarthy SA, Samuels ML, Pritchard CA, Abraham JA, McMahon M. Rapid induction of heparin-binding epidermal growth factor/diphtheria toxin receptor expression by Raf and Ras oncogenes. Genes Dev 1995; 9: 1953-1964.
53. Schulze A, Lehmann K, Jefferies HB, McMahon M. Downward J. Analysis of the transcriptional program induced by Raf in epithelial cells. Genes Dev 2001; 15: 981-994.
54. Li J, Ma C, Huang Y, Luo J, Huang C. Differential requirement of EGF receptor and its tyrosine kinase for AP-1 transactivation induced by EGF and TPA. Oncogene 2003; 22: 211-219.
55. Sakai M, Tsukada T, Harris RC. Oxidant stress activates AP-1 and heparin-binding epidermal growth factor-like growth factor transcription in renal epithelial cells. Exp Nephrol 2001; 9: 28-39.
56. Kitamura S, Miyazaki Y, Hiraoka S, Nagasawa Y, Toyota M, Takakura R et al. PPARgamma agonists inhibit cell growth and suppress the expression of cyclin D1 and EGF-like growth factors in ras-transformed rat intestinal epithelial cells. Int J Cancer 2001; 94: 335-342.
57. Li CW, Cheung W, Lin ZB, Li TY, Lim JT, Wang DY. Oral steroids enhance epithelial repair in nasal polyposis via upregulation of the AP-1 gene network. Thorax 2009; 64: 306-312.
58. Park JM, Adam RM, Peters CA, Guthrie PD, Sun Z, Klagsbrun M et al. AP-1 mediates stretch-induced expression of HB-EGF in bladder smooth muscle cells. Am J Physiol 1999; 277(2 Part 1): C294-C301.
59. Wellbrock C, Weisser C, Geissinger E, Troppmair J, Schartl M. Activation of p59(Fyn) leads to melanocyte dedifferentiation by influencing MKP-1-regulated mitogen-activated protein kinase signaling. J Biol Chem 2002; 277: 6443-6454.
60. Yotsumoto F, Yagi H, Suzuki SO, Oki E, Tsujioka H, Hachisuga T et al. Validation of HB-EGF and amphiregulin as targets for human cancer therapy. Biochem Biophys Res Commun 2008; 365: 555-561.
61. Riese II DJ, Gallo RM, Settleman J. Mutational activation of ErbB family receptor tyrosine kinases: insights into mechanisms of signal transduction and tumor-igenesis. Bioessays 2007; 29: 558-565.
62. Ward CW, Lawrence MC, Streltsov VA, Adams TE, McKern NM. The insulin and EGF receptor structures: new insights into ligand-induced receptor activation. Trends Biochem Sci 2007; 32: 129-137.
63. Dawson JP, Bu Z, Lemmon MA. Ligand-induced structural transitions in ErbB receptor extracellular domains. Structure 2007; 15: 942-954.
64. Mattoon D, Klein P, Lemmon MA, Lax I, Schlessinger J. The tethered configuration of the EGF receptor extracellular domain exerts only a limited control of receptor function. Proc Natl Acad Sci USA 2004; 101: 923-928.
65. Moriki T, Maruyama H, Maruyama IN. Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J Mol Biol 2001; 311: 1011-1026.
66. Wittbrodt J, Lammers R, Malitschek B, Ullrich A, Schartl M. The Xmrk receptor tyrosine kinase is activated in Xiphophorus malignant melanoma. EMBO J 1992; 11: 4239-4246.
67. Chen C. Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 1987; 7: 2745-2752.
68. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
69. Lu C, Mi LZ, Grey MJ, Zhu J, Graef E, Yokoyama S et al. Structural evidence for loose linkage between ligand binding and kinase activation in the epidermal growth factor receptor. Mol Cell Biol 2010; 30: 5432-5443.
70. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M, Kim JH et al. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 2002; 110: 775-787.