Integrated genomic analysis of colorectal cancer progression reveals activation of EGFR through demethylation of the EREG promoter

Oncogene

Volumn 35, Issue 50, 2016, Pages 6403-6415

  Qu, X ^a   Sandmann, T ^a   Frierson, H ^a   Fu, L ^a   Fuentes, E ^a   Walter, K ^a   Okrah, K ^a   Rumpel, C ^b   Moskaluk, C ^b   Lu, S ^a   Wang, Y ^a   Bourgon, R ^a   Penuel, E ^a   Pirzkall, A ^a   Amler, L ^a   Lackner, M R ^a   Tabernero, J ^c   Hampton, G M ^a   Kabbarah, O ^a  

^a GENENTECH INC   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; AZACITIDINE; DECITABINE; EPIREGULIN; EREG PROTEIN, HUMAN;

ADENOMA; ARTICLE; BLADDER CANCER; CANCER GROWTH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; CRYPT CELL; DEMETHYLATION; DRUG SENSITIZATION; EPIGENETICS; EPITHELIUM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENOMICS; HEAD AND NECK CANCER; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; LUNG CANCER; METASTASIS; METHYLATION; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; STAINING; TREATMENT RESPONSE; UPREGULATION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; COLORECTAL NEOPLASMS; DISEASE COURSE; DNA METHYLATION; GENETICS; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

AZACITIDINE; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; DNA METHYLATION; EPIREGULIN; HUMANS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84976308262     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.170     Document Type: Article

References (56)

1. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-767.
2. de Santa Barbara P, van den Brink GR, Roberts DJ. Development and differentiation of the intestinal epithelium. Cell Mol Life Sci 2003; 60: 1322-1332.
3. de Lau W, Barker N, Clevers H. WNT signaling in the normal intestine and colorectal cancer. Front Biosci 2007; 12: 471-491.
4. Gryfe R, Swallow C, Bapat B, Redston M, Gallinger S, Couture J. Molecular biology of colorectal cancer. Curr Probl Cancer 1997; 21: 233-300.
5. Nathke IS. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 2004; 20: 337-366.
6. Oving IM, Clevers HC. Molecular causes of colon cancer. Eur J Clin Invest 2002; 32: 448-457.
7. Pasparakis M. Role of NF-kappaB in epithelial biology. Immunol Rev 2012; 246: 346-358.
8. Skeen VR, Paterson I, Paraskeva C, Williams AC. TGF-beta1 signalling, connecting aberrant inflammation and colorectal tumorigenesis. Curr Pharm Des 2012; 18: 3874-3888.
9. van Es JH, Clevers H. Notch and Wnt inhibitors as potential new drugs for intestinal neoplastic disease. Trends Mol Med 2005; 11: 496-502.
10. Watt FM. Unexpected Hedgehog-Wnt interactions in epithelial differentiation. Trends Mol Med 2004; 10: 577-580.
11. Grady WM, Markowitz SD. Genetic and epigenetic alterations in colon cancer. Annu Rev Genom Hum Genet 2002; 3: 101-128.
12. Luo Y, Wong CJ, Kaz AM, Dzieciatkowski S, Carter KT, Morris SM et al. Differences in DNA methylation signatures reveal multiple pathways of progression from adenoma to colorectal cancer. Gastroenterology 2014; 147: e418.
13. 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.
14. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487: 330-337.
15. Yao YL, Shao J, Zhang C, Wu JH, Zhang QH, Wang JJ et al. Proliferation of colorectal cancer is promoted by two signaling transduction expression patterns: ErbB2/ErbB3/AKT and MET/ErbB3/MAPK. PLoS One 2013; 8: e78086.
16. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M et al. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol 2010; 28: 4697-4705.
17. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004; 350: 2335-2342.
18. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009; 360: 1408-1417.
19. Lievre A, Bachet JB, Boige V, Cayre A, Le Corre D, Buc E et al. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J Clin Oncol 2008; 26: 374-379.
20. Peeters M, Douillard JY, Van Cutsem E, Siena S, Zhang K, Williams R et al. Mutant KRAS codon 12 and 13 alleles in patients with metastatic colorectal cancer: assessment as prognostic and predictive biomarkers of response to panitumumab. J Clin Oncol 2013; 31: 759-765.
21. Pentheroudakis G, Kotoula V, De Roock W, Kouvatseas G, Papakostas P, Makatsoris T et al. Biomarkers of benefit from cetuximab-based therapy in metastatic colorectal cancer: interaction of EGFR ligand expression with RAS/RAF, PIK3CA genotypes. BMC Cancer 2013; 13: 49.
22. Price TJ, Hardingham JE, Lee CK, Weickhardt A, Townsend AR, Wrin JW et al. Impact of KRAS and BRAF gene mutation status on outcomes from the phase III AGITG MAX Trial of capecitabine alone or in combination with bevacizumab and mitomycin in advanced colorectal cancer. J Clin Oncol 2011; 29: 2675-2682.
23. Di Nicolantonio F, Martini M, Molinari F, Sartore-Bianchi A, Arena S, Saletti P et al. Wild-type BRAF is required for response to panitumumab or cetuximab in metastatic colorectal cancer. J Clin Oncol 2008; 26: 5705-5712.
24. Khambata-Ford S, Garrett CR, Meropol NJ, Basik M, Harbison CT, Wu S et al. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol 2007; 25: 3230-3237.
25. Jonker DJ, Karapetis CS, Harbison C, O'Callaghan CJ, Tu D, Simes RJ et al. Epiregulin gene expression as a biomarker of benefit from cetuximab in the treatment of advanced colorectal cancer. Br J Cancer 2014; 110: 648-655.
26. Jones S, Chen WD, Parmigiani G, Diehl F, Beerenwinkel N, Antal T et al. Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci USA 2008; 105: 4283-4288.
27. Makky K, Tekiela J, Mayer AN. Target of rapamycin (TOR) signaling controls epithelial morphogenesis in the vertebrate intestine. Dev Biol 2007; 303: 501-513.
28. Sancho E, Batlle E, Clevers H. Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol 2004; 20: 695-723.
29. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6: 479-507.
30. Bourgon R, Lu S, Yan Y, Lackner MR, Wang W, Weigman V et al. High-throughput detection of clinically relevant mutations in archived tumor samples by multiplexed PCR and next-generation sequencing. Clin Cancer Res 2014; 20: 2080-2091.
31. Zhang H, Berezov A, Wang Q, Zhang G, Drebin J, Murali R et al. ErbB receptors: from oncogenes to targeted cancer therapies. J Clin Invest 2007; 117: 2051-2058.
32. Yonesaka K, Zejnullahu K, Lindeman N, Homes AJ, Jackman DM, Zhao F et al. Autocrine production of amphiregulin predicts sensitivity to both gefitinib and cetuximab in EGFR wild-type cancers. Clin Cancer Res 2008; 14: 6963-6973.
33. Oshima G, Wennerberg J, Yamatodani T, Kjellen E, Mineta H, Johnsson A et al. Autocrine epidermal growth factor receptor ligand production and cetuximab response in head and neck squamous cell carcinoma cell lines. J Cancer Res Clin Oncol 2012; 138: 491-499.
34. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz Jr LA, Kinzler KW. Cancer genome landscapes. Science (New York, NY) 2013; 339: 1546-1558.
35. Akiyama Y, Watkins N, Suzuki H, Jair KW, van Engeland M, Esteller M et al. GATA-4 and GATA-5 transcription factor genes and potential downstream antitumor target genes are epigenetically silenced in colorectal and gastric cancer. Mol Cell Biol 2003; 23: 8429-8439.
36. Orre LM, Panizza E, Kaminskyy VO, Vernet E, Graslund T, Zhivotovsky B et al. S100A4 interacts with p53 in the nucleus and promotes p53 degradation. Oncogene 2013; 32: 5531-5540.
37. Kohsaka S, Hinohara K, Wang L, Nishimura T, Urushido M, Yachi K et al. Epiregulin enhances tumorigenicity by activating the ERK/MAPK pathway in glioblastoma. Neuro-oncology 2014; 16: 960-970.
38. Auf G, Jabouille A, Delugin M, Guerit S, Pineau R, North S et al. High epiregulin expression in human U87 glioma cells relies on IRE1alpha and promotes autocrine growth through EGF receptor. BMC Cancer 2013; 13: 597.
39. Komurasaki T, Toyoda H, Uchida D, Nemoto N. Mechanism of growth promoting activity of epiregulin in primary cultures of rat hepatocytes. Growth Factors (Chur, Switzerland) 2002; 20: 61-69.
40. Walter K, Holcomb T, Januario T, Du P, Evangelista M, Kartha N et al. DNA methylation profiling defines clinically relevant biological subsets of non-small cell lung cancer. Clin Cancer Res 2012; 18: 2360-2373.
41. Jover R, Nguyen TP, Perez-Carbonell L, Zapater P, Paya A, Alenda C et al. 5-Fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer. Gastroenterology 2011; 140: 1174-1181.
42. Shen L, Catalano PJ, Benson AB III, O'Dwyer P, Hamilton SR, Issa JP. Association between DNA methylation and shortened survival in patients with advanced colorectal cancer treated with 5-fluorouracil based chemotherapy. Clin Cancer Res 2007; 13: 6093-6098.
43. Seniski GG, Camargo AA, Ierardi DF, Ramos EA, Grochoski M, Ribeiro ES et al. ADAM33 gene silencing by promoter hypermethylation as a molecular marker in breast invasive lobular carcinoma. BMC Cancer 2009; 9: 80.
44. Weng WH, Leung WH, Pang YJ, Hsu HH. Lauric acid can improve the sensitization of Cetuximab in KRAS/BRAF mutated colorectal cancer cells by retrievable microRNA-378 expression. Oncol Rep 2016; 35: 107-116.
45. Sun JZ, Lu Y, Xu Y, Liu F, Li FQ, Wang QL et al. Epidermal growth factor receptor expression in acute myelogenous leukaemia is associated with clinical prognosis. Hematol Oncol 2012; 30: 89-97.
46. Riese DJ 2nd, Cullum RL. Epiregulin: roles in normal physiology and cancer. Semin Cell Dev Biol 2014; 28: 49-56.
47. Deangelo DJ, Neuberg D, Amrein PC, Berchuck J, Wadleigh M, Sirulnik LA et al. A phase II study of the EGFR inhibitor gefitinib in patients with acute myeloid leukemia. Leuk Res 2014; 38: 430-434.
48. Lainey E, Wolfromm A, Marie N, Enot D, Scoazec M, Bouteloup C et al. Azacytidine and erlotinib exert synergistic effects against acute myeloid leukemia. Oncogene 2013; 32: 4331-4342.
49. Hansen AR, Siu LL. Epidermal growth factor receptor targeting in head and neck cancer: have we been just skimming the surface? J Clin Oncol 2013; 31: 1381-1383.
50. Busser B, Sancey L, Brambilla E, Coll JL, Hurbin A. The multiple roles of amphiregulin in human cancer. Biochim Biophys Acta 2011; 1816: 119-131.
51. Revillion F, Lhotellier V, Hornez L, Bonneterre J, Peyrat JP. ErbB/HER ligands in human breast cancer, and relationships with their receptors, the bio-pathological features and prognosis. Ann Oncol 2008; 19: 73-80.
52. Troiani T, Martinelli E, Napolitano S, Vitagliano D, Ciuffreda LP, Costantino S et al. Increased TGF-alpha as a mechanism of acquired resistance to the anti-EGFR inhibitor cetuximab through EGFR-MET interaction and activation of MET signaling in colon cancer cells. Clin Cancer Res 2013; 19: 6751-6765.
53. Neufert C, Becker C, Türeci Ö, Waldner MJ, Backert I, Floh K et al. Tumor fibroblastderived epiregulin promotes growth of colitis-associated neoplasms through ERK. J Clin Invest 2013; 123: 1428-1443.
54. Rebouissou S, Bernard-Pierrot I, de Reynies A, Lepage ML, Krucker C, Chapeaublanc E et al. EGFR as a potential therapeutic target for a subset of muscle-invasive bladder cancers presenting a basal-like phenotype. Sci Transl Med 2014; 6: 244-291.
55. Yun J, Song SH, Park J, Kim HP, Yoon YK, Lee KH et al. Gene silencing of EREG mediated by DNA methylation and histone modification in human gastric cancers. Lab Invest 2012; 92: 1033-1044.
56. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31: e15.