Cetuximab induces eme1-mediated DNA repair: A novel mechanism for cetuximab resistance

Neoplasia (United States)

Volumn 16, Issue 3, 2014, Pages 207-220.e4

  Weinandy, Agnieszka ^a   Piroth, Marc D ^a   Goswami, Anand ^a   Nolte, Kay ^a   Sellhaus, Bernd ^a   Gerardo Nava, Jose ^a   Eble, Michael ^a   Weinandy, Stefan ^a   Cornelissen, Christian ^a   Clusmann, Hans ^a   Lüscher, Bernhard ^a   Weis, Joachim ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN P53; STAT3 PROTEIN; ANTINEOPLASTIC AGENT; DEOXYRIBONUCLEASE; DNA; EME1 PROTEIN, HUMAN; MONOCLONAL ANTIBODY; PROTEIN KINASE B; STAT3 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER RADIOTHERAPY; CELL COUNTING; CELL CULTURE; CELL LYSATE; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; COMET ASSAY; CONTROLLED STUDY; DNA REPAIR; DNA SYNTHESIS; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; GLIOBLASTOMA; METABOLISM; PATHOLOGY; PROTEIN STABILITY; RADIATION RESPONSE; TUMOR CELL CULTURE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; DNA; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; ENDODEOXYRIBONUCLEASES; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; STAT3 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 84900399061     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.03.004     Document Type: Article

References (56)

1. Maurizi M, Almadori G, Ferrandina G, Distefano M, Romanini ME, Cadoni G, Benedetti-Panici P, Paludetti G, Scambia G, and Mancuso S (1996). Prognostic significance of epidermal growth factor receptor in laryngeal squamous cell carcinoma. Br J Cancer 74, 1253-1257.
2. Normanno N, Bianco C, De Luca A, Maiello MR, and Salomon DS (2003). Target-based agents against ErbB receptors and their ligands: a novel approach to cancer treatment. Endocr Relat Cancer 10, 1-21.
3. Li S, Schmitz KR, Jeffrey PD, Wiltzius JJ, Kussie P, and Ferguson KM (2005). Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7, 301-311.
4. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, Bets D, Mueser M, Harstrick A, and Verslype C, et al (2004). Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med 351, 337-345.
5. Glynne-Jones R, Mawdsley S, and Harrison M (2010). Cetuximab and chemoradiation for rectal cancer-is the water getting muddy? Acta Oncol 49, 278-286.
6. Wheeler DL, Huang S, Kruser TJ, Nechrebecki MM, Armstrong EA, Benavente S, Gondi V, Hsu KT, and Harari PM (2008). Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 27, 3944-3956.
7. Saridaki Z, Tzardi M, Papadaki C, Sfakianaki M, Pega F, Kalikaki A, Tsakalaki E, Trypaki M, Messaritakis I, and Stathopoulos E, et al (2011). Impact of KRAS, BRAF, PIK3CA mutations, PTEN, AREG, EREG expression and skin rash in ≥ 2nd line cetuximab-based therapy of colorectal cancer patients. PLoS One 6, e15980.
8. Engelman JA and Jänne PA (2008). Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 14, 2895-2899.
9. Helleday T, Petermann E, Lundin C, Hodgson B, and Sharma RA (2008). DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8, 193-204.
10. Rouse J and Jackson SP (2002). Interfaces between the detection, signaling, and repair of DNA damage. Science 297, 547-551.
11. Golla RM, Li M, Shen Y, Ji M, Yan Y, Fu K, Greiner TC, McKeithan TW, and Chan WC (2012). Inhibition of poly(ADP-ribose) polymerase (PARP) and ataxia telangiectasia mutated (ATM) on the chemosensitivity of mantle cell lymphoma to agents that induce DNA strand breaks. Hematol Oncol 30, 175-179.
12. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, Mortimer P, Swaisland H, Lau A, and O'Connor MJ, et al (2009). Inhibition of poly (ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361, 123-134.
13. Nowsheen S, Bonner JA, Lobuglio AF, Trummell H, Whitley AC, Dobelbower MC, and Yang ES (2011). Cetuximab augments cytotoxicity with poly (adp-ribose) polymerase inhibition in head and neck cancer. PLoS One 6, e24148.
14. Ciccia A, Constantinou A, and West SC (2003). Identification and characterization of the human Mus81-Eme1 endonuclease. J Biol Chem 278, 25172-25178.
15. Abraham J, Lemmers B, Hande MP, Moynahan ME, Chahwan C, Ciccia A, Essers J, Hanada K, Chahwan R, and Khaw AK, et al (2003). Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J 22, 6137-6147.
16. Jhawer M, Goel S, Wilson AJ, Montagna C, Ling YH, Byun DS, Nasser S, Arango D, Shin J, and Klampfer L, et al (2008). PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res 68, 1953-1961.
17. Dreier A, Barth S, Goswami A, and Weis J (2012). Cetuximab induces mitochondrial translocalization of EGFRvIII, but not EGFR: involvement of mitochondria in tumor drug resistance? Tumour Biol 33, 85-94.
18. Meira DD, de Almeida VH, Mororo JS, Nobrega I, Bardella L, Silva RL, Albano RM, and Ferreira CG (2009). Combination of cetuximab with chemoradiation, trastuzumab or MAPK inhibitors: mechanisms of sensitisation of cervical cancer cells. Br J Cancer 101, 782-791.
19. Matar P, Rojo F, Cassia R, Moreno-Bueno G, Di Cosimo S, Tabernero J, Guzman M, Rodriguez S, Arribas J, and Palacios J, et al (2004). Combined epidermal growth factor receptor targeting with the tyrosine kinase inhibitor gefitinib (ZD1839) and the monoclonal antibody cetuximab (IMC-C225): superiority over single-agent receptor targeting. Clin Cancer Res 10, 6487-6501.
20. Dhupkar P, Dowling M, Cengel K, and Chen B (2010). Effects of anti-EGFR antibody cetuximab on androgen-independent prostate cancer cells. Anticancer Res 30, 1905-1910.
21. Brantley EC and Benveniste EN (2008). Signal transducer and activator of transcription-3: a molecular hub for signaling pathways in gliomas. Mol Cancer Res 6, 675-684.
22. Shodeinde AL and Barton BE (2012). Potential use of STAT3 inhibitors in targeted prostate cancer therapy: future prospects. Onco Targets Ther 5, 119-125.
23. Schust J, Sperl B, Hollis A, Mayer TU, and Berg T (2006). Stattic: a smallmolecule inhibitor of STAT3 activation and dimerization. Chem Biol 13, 1235-1242.
24. Macallan DC, Fullerton CA, Neese RA, Haddock K, Park SS, and Hellerstein MK (1998). Measurement of cell proliferation by labeling of DNA with stable isotope-labeled glucose: studies in vitro, in animals, and in humans. Proc Natl Acad Sci U S A 95, 708-713.
25. Roos WP and Kaina B (2006). DNA damage-induced cell death by apoptosis. Trends Mol Med 12, 440-450.
26. Vigneron A, Gamelin E, and Coqueret O (2008). The EGFR-STAT3 oncogenic pathway up-regulates the Eme1 endonuclease to reduce DNA damage after topoisomerase I inhibition. Cancer Res 68, 815-825.
27. Osman F and Whitby MC (2007). Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst) 6, 1004-1017.
28. Dikshit P, Goswami A, Mishra A, Chatterjee M, and Jana NR (2006). Curcumin induces stress response, neurite outgrowth and prevent NF-κB activation by inhibiting the proteasome function. Neurotox Res 9, 29-37.
29. Jana NR, Zemskov EA, Wang G, and Nukina N (2001). Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10, 1049-1059.
30. Forment JV, Blasius M, Guerini I, and Jackson SP (2011). Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation. PLoS One 6, e23517.
31. Barry SP, Townsend PA, Knight RA, Scarabelli TM, Latchman DS, and Stephanou A (2010). STAT3 modulates the DNA damage response pathway. Int J Exp Pathol 91, 506-514.
32. Katsumi S, Kobayashi N, Imoto K, Nakagawa A, Yamashina Y, Muramatsu T, Shirai T, Miyagawa S, Sugiura S, and Hanaoka F, et al (2001). In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts. J Invest Dermatol 117, 1156-1161.
33. Moné MJ, Volker M, Nikaido O, Mullenders LH, van Zeeland AA, Verschure PJ, Manders EM, and van Driel R (2001). Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep 2, 1013-1017.
34. Thacker J (1986). The nature of mutants induced by ionising radiation in cultured hamster cells. III. Molecular characterization of HPRT-deficient mutants induced by γ-rays or α-particles showing that the majority have deletions of all or part of the hprt gene. Mutat Res 160, 267-275.
35. Hasselbalch B, Lassen U, Hansen S, Holmberg M, Sorensen M, Kosteljanetz M, Broholm H, Stockhausen MT, and Poulsen HS (2010). Cetuximab, bevacizumab, and irinotecan for patients with primary glioblastoma and progression after radiation therapy and temozolomide: a phase II trial. Neuro Oncol 12, 508-516.
36. Carey LA, Rugo HS, Marcom PK, Mayer EL, Esteva FJ, Ma CX, Liu MC, Storniolo AM, Rimawi MF, and Forero-Torres A, et al (2012). TBCRC 001: randomized phase II study of cetuximab in combination with carboplatin in stage IV triple-negative breast cancer. J Clin Oncol 30, 2615-2623.
37. Salomon DS, Brandt R, Ciardiello F, and Normanno N (1995). Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 19, 183-232.
38. Huang SM, Bock JM, and Harari PM (1999). Epidermal growth factor receptor blockade with C225 modulates proliferation, apoptosis, and radiosensitivity in squamous cell carcinomas of the head and neck. Cancer Res 59, 1935-1940.
39. Lu Y, Liang K, Li X, and Fan Z (2007). Responses of cancer cells with wild-type or tyrosine kinase domain-mutated epidermal growth factor receptor (EGFR) to EGFR-targeted therapy are linked to downregulation of hypoxia-inducible factor-1α. Mol Cancer 6, 63.
40. Mora LB, Buettner R, Seigne J, Diaz J, Ahmad N, Garcia R, Bowman T, Falcone R, Fairclough R, and Cantor A, et al (2002). Constitutive activation of Stat3 in human prostate tumors and cell lines: direct inhibition of Stat3 signaling induces apoptosis of prostate cancer cells. Cancer Res 62, 6659-6666.
41. Wu K, Chang Q, Lu Y, Qiu P, Chen B, Thakur C, Sun J, Li L, Kowluru A, and Chen F (2013). Gefitinib resistance resulted from STAT3-mediated Akt activation in lung cancer cells. Oncotarget 4, 2430-2438.
42. Li C, Iida M, Dunn EF, Ghia AJ, and Wheeler DL (2009). Nuclear EGFR contributes to acquired resistance to cetuximab. Oncogene 28, 3801-3813.
43. Lo HW, Hsu SC, Ali-Seyed M, Gunduz M, Xia W, Wei Y, Bartholomeusz G, Shih JY, and Hung MC (2005). Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 7, 575-589.
44. Sen M, Joyce S, Panahandeh M, Li C, Thomas SM, Maxwell J, Wang L, Gooding WE, Johnson DE, and Grandis JR (2012). Targeting Stat3 Abrogates EGFR Inhibitor Resistance in Cancer. Clin Cancer Res 18, 4986-4996.
45. Ciccia A, McDonald N, and West SC (2008). Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77, 259-287.
46. Ciccia A and Elledge SJ (2010). The DNA damage response: making it safe to play with knives. Mol Cell 40, 179-204.
47. Dominguez-Kelly R, Martin Y, Koundrioukoff S, Tanenbaum ME, Smits VA, Medema RH, Debatisse M, and Freire R (2011). Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J Cell Biol 194, 567-579.
48. Ryu SH, Lee SW, Yang YJ, Song SY, Kim JH, Choi EK, and Ahn SD (2012). Intracytoplasmic epidermal growth factor receptor shows poor response to the cetuximab antitumor effect in irradiated non-small cell lung cancer cell lines. Lung Cancer 77, 482-487.
49. Huang S, Benavente S, Armstrong EA, Li C, Wheeler DL, and Harari PM (2011). p53 modulates acquired resistance to EGFR inhibitors and radiation. Cancer Res 71, 7071-7079.
50. Tomoda Y, Katsura M, Okajima M, Hosoya N, Kohno N, and Miyagawa K (2009). Functional evidence for Eme1 as a marker of cisplatin resistance. Int J Cancer 124, 2997-3001.
51. McHugh PJ, Spanswick VJ, and Hartley JA (2001). Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2, 483-490.
52. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, and Kanaar R (2006). The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 25, 4921-4932.
53. de Gruijl FR, van Kranen HJ, and Mullenders LH (2001). UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J Photochem Photobiol B 63, 19-27.
54. Wang TC and Smith KC (1986). Postreplication repair in ultraviolet-irradiated human fibroblasts: formation and repair of DNA double-strand breaks. Carcinogenesis 7, 389-392.
55. Thompson LH and Schild D (2001). Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat Res 477, 131-153.
56. Nieder C, Pawinski A, Dalhaug A, and Andratschke N (2012). A review of clinical trials of cetuximab combined with radiotherapy for non-small cell lung cancer. Radiat Oncol 7, 3.