Mitogen-activated protein kinase phosphatase-1 (MKP-1) impairs the response to anti-epidermal growth factor receptor (EGFR) antibody cetuximab in metastatic colorectal cancer patients

British Journal of Cancer

Volumn 102, Issue 7, 2010, Pages 1137-1144

  Montagut, C ^a   Iglesias, M ^a,d   Arumi, M ^a,d   Bellosillo, B ^a   Gallen, M ^a   Martinez Fernandez, A ^a   Martinez Aviles, L ^a   Caadas I ^a   Dalmases, A ^a   Moragon, E ^a   Lema, L ^a   Serrano, S ^a,b   Rovira, A ^a   Rojo, F ^a,c   Bellmunt, J ^a,b,d   Albanell, J ^a,b  

^a HOSPITAL DEL MAR   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c Hospital UniversitarioFundación Jiménez Díaz   (Spain)

^d UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Cetuximab; CRC; MKP 1; Molecular marker; RAS

Indexed keywords

B RAF KINASE; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; IRINOTECAN; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; OXALIPLATIN;

ADULT; AGED; ANTIBODY RESPONSE; ARTICLE; CANCER CHEMOTHERAPY; CANCER PATIENT; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME INACTIVATION; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LOADING DRUG DOSE; MALE; METASTASIS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

AGED; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; DUAL SPECIFICITY PHOSPHATASE 1; FEMALE; HUMANS; MALE; MUTATION; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR MARKERS, BIOLOGICAL;

EID: 77950368212     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605612     Document Type: Article

References (57)

1. Albanell J, Codony-Servat J, Rojo F, Del Campo JM, Sauleda S, Anido J, Raspall G, Giralt J, Rosello J, Nicholson RI, Mendelsohn J, Baselga J (2001) Activated extracellular signal-regulated kinases: association with epidermal growth factor receptor/transforming growth factor alpha expression in head and neck squamous carcinoma and inhibition by anti-epidermal growth factor receptor treatments. Cancer Res 61: 6500-6510
2. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ, Juan T, Sikorski R, Suggs S, Radinsky R, Patterson SD, Chang DD (2008) Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol 26: 1626-1634
3. Baselga J (2006) Targeting tyrosine kinases in cancer: the second wave. Science 312: 1175-1178
4. Benvenuti S, Sartore-Bianchi A, Di Nicolantonio F, Zanon C, Moroni M, Veronese S, Siena S, Bardelli A (2007) Oncogenic activation of the RAS/ RAF signaling pathway impairs the response of metastatic colorectal cancers to anti-epidermal growth factor receptor antibody therapies. Cancer Res 67: 2643-2648
5. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, Olson Jr JA, Marks JR, Dressman HK, West M, Nevins JR (2006) Oncogenic pathways signatures in human cancers as a guide to targeted therapies. Nature 439: 353-357
6. Bokemeyer C, Bondarenko I, Makhson A, Hartmann JT, Aparicio J, de Braud F, Donea S, Ludwig H, Schuch G, Stroh C, Loos AH, Zubel A, Koralewski P (2009) Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the first-line treatment of metastatic colorectal cancer. J Clin Oncol 27: 663-671
7. Brondello JM, Pouyssegur J, McKenzie FR (1999) Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphory-lation. Science 286: 2514-2517
8. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, Bets D, Mueser M, Harstrick A, Verslype C, Chau I, Van Cutsem E (2004) Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med 351: 337-345 (Pubitemid 38944402) (Pubitemid 38944402)
9. Chu Y, Solski PA, Khosravi-Far R, Der CJ, Kelly K (1996) The mitogen-activated protein kinase phosphatases PAC1, MKP-1, and MKP-2 have unique substrate specificities and reduced activity in vivo toward the ERK2 sevenmaker mutation. J Biol Chem 271: 6497-6501
10. Chung KY, Shia J, Kemeny NE, Shah M, Schwartz GK, Tse A, Hamilton A, Pan D, Schrag D, Schwartz L, Klimstra DS, Fridman D, Kelsen DP, Saltz LB (2005) Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J Clin Oncol 23: 1803-1810
11. De Roock W, Jansenss M, Biesmans B, Jacobs J, De Schutter J, Fieuws E, Van Cutsem E, Tejpar S (2009) DUSPs as marker of MEK/Erk activation in primary colorectal cancer. J Clin Oncol 27: 15s. (abstr 4064)
12. De Roock W, Piessevaux H, De Schutter J, Janssens M, De Hertogh G, Personeni N, Biesmans B, Van Laethem JL, Peeters M, Humblet Y, Van Cutsem E, Tejpar S (2008) KRAS wild-type state predicts survival and is associated to early radiological response in metastatic colorectal cancer treated with cetuximab. Ann Oncol 19: 508-515
13. Dhillon AS, Hagan S, Rath O, Kolch W (2007) MAP kinase signalling pathways in cancer. Oncogene 26: 3279-3290
14. Di Fiore F, Blanchard F, Charbonnier F, Le Pessot F, Lamy A, Galais MP, Bastit L, Killian A, Sesboue R, Tuech JJ, Queuniet AM, Paillot B, Sabourin JC, Michot F, Michel P, Frebourg T (2007) Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by cetuximab plus chemotherapy. Br J Cancer 96: 1166-1169
15. Di Nicolantonio F, Martini M, Molinari F, Sartore-Bianchi A, Arena S, Saletti P, De Dosso S, Mazzucchelli L, Frattini M, Siena S, Bardelli A (2008) Wild-type BRAF is required for response to panitumumab or cetuximab in metastatic colorectal cancer. J Clin Oncol 26: 5705-5712
16. Frattini M, Saletti P, Romagnani E, Martin V, Molinari F, Ghisletta M, Camponovo A, Etienne LL, Cavalli F, Mazzucchelli L (2007) PTEN loss of expression predicts cetuximab efficacy in metastatic colorectal cancer patients. Br J Cancer 97: 1139-1145
17. Haigis KM, Kendall KR, Wang Y, Cheung A, Haigis MC, Glickman JN, Niwa-Kawakita M, Sweet-Cordero A, Sebolt-Leopold J, Shannon KM, Settleman J, Giovannini M, Jacks T (2008) Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation and tumor progression in the colon. Nat Genet 40: 600-608
18. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100: 57-70
19. Jacobs B, De Roock W, Piessevaux H, Van Oirbeek R, Biesmans B, De Schutter J, Fieuws S, Vandesompele J, Peeters M, Van Laethem JL, Humblet Y, Penault-Llorca F, De Hertogh G, Laurent-Puig P, Van Cutsem E, Tejpar S (2009) Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol 27: 5068-5074
20. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, Berry SR, Krahn M, Price T, Simes RJ, Tebbutt NC, van Hazel G, Wierzbicki R, Langer C, Moore MJ (2007) Cetuximab for the treatment of colorectal cancer. N Engl J Med 357: 2040-2048
21. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, Simes RJ, Chalchal H, Shapiro JD, Robitaille S, Price TJ, Shepherd L, Au HJ, Langer C, Moore MJ, Zalcberg JR (2008) K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 359: 1757-1765
22. Keyse SM (2008) Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev 27: 253-261
23. Khambata-Ford S, Garrett CR, Meropol NJ, Basik M, Harbison CT, Wu S, Wong TW, Huang X, Takimoto CH, Godwin AK, Tan BR, Krishnamurthi SS, Burris 3rd HA, Poplin EA, Hidalgo M, Baselga J, Clark EA, Mauro DJ (2007) Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol 25: 3230-3237
24. Li J, Gorospe M, Hutter D, Barnes J, Keyse SM, Liu Y (2001) Transcriptional induction of MKP-1 in response to stress is associated with histone H3 phosphorylation-acetylation. Mol Cell Biol 21: 8213-8224
25. Lievre A, Bachet JB, Boige V, Cayre A, Le Corre D, Buc E, Ychou M, Bouche O, Landi B, Louvet C, Andre T, Bibeau F, Diebold MD, Rougier P, Ducreux M, Tomasic G, Emile JF, Penault-Llorca F, Laurent-Puig P (2008) KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J Clin Oncol 26: 374-379
26. Lin YW, Chuang SM, Yang JL (2003) ERK1/2 achieves sustained activation by stimulating MAPK phosphatase-1 degradation via the ubiquitin-proteasome pathway. J Biol Chem 278: 21534-21541
27. Lin YW, Yang JL (2006) Cooperation of ERK and SCFSkp2 for MKP-1 destruction provides a positive feedback regulation of proliferating signaling. J Biol Chem 281: 915-926
28. Liu YX, Wang J, Guo J, Wu J, Lieberman HB, Yin Y (2008) DUSP1 is controlled by p53 during the cellular response to oxidative stress. Mol Cancer Res 6: 624-633
29. Loda M, Capodieci P, Mishra R, Yao H, Corless C, Grigioni W, Wang Y, Magi-Galluzzi C, Stork PJ (1996) Expression of mitogen-activated protein kinase phosphatase-1 in the early phases of human epithelial carcino-genesis. Am J Pathol 149: 1553-1564
30. Loupakis F, Pollina L, Stasi I, Ruzzo A, Scartozzi M, Santini D, Masi G, Graziano F, Cremolini C, Rulli E, Canestrari E, Funel N, Schiavon G, Petrini I, Magnani M, Tonini G, Campani D, Floriani I, Cascinu S, Falcone A (2009) PTEN expression and KRAS mutations on primary tumors and metastases in the prediction of benefit from cetuximab plus irinotecan for patients with metastatic colorectal cancer. J Clin Oncol 27: 2622-2629
31. McDermott U, Sharma SV, Dowell L, Greninger P, Montagut C, Lamb J, Archibald H, Raudales R, Tam A, Lee D, Rothenberg SM, Supko J, Sordella R, Ulkus LE, Maheswaran S, Njauw CN, Tsao H, Drew L, Hanke JH, Xiao-Jun M, Erlander MG, Gray N, Haber DA, Settleman J (2007) Identification of genotype-correlated sensitivity to selective kinase inhibitors using high-throughput tumor cell line profiling. Proc Natl Acad Sci USA 104: 19936-19941
32. Mendelsohn J, Baselga J (2006) Epidermal growth factor receptor targeting in cancer. Semin Oncol 33: 369-385 (Pubitemid 44142736) (Pubitemid 44142736)
33. Oden-Gangloff A, Di Fiore F, Bibeau F, Lamy A, Bougeard G, Charbonnier F, Blanchard F, Tougeron D, Ychou M, Boissiere F, Le Pessot F, Sabourin JC, Tuech JJ, Michel P, Frebourg T (2009) TP53 mutations predict disease control in metastatic colorectal cancer treated with cetuximab-based chemotherapy. Br J Cancer 100: 1330-1335
34. Ogino S, Nosho K, Kirkner GJ, Shima K, Irahara N, Kure S, Chan AT, Engelman JA, Kraft P, Cantley LC, Giovannucci EL, Fuchs CS (2009) PIK3CA mutation is associated with poor prognosis among patients with curatively resected colon cancer. J Clin Oncol 27: 1477-1484
35. Prenen H, De Schutter J, Jacobs B, De Roock W, Biesmans B, Claes B, Lambrechts D, Van Cutsem E, Tejpar S (2009) PIK3CA mutations are not a major determinant of resistance to the epidermal growth factor receptor inhibitor cetuximab in metastatic colorectal cancer. Clin Cancer Res 15: 3184-3188
36. Richman SD, Seymour MT, Chambers P, Elliot F, Daly CL, Meade AM, Taylor G, Barrett JH, Quirke P (2009) KRAS and BRAF mutations in advanced colorectal cancer are associated with poor prognosis but do not preclude benefit from oxaliplatin or irinotecan: results from the MRC FOCUS trial. J Clin Oncol 27: 5931-5937
37. Rojo F, Gonzalez-Navarrete I, Bragado R, Dalmases A, Menendez S, Cortes-Sempere M, Suarez C, Oliva C, Servitja S, Rodriguez-Fanjul V, Sanchez-Perez I, Campas C, Corominas JM, Tusquets I, Bellosillo B, Serrano S, Perona R, Rovira A, Albanell J (2009) Mitogen-activated protein kinase phosphatase-1 in human breast cancer independently predicts prognosis and is repressed by doxorubicin. Clin Cancer Res 15: 3530-3539
38. Roth AD, Tejpar S, Delorenzi M, Yan P, Fiocca R, Klingbiel D, Dietrich D, Biesmans B, Bodoky G, Barone C, Aranda E, Nordlinger B, Cisar L, Labianca R, Cunningham D, Van Cutsem E, Bosman F (2010) Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study on the PETACC-3, EORTC 40993, SAKK 60-00 trial. J Clin Oncol 28: 466-474
39. Saltz LB, Meropol NJ, Loehrer Sr PJ, Needle MN, Kopit J, Mayer RJ (2004) Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J Clin Oncol 22: 1201-1208
40. Sanchez-Perez I, Martinez-Gomariz M, Williams D, Keyse SM, Perona R (2000) CL100/MKP-1 modulates JNK activation and apoptosis in response to cisplatin. Oncogene 19: 5142-5152
41. Sanchez-Perez I, Murguia JR, Perona R (1998) Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene 16: 533-540
42. Sartore-Bianchi A, Martini M, Molinari F, Veronese S, Nichelatti M, Artale S, Di Nicolantonio F, Saletti P, De Dosso S, Mazzucchelli L, Frattini M, Siena S, Bardelli A (2009) PIK3CA mutations in colorectal cancer are associated with clinical resistance to EGFR-targeted monoclonal antibodies. Cancer Res 69: 1851-1857
43. Small GW, Shi YY, Edmund NA, Somasundaram S, Moore DT, Orlowski RZ (2004) Evidence that mitogen-activated protein kinase phosphatase-1 induction by proteasome inhibitors plays an antiapoptotic role. Mol Pharmacol 66: 1478-1490
44. Small GW, Shi YY, Higgins LS, Orlowski RZ (2007) Mitogen-activated protein kinase phosphatase-1 is a mediator of breast cancer chemo-resistance. Cancer Res 67: 4459-4466
45. Takeuchi K, Ito F (2010) EGF receptor in relation to tumor development: molecular basis of responsiveness of cancer cells to EGFR-targeting tyrosine kinase inhibitors. Febs J 277: 316-326
46. Takeuchi K, Shin-ya T, Nishio K, Ito F (2009) Mitogen-activated protein kinase phosphatase-1 modulated JNK activation is critical for apoptosis induced by inhibitor of epidermal growth factor receptor-tyrosine kinase. FEBS J 276: 1255-1265
47. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92: 205-216
48. Tol J, Nagtegaal ID, Punt CJ (2009) BRAF mutation in metastatic colorectal cancer. N Engl J Med 361: 98-99
49. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A, D'Haens G, Pinter T, Lim R, Bodoky G, Roh JK, Folprecht G, Ruff P, Stroh C, Tejpar S, Schlichting M, Nippgen J, Rougier P (2009) Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 360: 1408-1417
50. Van Cutsem E, Peeters M, Siena S, Humblet Y, Hendlisz A, Neyns B, Canon JL, Van Laethem JL, Maurel J, Richardson G, Wolf M, Amado RG (2007) Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer. J Clin Oncol 25: 1658-1664
51. Vicent S, Garayoa M, Lopez-Picazo JM, Lozano MD, Toledo G, Thunnissen FB, Manzano RG, Montuenga LM (2004) Mitogen-activated protein kinase phosphatase-1 is overexpressed in non-small cell lung cancer and is an independent predictor of outcome in patients. Clin Cancer Res 10: 3639-3649
52. Wang J, Zhou JY, Wu GS (2007) ERK-dependent MKP-1-mediated cisplatin resistance in human ovarian cancer cells. Cancer Res 67: 11933-11941
53. Wang Z, Xu J, Zhou JY, Liu Y, Wu GS (2006) Mitogen-activated protein kinase phosphatase-1 is required for cisplatin resistance. Cancer Res 66: 8870-8877
54. Workman P, de Bono J (2008) Targeted therapeutics for cancer treatment: major progress towards personalised molecular medicine. Curr Opin Pharmacol 8: 359-362
55. Wu GS (2007) Role of mitogen-activated protein kinase phosphatases (MKPs) in cancer. Cancer Metastasis Rev 26: 579-585
56. Xing J, Ginty DD, Greenberg ME (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273: 959-963
57. Yang H, Wu GS (2004) p53 Transactivates the phosphatase MKP1 through both intronic and exonic p53 responsive elements. Cancer Biol Ther 3: 1277-1282