Hsa-miR-31-3p expression is linked to progression-free survival in patients with KRAS wild-type metastatic colorectal cancer treated with anti-EGFR therapy

Clinical Cancer Research

Volumn 20, Issue 12, 2014, Pages 3338-3347

  Manceau, Gilles ^a,d   Imbeaud, Sandrine ^b   Thiébaut, Raphaële ^c   Liébaert, François ^c   Fontaine, Karine ^c   Rousseau, Francis ^c   Génin, Bérengère ^c   Le Corre, Delphine ^a   Didelot, Audrey ^a   Vincent, Marc ^a   Bachet, Jean Baptiste ^d   Chibaudel, Benoist ^e   Bouché, Olivier ^j   Landi, Bruno ^f   Bibeau, Frédéric ^k   Leroy, Karen ^g   Penault Llorca, Frédérique ^l   Van Laethem, Jean Luc ^m   Demetter, Pieter ⁿ   Tejpar, Sabine ^o   Rossi, Simona ^p   Mosakhani, Neda ^q   Österlund, Pia ^r   Ristamäki, Raija ^s   Sarhadi, Virinder ^r   Knuutila, Sakari ^q,r   Boige, Valérie ^a,h   André, Thierry ^e   Laurent Puig, Pierre ^a,i   more..

^a Therapeutic Implications Laboratoire d'Excellence GR Ex   (France)

^b INSERM   (France)

^c Integragen   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e HÔPITAL SAINT ANTOINE   (France)

^f HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^g HENRI MONDOR HOSPITAL   (France)

^h INSTITUT GUSTAVE ROUSSY   (France)

ⁱ ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^j UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^k CENTRE VAL D AURELLE   (France)

^l UNIVERSITÉ CLERMONT AUVERGNE   (France)

^m Department of Gastroenterology GI Cancer Unit   (United States)

ⁿ ERASME HOSPITAL   (Belgium)

^o UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^p SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^q UNIVERSITY OF HELSINKI   (Finland)

^r HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^s TURKU UNIVERSITY HOSPITAL   (Finland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CAPECITABINE; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; FLUOROURACIL; HSA MICRORNA 31 3P; IRINOTECAN; MICRORNA; OXALIPLATIN; PANITUMUMAB; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; KRAS PROTEIN, HUMAN; MIRN31 MICRORNA, HUMAN; ONCOPROTEIN; PARAFFIN; RAS PROTEIN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC SCREENING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; METASTATIC COLORECTAL CANCER; MIDDLE AGED; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RISK ASSESSMENT; SURVIVAL PREDICTION; WILD TYPE; YOUNG ADULT; ANTAGONISTS AND INHIBITORS; CANCER STAGING; COLORECTAL NEOPLASMS; FOLLOW UP; GENETICS; LIVER NEOPLASMS; MORTALITY; MUTATION; PATHOLOGY; PROGNOSIS; PROSPECTIVE STUDY; RETROSPECTIVE STUDY; SECONDARY; SURVIVAL RATE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; COLORECTAL NEOPLASMS; FEMALE; FOLLOW-UP STUDIES; HUMANS; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; MUTATION; NEOPLASM STAGING; PARAFFIN EMBEDDING; PROGNOSIS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETROSPECTIVE STUDIES; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 84902664252     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2750     Document Type: Article

References (45)

1. van der Pool AE, Damhuis RA, Ijzermans JN, de Wilt JH, Eggermont AM, Kranse R, et al. Trends in incidence, treatment and survival of patients with stage IV colorectal cancer: a population-based series. Colorectal Dis 2012;14:56-61.
2. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011;39: D945 -50.
3. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ, et al. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol 2008;26: 1626-34.
4. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008;359:1757-65.
5. Tol J, Koopman M, Cats A, Rodenburg CJ, Creemers GJ, Schrama JG, et al. Chemotherapy, bevacizumab, and cetuximab in metastatic colorectal cancer. N Engl J Med 2009;360:563-72.
6. Peeters M, Price TJ, Cervantes A, Sobrero AF, Ducreux M, Hotko Y, et al. Randomized phase III study of panitumumab with fluorouracil, leucovorin, and irinotecan (FOLFIRI) compared with FOLFIRI alone as second-line treatment in patients with metastatic colorectal cancer. J Clin Oncol 2010;28:4706-13.
7. Ocvirk J, Brodowicz T, Wrba F, Ciuleanu TE, Kurteva G, Beslija S, et al. Cetuximab plus FOLFOX6 or FOLFIRI in metastatic colorectal cancer: CECOG trial. World J Gastroenterol 2010;16:3133-43.
8. 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; 28:4697-705.
9. Bokemeyer C, Bondarenko I, Hartmann JT, de Braud F, Schuch G, Zubel A, et al. Efficacy according to biomarker status of cetuximab plus FOLFOX-4 as first-line treatment for metastatic colorectal cancer: the OPUS study. Ann Oncol 2011;22:1535-46.
10. Van Cutsem E, Kohne CH, Lang I, Folprecht G, Nowacki MP, Cascinu S, et al. Cetuximab plus irinotecan, fluorouracil, and leucovorin as firstline treatment for metastatic colorectal cancer: updated analysis of overall survival according to tumor KRAS and BRAF mutation status. J Clin Oncol 2011;29:2011-9.
11. Allegra CJ, Jessup JM, Somerfield MR, Hamilton SR, Hammond EH, Hayes DF, et al. American Society of Clinical Oncology provisional clinical opinion: testing for KRAS gene mutations in patients with metastatic colorectal carcinoma to predict response to anti-epidermal growth factor receptor monoclonal antibody therapy. J Clin Oncol 2009;27:2091-6.
12. Van Cutsem E, Dicato M, Arber N, Berlin J, Cervantes A, Ciardiello F, et al. Molecular markers and biological targeted therapies in metastatic colorectal cancer: expert opinion and recommendations derived from the 11th ESMO/World Congress on Gastrointestinal Cancer, Barcelona, 2009. Ann Oncol 2010;21 Suppl 6:vi1-10.
13. 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- 9.
14. Tol J, Dijkstra JR, Klomp M, Teerenstra S, Dommerholt M, Vink-Borger ME, et al. Markers for EGFR pathway activation as predictor of outcome in metastatic colorectal cancer patients treated with or without cetuximab. Eur J Cancer 2010;46:1997-2009.
15. Bokemeyer C, Cutsem EV, Rougier P, Ciardiello F, Heeger S, Schlichting M, et al. Addition of cetuximab to chemotherapy as first-line treatment for KRAS wild-type metastatic colorectal cancer: pooled analysis of the CRYSTAL and OPUS randomised clinical trials. Eur J Cancer 2012;48:1466-75.
16. Lievre A, Bachet JB, Le Corre D, Boige V, Landi B, Emile JF, et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res 2006;66:3992-5.
17. Prenen H, De Schutter J, Jacobs B, De Roock W, Biesmans B, Claes B, et al. PIK3CA mutations are not a major determinant of resistance to the epidermal growth factor receptor inhibitor cetuximab in metastatic colorectal cancer. Clin Cancer Res 2009;15:3184-8.
18. Sartore-Bianchi A, Martini M, Molinari F, Veronese S, Nichelatti M, Artale S, et al. PIK3CA mutations in colorectal cancer are associated with clinical resistance to EGFR-targeted monoclonal antibodies. Cancer Res 2009;69:1851- 7.
19. De Roock W, Claes B, Bernasconi D, De Schutter J, Biesmans B, Fountzilas G, et al. Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemo-therapy-refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol 2010;11:753-62.
20. Laurent-Puig P, Cayre A, Manceau G, Buc E, Bachet JB, Lecomte T, et al. Analysis of PTEN, BRAF, and EGFR status in determining benefit from cetuximab therapy in wild-type KRAS metastatic colon cancer. J Clin Oncol 2009;27:5924-30.
21. Frattini M, Saletti P, Romagnani E, Martin V, Molinari F, Ghisletta M, et al. PTEN loss of expression predicts cetuximab ef ficacy in metastatic colorectal cancer patients. Br J Cancer 2007;97: 1139-45. (Pubitemid 47587019)
22. Loupakis F, Pollina L, Stasi I, Ruzzo A, Scartozzi M, Santini D, et al. 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 2009;27:2622- 9.
23. Sartore-Bianchi A, Moroni M, Veronese S, Carnaghi C, Bajetta E, Luppi G, et al. Epidermal growth factor receptor gene copy number and clinical outcome of metastatic colorectal cancer treated with panitumumab. J Clin Oncol 2007;25:3238-45. (Pubitemid 47325607)
24. Moroni M, Veronese S, Benvenuti S, Marrapese G, Sartore-Bianchi A, Di Nicolantonio F, et al. Gene copy number for epidermal growth factor receptor (EGFR) and clinical response to antiEGFR treatment in colorectal cancer: a cohort study. Lancet Oncol 2005;6:279-86. (Pubitemid 40590264)
25. Italiano A, Follana P, Caroli FX, Badetti JL, Benchimol D, Garnier G, et al. Cetuximab shows activity in colorectal cancer patients with tumors for which FISH analysis does not detect an increase in EGFR gene copy number. Ann Surg Oncol 2008;15:649-54.
26. Bibeau F, Lopez-Crapez E, Di Fiore F, Thezenas S, Ychou M, Blanchard F, et al. Impact of Fc{gamma}RIIa-Fc{gamma}RIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol 2009;27:1122-9.
27. Park SJ, Hong YS, Lee JL, Ryu MH, Chang HM, Kim KP, et al. Genetic polymorphisms of FcgammaRIIa and FcgammaRIIIa are not predictive of clinical outcomes after cetuximab plus irinotecan chemotherapy in patients with metastatic colorectal cancer. Oncology 2012;82:83-9.
28. 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;25:3230-7. (Pubitemid 47325606)
29. Jacobs B, De Roock W, Piessevaux H, Van Oirbeek R, Biesmans B, De Schutter J, et al. Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol 2009;27:5068-74.
30. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 2009;27:5848-56.
31. Corte H, Manceau G, Blons H, Laurent-Puig P. MicroRNA and colorectal cancer. Dig Liver Dis 2012;44:195-200.
32. Mosakhani N, Lahti L, Borze I, Karjalainen-Lindsberg ML, Sundstrom J, Ristamaki R, et al. MicroRNA profiling predicts survival in anti-EGFR treated chemorefractory metastatic colorectal cancer patients with wild-type KRAS and BRAF. Cancer Genet 2012;205: 545- 51.
33. Andre T, Blons H, Mabro M, Chibaudel B, Bachet JB, Tournigand C, et al. Panitumumab combined with irinotecan for patients with KRAS wild-type metastatic colorectal cancer refractory to standard chemotherapy: a GERCOR efficacy, tolerance, and translational molecular study. Ann Oncol 2013;24:412-9.
34. Didelot A, Le Corre D, Luscan A, Cazes A, Pallier K, Emile JF, et al. Competitive allele specific TaqMan PCR for KRAS, BRAF and EGFR mutation detection in clinical formalin-fixed paraffin-embedded samples. Exp Mol Pathol 2012;92:275-80.
35. Bair E, Hastie T, Paul D, Tibshirani R. Prediction by supervised principal components. J Am Stast Ass 2006;101:119-37. (Pubitemid 43500030)
36. Bair E, Tibshirani R. Semi-supervised methods to predict patient survival from gene expression data. PLoS Biol 2004;2:E108.
37. Wei J, Gao W, Zhu CJ, Liu YQ, Mei Z, Cheng T, et al. Identification of plasma microRNA-21 as a biomarker for early detection and chemosensitivity of non -small cell lung cancer. Chin J Cancer 2011;30: 407-14.
38. Odenthal M, Bollschweiler E, Grimminger PP, Schroder W, Brabender J, Drebber U, et al. MicroRNA pro fi ling in locally advanced esophageal cancer indicates a high potential of miR-192 in prediction of multimodality therapy response. Int J Cancer 2013;133: 2454-63.
39. Ali S, Ahmad A, Banerjee S, Padhye S, Dominiak K, Schaffert JM, et al. Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res 2010;70:3606-17.
40. Pichler M, Winter E, Stotz M, Eberhard K, Samonigg H, Lax S, et al. Downregulation of KRAS-interacting miRNA-143 predicts poor prognosis but not response to EGFR-targeted agents in colorectal cancer. Br J Cancer 2012;106:1826-32.
41. Borralho PM, Kren BT, Castro RE, da Silva IB, Steer CJ, Rodrigues CM. MicroRNA-143 reduces viability and increases sensitivity to 5-fluorouracil in HCT116 human colorectal cancer cells. FEBS J 2009;276: 6689-700.
42. Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, et al. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013;497:383-7.
43. Franovic A, Gunaratnam L, Smith K, Robert I, Patten D, Lee S. Translational upregulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proc Natl Acad Sci U S A 2007;104:13092-7. (Pubitemid 351737598)
44. Van Cutsem E, Labianca R, Bodoky G, Barone C, Aranda E, Nordlinger B, et al. Randomized phase III trial comparing biweekly infusional fluorouracil/leucovorin alone or with irinotecan in the adjuvant treatment of stage III colon cancer: PETACC-3. J Clin Oncol 2009;27:3117-25.
45. Roth AD, Tejpar S, Delorenzi M, Yan P, Fiocca R, Klingbiel D, et al. 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 2010;28:466-74.