KRAS amplification in metastatic colon cancer is associated with a history of inflammatory bowel disease and may confer resistance to anti-EGFR therapy.


Journal

Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc
ISSN: 1530-0285
Titre abrégé: Mod Pathol
Pays: United States
ID NLM: 8806605

Informations de publication

Date de publication:
09 2020
Historique:
received: 04 01 2020
accepted: 24 04 2020
revised: 24 04 2020
pubmed: 8 5 2020
medline: 21 7 2021
entrez: 8 5 2020
Statut: ppublish

Résumé

Mutations in RAS occur in 30-50% of metastatic colorectal carcinomas (mCRCs) and correlate with resistance to anti-EGFR therapy. Consequently, mCRC biomarker guidelines state RAS mutational testing should be performed when considering EGFR inhibitor treatment. However, a small subset of mCRCs are reported to harbor RAS amplification. In order to elucidate the clinicopathologic features and anti-EGFR treatment response associated with RAS amplification, we retrospectively reviewed a large cohort of mCRC patients that underwent targeted next-generation sequencing and copy number analysis for KRAS, NRAS, HRAS, BRAF, and PIK3CA. Molecular testing was performed on 1286 consecutive mCRC from 1271 patients as part of routine clinical care, and results were correlated with clinicopathologic findings, mismatch repair (MMR) status and follow-up. RAS amplification was detected in 22 (2%) mCRCs and included: KRAS, NRAS, and HRAS for 15, 5, and 2 cases, respectively (6-21 gene copies). Patients with a KRAS-amplified mCRC were more likely to report a history of inflammatory bowel disease (p < 0.001). In contrast, mutations in KRAS were associated with older patient age, right-sided colonic origin, low-grade differentiation, mucinous histology, and MMR proficiency (p ≤ 0.017). Four patients with a KRAS-amplified mCRC and no concomitant RAS/BRAF/PIK3CA mutations received EGFR inhibitor-based therapy, and none demonstrated a clinicoradiographic response. The therapeutic impact of RAS amplification was further evaluated using a separate, multi-institutional cohort of 23 patients. Eight of 23 patients with KRAS-amplified mCRC received anti-EGFR therapy and all 8 patients exhibited disease progression on treatment. Although the number of KRAS-amplified mCRCs is limited, our data suggest the clinicopathologic features associated with mCRC harboring a KRAS amplification are distinct from those associated with a KRAS mutation. However, both alterations seem to confer EGFR inhibitor resistance and, therefore, RAS testing to include copy number analyses may be of consideration in the treatment of mCRC.

Identifiants

pubmed: 32376853
doi: 10.1038/s41379-020-0560-x
pii: S0893-3952(22)00712-8
pmc: PMC7483889
mid: NIHMS1587861
doi:

Substances chimiques

Antineoplastic Agents, Immunological 0
KRAS protein, human 0
Panitumumab 6A901E312A
EGFR protein, human EC 2.7.10.1
ErbB Receptors EC 2.7.10.1
Proto-Oncogene Proteins p21(ras) EC 3.6.5.2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1832-1843

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK120531
Pays : United States

Références

Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–34.
doi: 10.3322/caac.21551
Van Cutsem E, Cervantes A, Adam R, Sobrero A, Van Krieken JH, Aderka D, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27:1386–422.
doi: 10.1093/annonc/mdw235
Lim HJ, Gill S, Speers C, Melosky B, Barnett J, Fitzgerald C, et al. Impact of irinotecan and oxaliplatin on overall survival in patients with metastatic colorectal cancer: a population-based study. J Oncol Pr. 2009;5:153–8.
doi: 10.1200/JOP.0942001
Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines): Colon Cancer, Version 4.2019. 2019. Last access date 1/1/2020. https://www.nccn.org/professionals/physician_gls/pdf/colon.pdf .
Douillard JY, Oliner KS, Siena S, Tabernero J, Burkes R, Barugel M, et al. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N. Engl J Med. 2013;369:1023–34.
doi: 10.1056/NEJMoa1305275
Amado RG, Wolf M, Peeter 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.
doi: 10.1200/JCO.2007.14.7116
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;360:1408–17.
doi: 10.1056/NEJMoa0805019
Maughan TS, Adams RA, Smith CG, Meade AM, Seymour MT, Wilson RH, et al. Addition of cetuximab to oxaliplatin-based first-line combination chemotherapy for treatment of advanced colorectal cancer: results of the randomised phase 3 MRC COIN trial. Lancet. 2011;377:2103–14.
doi: 10.1016/S0140-6736(11)60613-2
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.
doi: 10.1200/JCO.2007.12.5906
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 chemotherapy-refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol. 2010;11:753–62.
doi: 10.1016/S1470-2045(10)70130-3
Sepulveda AR, Hamilton SR, Allegra CJ, Grody W, Cushman-Vokoun AM, Funkhouser WK, et al. Molecular biomarkers for the evaluation of colorectal cancer: guideline from the american society for clinical pathology, college of american pathologists, association for molecular pathology, and the american society of clinical oncology. J Clin Oncol. 2017;35:1453–86.
doi: 10.1200/JCO.2016.71.9807
Valtorta E, Misale S, Sartore-Bianchi A, Nagtegaal ID, Paraf F, Lauricella C, et al. KRAS gene amplification in colorectal cancer and impact on response to EGFR-targeted therapy. Int J Cancer. 2013;133:1259–65.
doi: 10.1002/ijc.28106
Serebriiskii IG, Connelly C, Frampton G, Newberg J, Cooke M, Miller V, et al. Comprehensive characterization of RAS mutations in colon and rectal cancers in old and young patients. Nat Commun. 2019;10:3722.
doi: 10.1038/s41467-019-11530-0
Mekenkamp LJ, Tol J, Dijkstra JR, de Krijger I, Vink-Borger ME, van Vliet S, et al. Beyond KRAS mutation status: influence of KRAS copy number status and microRNAs on clinical outcome to cetuximab in metastatic colorectal cancer patients. BMC Cancer. 2012;12:292.
doi: 10.1186/1471-2407-12-292
Hartman DJ, Chiosea SI. Colorectal carcinomas, KRAS p.G13D mutant allele-specific imbalance, and anti-epidermal growth factor receptor therapy. Cancer. 2013;119:4366.
doi: 10.1002/cncr.28371
Tumours of the Colon and Rectum, In: WHO classification of tumours of the digestive system. 5th edn. Vol. 1. Lyon: International Agency for Research on Cancer; 2019;157–92.
Singhi AD, McGrath K, Brand RE, Khalid A, Zeh HJ, Chennat JS, et al. Preoperative next-generation sequencing of pancreatic cyst fluid is highly accurate in cyst classification and detection of advanced neoplasia. Gut. 2018;67:2131–41.
doi: 10.1136/gutjnl-2016-313586
Singhi AD, Nikiforova MN, Chennat J, Papachristou GI, Khalid A, Rabinovitz M, et al. Integrating next-generation sequencing to endoscopic retrograde cholangiopancreatography (ERCP)-obtained biliary specimens improves the detection and management of patients with malignant bile duct strictures. Gut. 2020;69:52–61.
doi: 10.1136/gutjnl-2018-317817
Li MM, Datto M, Duncavage EJ, Kulkarni S, Lindeman NI, Roy S, et al. Standards and Guidelines for the Interpretation and Reporting of Sequence Variants in Cancer: A Joint Consensus Recommendation of the Association for Molecular Pathology, American Society of Clinical Oncology, and College of American Pathologists. J Mol Diagn. 2017;19:4–23.
doi: 10.1016/j.jmoldx.2016.10.002
Grasso C, Butler T, Rhodes K, Quist M, Neff TL, Moore S, et al. Assessing copy number alterations in targeted, amplicon-based next-generation sequencing data. J Mol Diagn. 2015;17:53–63.
doi: 10.1016/j.jmoldx.2014.09.008
Nikiforova MN, Wald AI, Melan MA, Roy S, Zhong S, Hamilton RL, et al. Targeted next-generation sequencing panel (GlioSeq) provides comprehensive genetic profiling of central nervous system tumors. Neuro Oncol. 2016;18:379–87.
doi: 10.1093/neuonc/nov289
Etienne-Grimaldi MC, Formento JL, Francoual M, Francois E, Formento P, Renee N, et al. K-Ras mutations and treatment outcome in colorectal cancer patients receiving exclusive fluoropyrimidine therapy. Clin Cancer Res. 2008;14:4830–5.
doi: 10.1158/1078-0432.CCR-07-4906
Bartley AN, Washington MK, Colasacco C, Ventura CB, Ismaila N, Benson AB 3rd, et al. HER2 Testing and Clinical Decision Making in Gastroesophageal Adenocarcinoma: Guideline From the College of American Pathologists, American Society for Clinical Pathology, and the American Society of Clinical Oncology. J Clin Oncol. 2017;35:446–64.
doi: 10.1200/JCO.2016.69.4836
Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N. Engl J Med. 1990;323:1228–33.
doi: 10.1056/NEJM199011013231802
Ullman T, Odze R, Farraye FA. Diagnosis and management of dysplasia in patients with ulcerative colitis and Crohn’s disease of the colon. Inflamm Bowel Dis. 2009;15:630–8.
doi: 10.1002/ibd.20766
Baker AM, Cross W, Curtius K, Al Bakir I, Choi CR, Davis HL, et al. Evolutionary history of human colitis-associated colorectal cancer. Gut. 2019;68:985–95.
doi: 10.1136/gutjnl-2018-316191
Lai LA, Risques RA, Bronner MP, Rabinovitch PS, Crispin D, Chen R, et al. Pan-colonic field defects are detected by CGH in the colons of UC patients with dysplasia/cancer. Cancer Lett. 2012;320:180–8.
doi: 10.1016/j.canlet.2012.02.031
Modrek B, Ge L, Pandita A, Lin E, Mohan S, Yue P, et al. Oncogenic activating mutations are associated with local copy gain. Mol Cancer Res. 2009;7:1244–52.
doi: 10.1158/1541-7786.MCR-08-0532
Poage GM, Christensen BC, Houseman EA, McClean MD, Wiencke JK, Posner MR, et al. Genetic and epigenetic somatic alterations in head and neck squamous cell carcinomas are globally coordinated but not locally targeted. PLoS ONE. 2010;5:e9651.
doi: 10.1371/journal.pone.0009651
Sasaki H, Yano M, Fujii Y. Evaluation of Kras gene mutation and copy number in thymic carcinomas and thymomas. J Thorac Oncol. 2010;5:1715–6.
doi: 10.1097/JTO.0b013e3181f1cab3
Wagner PL, Stiedl AC, Wilbertz T, Petersen K, Scheble V, Menon R, et al. Frequency and clinicopathologic correlates of KRAS amplification in non-small cell lung carcinoma. Lung Cancer. 2011;74:118–23.
doi: 10.1016/j.lungcan.2011.01.029
Sasaki H, Hikosaka Y, Kawano O, Moriyama S, Yano M, Fujii Y. Evaluation of Kras gene mutation and copy number gain in non-small cell lung cancer. J Thorac Oncol. 2011;6:15–20.
doi: 10.1097/JTO.0b013e31820594f0
Hanrahan AJ, Schultz N, Westfal ML, Sakr RA, Giri DD, Scarperi S, et al. Genomic complexity and AKT dependence in serous ovarian cancer. Cancer Discov. 2012;2:56–67.
doi: 10.1158/2159-8290.CD-11-0170
Ricordel C, Friboulet L, Facchinetti F, Soria JC. Molecular mechanisms of acquired resistance to third-generation EGFR-TKIs in EGFR T790M-mutant lung cancer. Ann Oncol. 2019;30:858.
doi: 10.1093/annonc/mdy222
Abdel-Rahman O, Fouad M. Correlation of cetuximab-induced skin rash and outcomes of solid tumor patients treated with cetuximab: a systematic review and meta-analysis. Crit Rev Oncol Hematol. 2015;93:127–35.
doi: 10.1016/j.critrevonc.2014.07.005
Liu HB, Wu Y, Lv TF, Yao YW, Xiao YY, Yuan DM, et al. Skin rash could predict the response to EGFR tyrosine kinase inhibitor and the prognosis for patients with non-small cell lung cancer: a systematic review and meta-analysis. PLoS ONE. 2013;8:e55128.
doi: 10.1371/journal.pone.0055128

Auteurs

Laura A Favazza (LA)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.
Department of Pathology, Henry Ford Health System, Detroit, MI, USA.

Christine M Parseghian (CM)

Department of Gastrointestinal Medical Oncology, Division of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Cihan Kaya (C)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Marina N Nikiforova (MN)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Somak Roy (S)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Abigail I Wald (AI)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Michael S Landau (MS)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Siobhan S Proksell (SS)

Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Jeffrey M Dueker (JM)

Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Elyse R Johnston (ER)

Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Randall E Brand (RE)

Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Nathan Bahary (N)

Department of Medicine, Hillman Cancer Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Vikram C Gorantla (VC)

Department of Medicine, Hillman Cancer Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

John C Rhee (JC)

Department of Medicine, Hillman Cancer Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

James F Pingpank (JF)

Department of Surgery, Division of Hepatopancreatobiliary Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Haroon A Choudry (HA)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Kenneth Lee (K)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Alessandro Paniccia (A)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Melanie C Ongchin (MC)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Amer H Zureikat (AH)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

David L Bartlett (DL)

Department of Surgery, Division of Gastrointestinal Surgical Oncology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Aatur D Singhi (AD)

Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA. singhiad@upmc.edu.

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