دورية أكاديمية

Dynamic nature of BRAF or KRAS p.G12C mutations in second-line therapy for advanced colorectal cancer patients: do early and late effects exist?

التفاصيل البيبلوغرافية
العنوان: Dynamic nature of BRAF or KRAS p.G12C mutations in second-line therapy for advanced colorectal cancer patients: do early and late effects exist?
المؤلفون: Contreras-Toledo D; Department of Medical Oncology, Hospital Universitario Central de Asturias, ISPA, Universidad de Oviedo, Oviedo, Spain. ct.debora@gmail.com., Jiménez-Fonseca P; Department of Medical Oncology, Hospital Universitario Central de Asturias, ISPA, Universidad de Oviedo, Oviedo, Spain., López CL; Department of Medical Oncology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Universidad de Cantabria (UNICAN), Santander, Spain., Montes AF; Department of Medical Oncology, Complexo Hospitalario Universitario de Ourense, Ourense, Spain., López Muñoz AM; Department of Medical Oncology, Hospital Universitario de Burgos, Burgos, Spain., Vázquez Rivera F; Department of Medical Oncology, Hospital Universitario de Santiago, Santiago de Compostela, Spain., Alonso V; Department of Medical Oncology, Hospital Universitario Miguel Servet, IISA, Zaragoza, Spain., Alcaide J; Department of Medical Oncology, Hospital Costa del Sol, Marbella, Medical Oncology Intercenter Unit, Hospital Universitario Regional y Virgen de la Victoria, IBIMA, Málaga, Spain., Salvà F; Department of Medical Oncology, Hospital Universitario Vall D'Hebrón, Vall D´Hebrón Institute of Oncology (VHIO), Barcelona, Spain., Covela Rúa M; Department of Medical Oncology, Hospital Universitario Lucus Augusti, Lugo, Spain., Guillot M; Department of Medical Oncology, Hospital Universitario Son Espases, Palma de Mallorca, Spain., Martín Carnicero A; Department of Medical Oncology, Hospital San Pedro, Logroño, Spain., Jimeno Mate R; Department of Medical Oncology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain., Cameselle García S; Department of Medical Oncology, Complexo Hospitalario Universitario de Ourense, Ourense, Spain., Asensio Martínez E; Department of Medical Oncology, Hospital General Universitario de Elche, Elche, Spain., González Astorga B; Department of Medical Oncology, Hospital Universitario Clínico San Cecilio, Granada, Spain., Fernandez-Diaz AB; Department of Medical Oncology, Hospital General de Valencia, Valencia, Spain., González Villaroel P; Department of Medical Oncology, Hospital Universitario Álvaro Cunqueiro, Vigo, Spain., Virgili Manrique AC; Department of Medical Oncology, Hospital Santa Creu i San Pau, Barcelona, Spain., Melián Sosa M; Department of Medical Oncology, Instituto Valenciano de Oncología (IVO), Valencia, Spain., Alonso B; Department of Medical Oncology, Hospital Universitario de Canarias, Tenerife, Spain., Cousillas Castiñeiras A; Department of Medical Oncology, Complejo Hospitalario de Pontevedra, Pontevedra, Spain., Castañón López C; Department of Medical Oncology, Hospital Universitario de León, León, Spain., Aparicio J; Department of Medical Oncology, Hospital Universitario y Politécnico La Fe de Valencia, Valencia, Spain., Carmona-Bayonas A; Department of Medical Oncology, Hospital Universitario Morales Meseguer, Universidad de Murcia, IMIB, Murcia, Spain. alberto.carmonabayonas@gmail.com.
المصدر: British journal of cancer [Br J Cancer] 2024 Mar; Vol. 130 (5), pp. 777-787. Date of Electronic Publication: 2024 Jan 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group on behalf of Cancer Research UK Country of Publication: England NLM ID: 0370635 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1532-1827 (Electronic) Linking ISSN: 00070920 NLM ISO Abbreviation: Br J Cancer Subsets: MEDLINE
أسماء مطبوعة: Publication: 2002- : London : Nature Publishing Group on behalf of Cancer Research UK
Original Publication: London, Lewis.
مواضيع طبية MeSH: Colorectal Neoplasms*/drug therapy , Colorectal Neoplasms*/genetics , Colorectal Neoplasms*/pathology , Colonic Neoplasms*/genetics, Humans ; Proto-Oncogene Proteins B-raf/genetics ; Proto-Oncogene Proteins p21(ras)/genetics ; Mutation ; Disease Progression
مستخلص: Introduction: The mitogen-activated protein kinase (MAPK) signalling network aberrations in metastatic colorectal cancer (mCRC) generate intrinsic dynamic effects and temporal variations that are crucial but often overlooked in clinical trial populations. Here, we investigate the time-varying impact of MAPK pathway mutation genotype on each treatment line's contribution to the overall clinical course.
Methods: The PROMETEO study focused on mCRC patients undergoing second-line treatment at 20 hospitals. We evaluated genotypes and employed flexible models to analyse the dynamic effect of each mutation.
Results: We examined data derived from 1160 patients. The effects of KRAS G12C or G12V, and BRAF V600E are clearly time-varying, with unexpected consequences such as the deleterious effect of BRAF V600E vs other genotypes dissipating over time when subjects receive antiangiogenics, or KRAS G12V and G12C showing increasing aggressiveness over time. Thus, contrary to expectations, the 12-month survival rate from the second line for those who survived >6 months was 49.9% (95% CI, 32.7-67.3) for KRAS G12C and 59% (95% CI, 38.5-80.6) for BRAF V600E.
Conclusions: The dynamic perspective is essential for understanding the behaviour of tumours with specific genotypes, especially from the second line onward. This may be relevant in patient monitoring and treatment decision-making, particularly in cases with distinct mutations.
(© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)
References: Ottaiano A, Normanno N, Facchini S, Cassata A, Nappi A, Romano C, et al. Study of Ras mutations’ prognostic value in metastatic colorectal cancer: STORIA analysis. Cancers. 2020;12:1919. (PMID: 327085757409181)
Bylsma LC, Gillezeau C, Garawin TA, Kelsh MA, Fryzek JP, Sangaré L, et al. Prevalence of RAS and BRAF mutations in metastatic colorectal cancer patients by tumor sidedness: a systematic review and meta‐analysis. Cancer Med. 2020;9:1044–57. (PMID: 31856410)
Bazan V, Migliavacca M, Zanna I, Tubiolo C, Grassi N, Latteri MA, et al. Specific codon 13 K-ras mutations are predictive of clinical outcome in colorectal cancer patients, whereas codon 12 K-ras mutations are associated with mucinous histotype. Ann Oncol. 2002;13:1438–46. (PMID: 12196370)
Zhu G, Pei L, Xia H, Tang Q, Bi F. Role of oncogenic KRAS in the prognosis, diagnosis and treatment of colorectal cancer. Mol Cancer. 2021;20:1–17.
Patelli G, Tosi F, Amatu A, Mauri G, Curaba A, Patane DA, et al. Strategies to tackle RAS-mutated metastatic colorectal cancer. ESMO Open. 2021;6:100156. (PMID: 340442868167159)
Goebel L, Müller MP, Goody RS, Rauh D. KRasG12C inhibitors in clinical trials: a short historical perspective. RSC Med Chem. 2020;11:760–70. (PMID: 334796737549139)
Ostrem JM, Peters U, Sos ML, Wells JA, Shokat KM. K-Ras (G12C) inhibitors allosterically control GTP affinity and effector interactions. Nature. 2013;503:548–51. (PMID: 242567304274051)
Henry JT, Coker O, Chowdhury S, Shen JP, Morris VK, Dasari A, et al. Comprehensive clinical and molecular characterization of KRAS G12C -mutant colorectal cancer. JCO Precis Oncol. 2021;5:PO.20.00256.
Dienstmann R, Connor K, Byrne AT, Fridman WH, Lambrechts D, Sadanandam A, et al. Precision therapy in RAS mutant colorectal cancer. Gastroenterology. 2020;158:806–11. (PMID: 31972237)
Amodio V, Yaeger R, Arcella P, Cancelliere C, Lamba S, Lorenzato A, et al. EGFR blockade reverts resistance to KRASG12C inhibition in colorectal cancer overcoming KRASG12C inhibitor resistance in colorectal cancer. Cancer Discov. 2020;10:1129–39. (PMID: 324303887416460)
Hong DS, Fakih MG, Strickler JH, Desai J, Durm GA, Shapiro GI, et al. KRASG12C inhibition with sotorasib in advanced solid tumors. N Engl J Med. 2020;383:1207–17. (PMID: 329551767571518)
Yaeger R, Weiss J, Pelster MS, Spira AI, Barve M, Ou S-HI, et al. Adagrasib with or without cetuximab in colorectal cancer with mutated KRAS G12C. N Engl J Med. 2023;388:44–54. (PMID: 36546659)
Hunter JC, Manandhar A, Carrasco MA, Gurbani D, Gondi S, Westover KD. Biochemical and structural analysis of common cancer-associated KRAS mutations. Mol Cancer Res. 2015;13:1325–35.
de la Chapelle A, Hampel H. Clinical relevance of microsatellite instability in colorectal cancer. J Clin Oncol. 2010;28:3380. (PMID: 205164442903331)
Kopetz S, Desai J, Chan E, Hecht JR, O’Dwyer PJ, Maru D, et al. Phase II pilot study of vemurafenib in patients with metastatic BRAF-mutated colorectal cancer. J Clin Oncol. 2015;33:4032. (PMID: 264603034669589)
Rowland A, Dias MM, Wiese MD, Kichenadasse G, McKinnon RA, Karapetis CS, et al. Meta-analysis of BRAF mutation as a predictive biomarker of benefit from anti-EGFR monoclonal antibody therapy for RAS wild-type metastatic colorectal cancer. Br J Cancer. 2015;112:1888–94. (PMID: 259892784580381)
Pietrantonio F, Petrelli F, Coinu A, Di Bartolomeo M, Borgonovo K, Maggi C, et al. Predictive role of BRAF mutations in patients with advanced colorectal cancer receiving cetuximab and panitumumab: a meta-analysis. Eur J Cancer. 2015;51:587–94. (PMID: 25673558)
Kopetz S, Grothey A, Yaeger R, Van Cutsem E, Desai J, Yoshino T, et al. Encorafenib, binimetinib, and cetuximab in BRAF V600E–mutated colorectal cancer. N Engl J Med. 2019;381:1632–43. (PMID: 31566309)
Seligmann JF, Fisher D, Smith CG, Richman SD, Elliott F, Brown S, et al. Investigating the poor outcomes ofBRAF-mutant advanced colorectal cancer: analysis from 2530 patients in randomised clinical trials. Ann Oncol. 2017;28:562–8. (PMID: 27993800)
Ciardiello D, Chiarazzo C, Famiglietti V, Damato A, Pinto C, Zampino MG, et al. Clinical efficacy of sequential treatments in KRASG12C-mutant metastatic colorectal cancer: findings from a real-life multicenter Italian study (CRC-KR GOIM). ESMO Open. 2022;7:100567. (PMID: 359947919588891)
Hochster H, Hager S, Pipas JM, Tebbutt N, Laurent S, Gravalos C, et al. O-010 KRAS and BRAF gene subgroup analysis in the phase 3 RECOURSE trial of TAS-102 versus placebo in patients with metastatic colorectal cancer. Ann Oncol. 2015;26:iv111.
Cervantes A, Adam R, Roselló S, Arnold D, Normanno N, Taïeb J, et al. Metastatic colorectal cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol. 2023;34:10–32. (PMID: 36307056)
Humbert M, Sitbon O, Yaïci A, Montani D, O’callaghan DS, Jaïs X, et al. Survival in incident and prevalent cohorts of patients with pulmonary arterial hypertension. Eur Respir J. 2010;36:549–55. (PMID: 20562126)
Carmona-Bayonas A, Jimenez-Fonseca P, Garrido M, Custodio A, Hernandez R, Lacalle A, et al. Multistate models: accurate and dynamic methods to improve predictions of thrombotic risk in patients with cancer. Thromb Haemost. 2019;119:1849–59. (PMID: 31461750)
Royston P, Parmar MKB. Flexible parametric proportional‐hazards and proportional‐odds models for censored survival data, with application to prognostic modelling and estimation of treatment effects. Stat Med. 2002;21:2175–97. (PMID: 12210632)
Harrell F. Regression modeling strategies: with applications to linear models, logistic and ordinal regression, and survival analysis. 2nd ed. New York: Springer; 2015.
Woods BS, Sideris E, Palmer S, Latimer N, Soares M. Partitioned survival and state transition models for healthcare decision making in oncology: where are we now? Value Health. 2020;23:1613–21. (PMID: 33248517)
Cranmer H, Shields GE, Bullement A. A comparison of partitioned survival analysis and state transition multi-state modelling approaches using a case study in oncology. J Med Econ. 2020;23:1176–85. (PMID: 32673128)
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2014.
De Wreede LC, Fiocco M, Putter H. The mstate package for estimation and prediction in non-and semi-parametric multi-state and competing risks models. Comput Methods Prog Biomed. 2010;99:261–74.
Therneau T, Crowson C, Atkinson E. Multi-state models and competing risks. 2016. https://cran.r-project.org/web/packages/survival/vignettes/compete.pdf .
Allaire JJ, Ellis P, Gandrud C, Kuo K, Lewis BW, Owen J, et al. Package ‘networkD3.’ D3 JavaScript Netw graphs from R. 2017. https://CRAN.R-project.org/package=networkD3 .
Incerti D, Jeroen G, Jansen P. hesim: Health Economic Simulation Modeling and Decision Analysis. 2021 Feb 18 [cited 2024 Jan 3]; Available from: https://arxiv.org/abs/2102.09437v2 .
Jones RP, Sutton PA, Evans JP, Clifford R, McAvoy A, Lewis J, et al. Specific mutations in KRAS codon 12 are associated with worse overall survival in patients with advanced and recurrent colorectal cancer. Br J Cancer. 2017;116:923–9. (PMID: 282081575379149)
Imamura Y, Morikawa T, Liao X, Lochhead P, Kuchiba A, Yamauchi M, et al. Specific mutations in KRAS codons 12 and 13, and patient prognosis in 1075 BRAF wild-type colorectal cancers. Clin Cancer Res. 2012;18:4753–63. (PMID: 227535893624899)
Modest DP, Ricard I, Heinemann V, Hegewisch-Becker S, Schmiegel W, Porschen R, et al. Outcome according to KRAS-, NRAS-and BRAF-mutation as well as KRAS mutation variants: pooled analysis of five randomized trials in metastatic colorectal cancer by the AIO Colorectal Cancer Study Group. Ann Oncol. 2016;27:1746–53. (PMID: 273583794999563)
Castañon E, Sanchez-Arraez Á, Jimenez-Fonseca P, Alvarez-Manceñido F, Martínez-Martínez I, Gongora LM, et al. Bayesian interpretation of immunotherapy trials with dynamic treatment effects. Eur J Cancer. 2022;161:79–89. (PMID: 34933154)
Castañon E, Sanchez-Arraez A, Alvarez-Manceñido F, Jimenez-Fonseca P, Carmona-Bayonas A. Critical reappraisal of phase III trials with immune checkpoint inhibitors in non-proportional hazards settings. Eur J Cancer. 2020;136:159–68. (PMID: 32698098)
Mitani S, Taniguchi H, Honda K, Masuishi T, Narita Y, Kadowaki S, et al. Analysis of efficacy and prognostic factors in second-line chemotherapy for BRAF V600E mutant metastatic colorectal cancer. Ann Oncol. 2017;28:v180.
Tabernero J, Van Cutsem E, Yoshino T, Yaeger R, Wasan H, Desai J, et al. SO-29 Clinical characteristics, efficacy, and safety in patients receiving second-or third-line encorafenib plus cetuximab (E+ C) vs control for metastatic colorectal cancer (mCRC): BEACON CRC post hoc analysis. Ann Oncol. 2023;34:S174.
Tabernero J, Grothey A, Van Cutsem E, Yaeger R, Wasan H, Yoshino T, et al. Encorafenib plus cetuximab as a new standard of care for previously treated BRAF V600E–mutant metastatic colorectal cancer: updated survival results and subgroup analyses from the BEACON study. J Clin Oncol. 2021;39:273. (PMID: 335033938078423)
Wirapati P, Pomella V, Vandenbosch B, Kerr P, Maiello E, Jeffery GM, et al. Velour trial biomarkers update: Impact of RAS, BRAF, and sidedness on aflibercept activity. J Clin Oncol. 2017;35:3538.
Loupakis F, Cremolini C, Masi G, Lonardi S, Zagonel V, Salvatore L, et al. Initial therapy with FOLFOXIRI and bevacizumab for metastatic colorectal cancer. N Engl J Med. 2014;371:1609–18. (PMID: 25337750)
Yoshino T, Portnoy DC, Obermannova R, Bodoky G, Prausová J, Garcia-Carbonero R, et al. Biomarker analysis beyond angiogenesis: RAS/RAF mutation status, tumour sidedness, and second-line ramucirumab efficacy in patients with metastatic colorectal carcinoma from RAISE—a global phase III study. Ann Oncol. 2019;30:124–31. (PMID: 30339194)
Chida K, Kotani D, Masuishi T, Kawakami T, Kawamoto Y, Kato K, et al. The prognostic impact of KRAS G12C mutation in patients with metastatic colorectal cancer: a multicenter retrospective observational study. Oncologist. 2021;26:845–53. (PMID: 342325468488780)
Fakih M, Tu H, Hsu H, Aggarwal S, Chan E, Rehn M, et al. Real-world study of characteristics and treatment outcomes among patients with KRAS p. G12C-mutated or other KRAS mutated metastatic colorectal cancer. Oncologist. 2022;27:663–74. (PMID: 354721769355827)
Cremolini C, Antoniotti C, Lonardi S, Bergamo F, Cortesi E, Tomasello G, et al. Primary tumor sidedness and benefit from FOLFOXIRI plus bevacizumab as initial therapy for metastatic colorectal cancer. Retrospective analysis of the TRIBE trial by GONO. Ann Oncol. 2018;29:1528–34. (PMID: 29873679)
Sunakawa Y, Satake H, Usher J, Jaimes Y, Miyamoto Y, Nakamura M, et al. Dynamic changes in RAS gene status in circulating tumour DNA: a phase II trial of first-line FOLFOXIRI plus bevacizumab for RAS-mutant metastatic colorectal cancer (JACCRO CC-11). ESMO Open. 2022;7:100512. (PMID: 356880619271512)
Mok TS, Wu Y-L, Thongprasert S, Yang C-H, Chu D-T, Saijo N, et al. Gefitinib or carboplatin–paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361:947–57. (PMID: 19692680)
Siena S, Sartore-Bianchi A, Garcia-Carbonero R, Karthaus M, Smith D, Tabernero J, et al. Dynamic molecular analysis and clinical correlates of tumor evolution within a phase II trial of panitumumab-based therapy in metastatic colorectal cancer. Ann Oncol. 2018;29:119–26. (PMID: 28945848)
المشرفين على المادة: EC 2.7.11.1 (Proto-Oncogene Proteins B-raf)
EC 3.6.5.2 (Proto-Oncogene Proteins p21(ras))
0 (KRAS protein, human)
EC 2.7.11.1 (BRAF protein, human)
تواريخ الأحداث: Date Created: 20240108 Date Completed: 20240306 Latest Revision: 20240308
رمز التحديث: 20240309
مُعرف محوري في PubMed: PMC10912758
DOI: 10.1038/s41416-023-02563-w
PMID: 38191609
قاعدة البيانات: MEDLINE
الوصف
تدمد:1532-1827
DOI:10.1038/s41416-023-02563-w