KRAS in NSCLC: State of the Art and Future Perspectives

Cascetta, Priscilla; Marinello, Arianna; Lazzari, Chiara; Gregorc, Vanesa; Planchard, David; Bianco, Roberto; Normanno, Nicola; Morabito, Alessandro

doi:10.3390/cancers14215430

Cited by 76Lung Cancer Treatments and MutationsProtein Kinase Regulation and GTPase SignalingCancer Genomics and Diagnostics

KRAS in NSCLC: State of the Art and Future Perspectives

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Cascetta, Priscilla, Marinello, Arianna, Lazzari, Chiara, Gregorc, Vanesa, Planchard, David, Bianco, Roberto, Normanno, Nicola, Morabito, Alessandro·2022·Cancers

DOI 10.3390/cancers14215430PMC PMC9656434

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Abstract

In NSCLC, KRAS mutations occur in up to 30% of all cases, most frequently at codon 12 and 13. KRAS mutations have been linked to adenocarcinoma histology, positive smoking history, and Caucasian ethnicity, although differences have been described across KRAS mutational variants subtypes. KRAS mutations often concur with other molecular alterations, notably TP53, STK11, and KEAP1, which could play an important role in treatment efficacy and patient outcomes. For many years, KRAS mutations have been considered undruggable mainly due to a high toxicity profile and low specificity of compounds. Sotorasib and adagrasib are novel KRAS inhibitors that recently gained FDA approval for pre-treated KRAS mutant NSCLC patients, and other molecules such as GDC-6036 are currently being investigated with promising results. Despite their approval, the efficacy of these drugs is lower than expected and progression among responders has been reported. Mechanisms of acquired resistance to anti-KRAS molecules typically involves either on target secondary mutations (e.g., G12, G13, Q61H, R68S, H95, Y96C, V8L) or off-target alterations. Ongoing trials are currently evaluating strategies for implementing efficacy and overcoming acquired resistance to these compounds. Finally, the efficacy of immune-checkpoint inhibitors still needs to be completely assessed and responses to anti-PD-1/PD-L1 agents may strongly depend on concomitant mutations.

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In a phase I trial of divarasib, among 57 evaluable patients with NSCLC, 26 were confirmed to be in partial remission, with a confirmed ORR of 46%.
“Of the 59 patients with NSCLC previously treated with divarasib monotherapy included, 57 patients had evaluable outcomes, 26 of whom were confirmed to be in partial remission (PR), with confirmed objective remission rate (ORR) of 46%.”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [67]
Divarasib irreversibly immobilizes KRASG12C in the inactivation state.
“It also irreversibly immobilizes KRASG12C in the inactivation state.”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [67]
Divarasib is a small molecule covalent inhibitor of KRASG12C developed by Genentech that is orally available, highly selective, and potent.
“Divarasib (5) is a small molecule covalent inhibitor of KRASG12C developed by Genentech that is orally available, highly selective, and potent.”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [67]

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LKB1/KRAS mutant lung cancers constitute a genetic subset of NSCLC with increased sensitivity to MAPK and mTOR signalling inhibition
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Afatinib restrains K-RAS–driven lung tumorigenesis
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Pooled Analysis of the Prognostic and Predictive Effects of TP53 Comutation Status Combined With KRAS or EGFR Mutation in Early-Stage Resected Non–Small-Cell Lung Cancer in Four Trials of Adjuvant Chemotherapy
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Activation of KRAS Mediates Resistance to Targeted Therapy in MET Exon 14–mutant Non–small Cell Lung Cancer
Suzawa, K., Offin, M. D., Lu, D., Kurzatkowski, C., Vojnic, M., Smith, R. S., Sabari, J. K., Tai, H., Mattar, M. S., Khodos, I., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-1640 · Cited by 123 · see citing works
Recommendations for a practical implementation of circulating tumor DNA mutation testing in metastatic non-small-cell lung cancer
Heitzer, E., van den Broek, D. A., Denis, M. G., Hofman, P. M., Hubank, M. J. F., Mouliere, F. C., Paz-Ares, L. G., Schuuring, E. M. D., Sültmann, H., Vainer, G. W., et al. (2022) · ESMO Open · doi:10.1016/j.esmoop.2022.100399 · Cited by 118 · see citing works
The genetics and biology of KRAS in lung cancer
Westcott, P. M. K., & To, M. D. (2013) · Chinese Journal of Cancer · doi:10.5732/cjc.012.10098 · Cited by 116 · see citing works
Prognostic value of KRAS mutation in advanced non-small-cell lung cancer treated with immune checkpoint inhibitors: A meta-analysis and review
Kim, J. H., Kim, H. S., & Kim, B. J. (2017) · Oncotarget · doi:10.18632/oncotarget.17594 · Cited by 115 · see citing works
Dissecting the clinicopathologic, genomic, and immunophenotypic correlates of KRASG12D-mutated non-small-cell lung cancer
Ricciuti, B., Alessi, J. V., Elkrief, A., Wang, X., Cortellini, A., Li, Y. Y., Vaz, V. R., Gupta, H., Pecci, F., Barrichello, A., et al. (2022) · Annals of Oncology · doi:10.1016/j.annonc.2022.07.005 · Cited by 112 · see citing works
Landscape of KRAS G12C , Associated Genomic Alterations, and Interrelation With Immuno-Oncology Biomarkers in KRAS -Mutated Cancers
Salem, M. E., El-Refai, S. M., Sha, W., Puccini, A., Grothey, A., George, T. J., Hwang, J. J., O’Neil, B. H., Barrett, A. S., Kadakia, K. C., et al. (2022) · JCO Precision Oncology · doi:10.1200/po.21.00245 · Cited by 110 · see citing works
OA03.06 CodeBreaK 100/101: First Report of Safety/Efficacy of Sotorasib in Combination with Pembrolizumab or Atezolizumab in Advanced KRAS p.G12C NSCLC
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LBA4 Association of KRAS mutational status with response to pembrolizumab monotherapy given as first-line therapy for PD-L1-positive advanced non-squamous NSCLC in Keynote-042
Herbst, R. S., Lopes, G. D. L., Jr., Kowalski, D. M., Kasahara, K., Wu, Y., de Castro, G., Cho, B. C., Turna, H. Z., Cristescu, R., Aurora-Garg, D., et al. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz453.001 · Cited by 91 · see citing works
Association Between KRAS Variant Status and Outcomes With First-line Immune Checkpoint Inhibitor–Based Therapy in Patients With Advanced Non–Small-Cell Lung Cancer
Sun, L., Hsu, M., Cohen, R. B., Langer, C. J., Mamtani, R., & Aggarwal, C. (2021) · JAMA Oncology · doi:10.1001/jamaoncol.2021.0546 · Cited by 87 · see citing works
KRAS G12C Mutations in NSCLC: From Target to Resistance
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Anti-PD-(L)1 for KRAS-mutant advanced non-small–cell lung cancers: a meta-analysis of randomized–controlled trials
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Real world outcomes in KRAS G12C mutation positive non-small cell lung cancer
Cui, W., Franchini, F., Alexander, M., Officer, A., Wong, H., IJzerman, M. J., Desai, J., & Solomon, B. (2020) · Lung Cancer · doi:10.1016/j.lungcan.2020.06.030 · Cited by 80 · see citing works
Clinical Outcome of ALK -Positive Non–Small Cell Lung Cancer (NSCLC) Patients with De Novo EGFR or KRAS Co-Mutations Receiving Tyrosine Kinase Inhibitors (TKIs)
Schmid, S., Gautschi, O. P., Rothschild, S. I., Mark, M. T., Froesch, P., Klingbiel, D., Reichegger, H., Jochum, W., Diebold, J., & Früh, M. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.12.003 · Cited by 78 · see citing works
KRAS Inhibitors– yes but what next? Direct targeting of KRAS– vaccines, adoptive T cell therapy and beyond
Nagasaka, M., Potugari, B. R., Nguyen, A., Sukari, A. W., Azmi, A. S., & Ou, S. I. (2021) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2021.102309 · Cited by 78 · see citing works
KRAS-Mutant Non-Small Cell Lung Cancer: An Emerging Promisingly Treatable Subgroup
Xie, M., Xu, X., & Fan, Y. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.672612 · Cited by 76 · see citing works
Tumor molecular profiling of NSCLC patients using next generation sequencing
Τσούλος, Ν., Papadopoulou, E., Metaxa-Mariatou, V., Tsaousis, G., Efstathiadou, C., Tounta, G., Scapeti, A., Bourkoula, E., Zarogoulidis, P., Pentheroudakis, G. E., et al. (2017) · Oncology Reports · doi:10.3892/or.2017.6051 · Cited by 75 · see citing works
The Presence of Concomitant Mutations Affects the Activity of EGFR Tyrosine Kinase Inhibitors in EGFR-Mutant Non-Small Cell Lung Cancer (NSCLC) Patients
Rachiglio, A. M., Fenizia, F., Piccirillo, M. C., Galetta, D., Crinò, L., Vincenzi, B., Barletta, E., Pinto, C., Ferraù, F., Lambiase, M., et al. (2019) · Cancers · doi:10.3390/cancers11030341 · Cited by 75 · see citing works
Self-citation
K-ras 4A and 4B are co-expressed widely in human tissues, and their ratio is altered in sporadic colorectal cancer.
Plowman, S. J., Berry, R. L., Bader, S. A., Luo, F., Arends, M. J., Harrison, D. J., Hooper, M. L., & Patek, C. E. (2006) · PubMed · Cited by 70 · see citing works
Assessing Therapeutic Efficacy of MEK Inhibition in a KRASG12C-Driven Mouse Model of Lung Cancer
Li, S., Liu, S., Deng, J., Akbay, E. A., Hai, J., Ambrogio, C., Zhang, L., Zhou, F., Jenkins, R. W., Adeegbe, D. O., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-3438 · Cited by 67 · see citing works
KRAS mutation as a prognostic factor and predictive factor in advanced/metastatic non-small cell lung cancer: A systematic literature review and meta-analysis
Goulding, R. E., Chenoweth, M. D., Carter, G. C., Boye, M. E., Sheffield, K. M., John, W. J., Leusch, M. S., Muehlenbein, C. E., Li, L., Jen, M., et al. (2020) · Cancer Treatment and Research Communications · doi:10.1016/j.ctarc.2020.100200 · Cited by 63 · see citing works
Prognostic Impact of KRAS G12C Mutation in Patients With NSCLC: Results From the European Thoracic Oncology Platform Lungscape Project
Finn, S. P., Addeo, A., Dafni, U. G., Thunnissen, E., Bubendorf, L., Madsen, L. B., Biernat, W., Verbeken, E. K., Hernández‐Losa, J., Marchetti, A., et al. (2021) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2021.02.016 · Cited by 63 · see citing works
Targeting KRAS Mutant in Non-Small Cell Lung Cancer: Novel Insights Into Therapeutic Strategies
Désage, A.-L., Léonce, C., Swalduz, A., & Ortiz‐Cuaran, S. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.796832 · Cited by 60 · see citing works
OA03.03 sotorasib in combination with RMC-4630, a SHP2 inhibitor, in KRAS p.G12C-mutated NSCLC and other solid tumors
Falchook, G., Li, B. T., Marrone, K. A., Bestvina, C. M., Langer, C. J., Krauss, J. C., Strickler, J. H., Meloni, A., Dai, T., Varrieur, T., et al. (2022) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2022.07.022 · Cited by 56 · see citing works
Towards Routine Implementation of Liquid Biopsies in Cancer Management: It Is Always Too Early, until Suddenly It Is Too Late
IJzerman, M. J., de Boer, J., Azad, A., Degeling, K., Geoghegan, J. M., Hewitt, C., Hollande, F., Lee, B., To, Y. H., Tothill, R. W., et al. (2021) · Diagnostics · doi:10.3390/diagnostics11010103 · Cited by 55 · see citing works
P52.03 Efficacy of Sotorasib in KRAS p.G12C-Mutated NSCLC with Stable Brain Metastases: A Post-Hoc Analysis of CodeBreaK 100
Ramalingam, S. S., Skoulidis, F., Govindan, R., Velcheti, V., Li, B., Besse, B., Dy, G. K., Kim, D. S., Schüler, M., Vincent, M. D., et al. (2021) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2021.08.547 · Cited by 52 · see citing works
Distinct Afatinib Resistance Mechanisms Identified in Lung Adenocarcinoma Harboring an EGFR Mutation
Yamaoka, T., Ohmori, T., Ohba, M., Arata, S., Murata, Y., Kusumoto, S., Andō, K., Ishida, H., Ohnishi, T., & Sasaki, Y. (2017) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-16-0482 · Cited by 47 · see citing works
Value of KRAS as prognostic or predictive marker in NSCLC: results from the TAILOR trial
Rulli, E., Marabese, M., Torri, V., Farina, G., Veronese, S. M., Bettini, A., Longo, F., Moscetti, L. I., Ganzinelli, M., Lauricella, C., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv318 · Cited by 46 · see citing works
Clinical and Molecular Predictors of PD-L1 Expression in Non–Small-Cell Lung Cancer: Systematic Review and Meta-analysis
Petrelli, F., Maltese, M., Tomasello, G., Conti, B., Borgonovo, K., Cabiddu, M., Ghilardi, M., Ghidini, M., Passalacqua, R., Barni, S., et al. (2018) · Clinical Lung Cancer · doi:10.1016/j.cllc.2018.02.006 · Cited by 46 · see citing works
Genomic Characterization of Concurrent Alterations in Non-Small Cell Lung Cancer (NSCLC) Harboring Actionable Mutations
Passaro, A., Attili, I., Rappa, A., Vacirca, D., Ranghiero, A., Fumagalli, C., Guarize, J., Spaggiari, L., de Marinis, F., Barberis, M. C. P., et al. (2021) · Cancers · doi:10.3390/cancers13092172 · Cited by 45 · see citing works
The Prognostic Role of KRAS Mutation in Patients with Advanced NSCLC Treated with Second- or Third-line Chemotherapy.
Svatoň, M., Fiala, O., Pešek, M., Bortlíček, Z., Minárik, M., Benešová, L., & Topolčan, O. (2016) · PubMed · Cited by 37 · see citing works
Immune checkpoint inhibitors in oncogene-addicted non-small cell lung cancer: a systematic review and meta-analysis
Guaitoli, G., Tiseo, M., Maïo, M. D., Friboulet, L., & Facchinetti, F. (2021) · Translational Lung Cancer Research · doi:10.21037/tlcr-20-941 · Cited by 37 · see citing works
Comparison of clinical outcome after first-line platinum-based chemotherapy in different types of KRAS mutated advanced non-small-cell lung cancer
Mellema, W. W., Masen-Poos, L., Smit, E. F., Hendriks, L. E. L., Aerts, J. G. J. V., Termeer, A., Goosens, M., Smit, H. J. M., van den Heuvel, M. M., van der Wekken, A. J., et al. (2015) · Lung Cancer · doi:10.1016/j.lungcan.2015.09.012 · Cited by 35 · see citing works
Clinical and Imaging Features of Non-Small Cell Lung Cancer with G12C KRAS Mutation
Wu, M. Y., Zhang, E. W., Strickland, M. R., Mendoza, D. P., Lipkin, L., Lennerz, J. K., Gainor, J. F., Heist, R. S., & Digumarthy, S. R. (2021) · Cancers · doi:10.3390/cancers13143572 · Cited by 35 · see citing works
Abstract 1260: First-in-class, orally bioavailable KRASG12V(ON) tri-complex inhibitors, as single agents and in combinations, drive profound anti-tumor activity in preclinical models of KRASG12V mutant cancers
Koltun, E., Cregg, J., Rice, M. A., Whalen, D. M., Freilich, R., Jiang, J., Hansen, R., Bermingham, A., Knox, J. E., Dinglasan, J., et al. (2021) · Cancer Research · doi:10.1158/1538-7445.am2021-1260 · Cited by 33 · see citing works
KRAS-Mutant Non-Small-Cell Lung Cancer: From Past Efforts to Future Challenges
Ceddia, S., Landi, L. M., & Cappuzzo, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169391 · Cited by 33 · see citing works
Concurrent ROS1 gene rearrangement and KRAS mutation in lung adenocarcinoma: A case report and literature review
Zhu, Y., Lin, X., Li, X., Wu, L., Chen, H., Wang, W., Xu, C., Shen, J., Wei, J., & Du, K. (2017) · Thoracic Cancer · doi:10.1111/1759-7714.12518 · Cited by 27 · see citing works
Lung adenocarcinoma patients with KEAP1 mutation harboring low immune cell infiltration and low activity of immune environment
Cheng, W., Xu, B., Zhang, H., & Fang, S. (2021) · Thoracic Cancer · doi:10.1111/1759-7714.14089 · Cited by 27 · see citing works
The Influence of Oncogenic RAS on Chemotherapy and Radiotherapy Resistance Through DNA Repair Pathways
Cáceres-Gutiérrez, R. E., Alfaro‐Mora, Y., Andonegui, M. A., Díaz‐Chávez, J., & Herrera, L. A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.751367 · Cited by 27 · see citing works
Abstract P05-02: A phase 1b study evaluating the combination of sotorasib, a KRASG12C inhibitor, and afatinib, a pan-ErbB tyrosine kinase inhibitor, in advanced KRAS p.G12C mutated non-small cell lung cancer (NSCLC)
Gandara, D., Marrone, K., Govindan, R., Skoulidis, F., Durm, G., Clarke, J., Frank, R., Krauss, J., Snyder, W., Dai, T., et al. (2021) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.targ-21-p05-02 · Cited by 24 · see citing works
Outcomes of Patients With Advanced NSCLC From the Intergroupe Francophone de Cancérologie Thoracique Biomarkers France Study by KRAS Mutation Subtypes
Ruppert, A.-M., Beau‐Faller, M., Debieuvre, D., Ouafik, L., Westeel, V., Rouquette, I., Mazières, J., Bringuier, P., Monnet, I., Escande, F., et al. (2020) · JTO Clinical and Research Reports · doi:10.1016/j.jtocrr.2020.100052 · Cited by 19 · see citing works
Association of outcomes and co-occuring genomic alterations in patients with KRAS-mutant non-small cell lung cancer.
Riely, G. J., Jordan, E., Kim, H. R., Yu, H. A., Berger, M. F., Solit, D. B., Kris, M. G., Ni, A., Arcila, M. E., & Ladanyi, M. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.15_suppl.9019 · Cited by 14 · see citing works
The KRAS G12C mutation in NSCLC: from target to resistancePreprint
Addeo, A., Banna, G. L., & Friedlaender, A. (2021) · Preprints.org · doi:10.20944/preprints202105.0471.v1 · Cited by 14 · see citing works
Case Report: Outcome of Osimertinib Treatment in Lung Adenocarcinoma Patients With Acquired KRAS Mutations
Xiu, W., Zhang, Q., Yu, M., Huang, Y. C., & Huang, M. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.630256 · Cited by 11 · see citing works
A Highly Verified Assay for KRAS Mutation Detection in Tissue and Plasma of Lung, Colorectal, and Pancreatic Cancer
Li, J., Gan, S., Blair, A., Min, K., Rehage, T., Hoeppner, C., Halait, H., & Brophy, V. H. (2018) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2017-0471-oa · Cited by 10 · see citing works
Abstract 1263: Dual RAF/MEK inhibitor VS-6766 enhances antitumor efficacy of KRAS-G12C inhibitors through a vertical pathway inhibition strategy
Coma, S., Chowdhury, S., & Pachter, J. A. (2021) · Cancer Research · doi:10.1158/1538-7445.am2021-1263 · Cited by 5 · see citing works
Exclusive modifications of NuMA in malignant epithelial cells: A potential therapeutic mechanism
Cohen‐Armon, M. (2022) · Drug Discovery Today · doi:10.1016/j.drudis.2022.02.002 · Cited by 4 · see citing works

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[3]KRAS—An Overview|ScienceDirect Topics Available online: https://www.sciencedirect.com/topics/biochemistry-genetics-and-molecular-biology/kras (accessed on 31 July 2022)
[63]Lumakras®/Lumykras® (Sotorasib) Demonstrates Superior Progression-Free Survival over Docetaxel in First Positive Phase 3 Trial of a Kras G12c Inhibitor in Non-Small Cell Lung Cancer Available online: https://www.amgen.com/newsroom/press-releases/2022/09/lumakraslumykras-sotorasib-demonstrates-superior-progressionfree-survival-over-docetaxel-in-first-positive-phase-3-trial-of-a-kras-g12c-inhibitor-in-nonsmall-cell-lung-cancer (accessed on 20 September 2022)

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Authors: Cascetta, P., Marinello, A., Lazzari, C., Gregorc, V., Planchard, D., Bianco, R., Normanno, N., & Morabito, A.
Affiliations: Institut Gustave Roussy (FR)
Candiolo Cancer Institute (IT)
Federico II University Hospital (IT)
Istituto Nazionale Tumori IRCCS "Fondazione G. Pascale" (IT)
Corresponding author: Morabito, Alessandro
ORCID: Cascetta, Priscilla
Marinello, Arianna
Gregorc, Vanesa
Planchard, David
Bianco, Roberto
Normanno, Nicola
Morabito, Alessandro
Venue: Cancers
Publisher: MDPI AG
Published: 2022-11-04
Volume: 14
Issue: 21
Pages: 5430
ISSN: 2072-6694 (ISSN-L)
DOI: 10.3390/cancers14215430
PMC: PMC9656434
OpenAlex: W4308333785
Cited by: 76
References: 111
Citations by year: 2026: 14 · 2025: 26 · 2024: 20 · 2023: 15 · 2022: 1
FWCI: 2.68
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Cancers (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Keywords: KRAS mutation, non-small cell lung cancer, KRAS inhibitors, sotorasib, adagrasib, acquired drug resistance, TP53, STK11, Keap1, immune checkpoint inhibitors, PD-1/PD-L1, molecular subtypes

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KRAS in NSCLC: State of the Art and Future Perspectives

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