Drug dependence in cancer is exploitable by optimally constructed treatment holidays.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
27 Nov 2023
27 Nov 2023
Historique:
received:
06
07
2022
accepted:
19
10
2023
pubmed:
28
11
2023
medline:
28
11
2023
entrez:
27
11
2023
Statut:
aheadofprint
Résumé
Cancers with acquired resistance to targeted therapy can become simultaneously dependent on the presence of the targeted therapy drug for survival, suggesting that intermittent therapy may slow resistance. However, relatively little is known about which tumours are likely to become dependent and how to schedule intermittent therapy optimally. Here we characterized drug dependence across a panel of over 75 MAPK-inhibitor-resistant BRAF
Identifiants
pubmed: 38012363
doi: 10.1038/s41559-023-02255-x
pii: 10.1038/s41559-023-02255-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : T32 GM007171
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007171
Pays : United States
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Larkin, J. et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 381, 1535–1546 (2019).
pubmed: 31562797
doi: 10.1056/NEJMoa1910836
Kreft, S. et al. MAPKinase inhibition after failure of immune checkpoint blockade in patients with advanced melanoma—an evaluation of the multicenter prospective skin cancer registry ADOREG. Eur. J. Cancer 167, 32–41 (2022).
pubmed: 35366571
doi: 10.1016/j.ejca.2022.02.023
Atkins, M. B. et al. Combination dabrafenib and trametinib versus combination nivolumab and ipilimumab for patients with advanced BRAF-mutant melanoma: the DREAMseq Trial—ECOG-ACRIN EA6134. J. Clin. Oncol. 41, 186–197 (2023).
pubmed: 36166727
doi: 10.1200/JCO.22.01763
Welsh, S. J., Rizos, H., Scolyer, R. A. & Long, G. V. Resistance to combination BRAF and MEK inhibition in metastatic melanoma: where to next? Eur. J. Cancer 62, 76–85 (2016).
pubmed: 27232329
doi: 10.1016/j.ejca.2016.04.005
Das Thakur, M. et al. Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 494, 251–255 (2013).
pubmed: 23302800
pmcid: 3930354
doi: 10.1038/nature11814
Sun, C. et al. Reversible and adaptive resistance to BRAF(V600E) inhibition in melanoma. Nature 508, 118–122 (2014).
pubmed: 24670642
doi: 10.1038/nature13121
Hong, A. et al. Exploiting drug addiction mechanisms to select against MAPKi-resistant melanoma. Cancer Discov. 8, 74–93 (2018).
pubmed: 28923912
doi: 10.1158/2159-8290.CD-17-0682
Moriceau, G. et al. Tunable-combinatorial mechanisms of acquired resistance limit the efficacy of BRAF/MEK cotargeting but result in melanoma drug addiction. Cancer Cell 27, 240–256 (2015).
pubmed: 25600339
pmcid: 4326539
doi: 10.1016/j.ccell.2014.11.018
Kong, X. et al. Cancer drug addiction is relayed by an ERK2-dependent phenotype switch. Nature 550, 270–274 (2017).
pubmed: 28976960
pmcid: 5640985
doi: 10.1038/nature24037
Algazi, A. P. et al. Continuous versus intermittent BRAF and MEK inhibition in patients with BRAF-mutated melanoma: a randomized phase 2 trial. Nat. Med. 26, 1564–1568 (2020).
pubmed: 33020646
pmcid: 8063889
doi: 10.1038/s41591-020-1060-8
Arozarena, I. & Wellbrock, C. Phenotype plasticity as enabler of melanoma progression and therapy resistance. Nat. Rev. Cancer 19, 377–391 (2019).
pubmed: 31209265
doi: 10.1038/s41568-019-0154-4
Tsoi, J. et al. Multi-stage differentiation defines melanoma subtypes with differential vulnerability to drug-induced iron-dependent oxidative stress. Cancer Cell 33, 890–904.e5 (2018).
pubmed: 29657129
pmcid: 5953834
doi: 10.1016/j.ccell.2018.03.017
Landsberg, J. et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 490, 412–416 (2012).
pubmed: 23051752
doi: 10.1038/nature11538
Mehta, A. et al. Immunotherapy resistance by inflammation-induced dedifferentiation. Cancer Discov. 8, 935–943 (2018).
pubmed: 29899062
pmcid: 6076867
doi: 10.1158/2159-8290.CD-17-1178
Kim, Y. J. et al. Melanoma dedifferentiation induced by IFN-γ epigenetic remodeling in response to anti-PD-1 therapy. J. Clin. Invest. 131, e145859 (2021).
pubmed: 33914706
pmcid: 8203459
doi: 10.1172/JCI145859
Müller, J. et al. Low MITF/AXL ratio predicts early resistance to multiple targeted drugs in melanoma. Nat. Commun. 5, 5712 (2014).
pubmed: 25502142
doi: 10.1038/ncomms6712
Konieczkowski, D. J. et al. A melanoma cell state distinction influences sensitivity to MAPK pathway inhibitors. Cancer Discov. 4, 816–827 (2014).
pubmed: 24771846
pmcid: 4154497
doi: 10.1158/2159-8290.CD-13-0424
Johannessen, C. M. et al. A melanocyte lineage program confers resistance to MAP kinase pathway inhibition. Nature 504, 138–142 (2013).
pubmed: 24185007
pmcid: 4098832
doi: 10.1038/nature12688
Enriquez-Navas, P. M. et al. Exploiting evolutionary principles to prolong tumor control in preclinical models of breast cancer. Sci. Transl. Med. 8, 327ra24 (2016).
pubmed: 26912903
pmcid: 4962860
doi: 10.1126/scitranslmed.aad7842
Silva, A. S. et al. Evolutionary approaches to prolong progression-free survival in breast cancer. Cancer Res. 72, 6362–6370 (2012).
pubmed: 23066036
pmcid: 3525750
doi: 10.1158/0008-5472.CAN-12-2235
Gatenby, R. A., Silva, A. S., Gillies, R. J. & Frieden, B. R. Adaptive therapy. Cancer Res. 69, 4894–4903 (2009).
pubmed: 19487300
pmcid: 3728826
doi: 10.1158/0008-5472.CAN-08-3658
Smalley, I. et al. Leveraging transcriptional dynamics to improve BRAF inhibitor responses in melanoma. eBioMedicine 48, 178–190 (2019).
pubmed: 31594749
pmcid: 6838387
doi: 10.1016/j.ebiom.2019.09.023
Lin, K. H. et al. Using antagonistic pleiotropy to design a chemotherapy-induced evolutionary trap to target drug resistance in cancer. Nat. Genet. 52, 408–417 (2020).
pubmed: 32203462
pmcid: 7398704
doi: 10.1038/s41588-020-0590-9
Zhao, B. et al. Exploiting temporal collateral sensitivity in tumor clonal evolution. Cell 165, 234–246 (2016).
pubmed: 26924578
pmcid: 5152932
doi: 10.1016/j.cell.2016.01.045
Maltas, J. & Wood, K. B. Pervasive and diverse collateral sensitivity profiles inform optimal strategies to limit antibiotic resistance. PLoS Biol 17, e3000515, https://doi.org/10.1371/journal.pbio.3000515 (2019).
doi: 10.1371/journal.pbio.3000515
pubmed: 31652256
pmcid: 6834293
Maltas, J., Krasnick, B. & Wood, K. B. Using selection by nonantibiotic stressors to sensitize bacteria to antibiotics. Mol. Biol. Evol. 37, 1394–1406 (2020).
pubmed: 31851309
doi: 10.1093/molbev/msz303
West, J., Ma, Y. & Newton, P. K. Capitalizing on competition: an evolutionary model of competitive release in metastatic castration resistant prostate cancer treatment. J. Theor. Biol. 455, 249–260 (2018).
pubmed: 30048718
pmcid: 7519622
doi: 10.1016/j.jtbi.2018.07.028
Wargo, A. R. et al. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl Acad. Sci. USA 104, 19914–19919, https://doi.org/10.1073/pnas.0707766104 (2007).
doi: 10.1073/pnas.0707766104
pubmed: 18056635
pmcid: 2148397
Kaznatcheev, A., Peacock, J., Basanta, D., Marusyk, A. & Scott, J. G. Fibroblasts and alectinib switch the evolutionary games played by non-small cell lung cancer. Nat. Ecol. Evol. 3, 450–456 (2019).
pubmed: 30778184
pmcid: 6467526
doi: 10.1038/s41559-018-0768-z
Farrokhian N. et al. Measuring competitive exclusion in non-small cell lung cancer. Sci Adv. 8, eabm7212 (2022); https://science.org/doi/10.1126/sciadv.abm7212
Korolev, K. S., Xavier, J. B. & Gore, J. Turning ecology and evolution against cancer. Nat. Rev. Cancer 14, 371–380 (2014).
pubmed: 24739582
doi: 10.1038/nrc3712
Li, Y., Cheng, H. S., Chng, W. J. & Tergaonkar, V. Activation of mutant TERT promoter by RAS–ERK signaling is a key step in malignant progression of BRAF-mutant human melanomas. Proc. Natl Acad. Sci. USA 113, 14402–14407 (2016).
pubmed: 27911794
pmcid: 5167176
doi: 10.1073/pnas.1611106113
Khaliq, M., Manikkam, M., Martinez, E. D. & Fallahi-Sichani, M. Epigenetic modulation reveals differentiation state specificity of oncogene addiction. Nat. Commun. 12, 1536 (2021).
pubmed: 33750776
pmcid: 7943789
doi: 10.1038/s41467-021-21784-2
Tsherniak, A. et al. Defining a cancer dependency map. Cell 170, 564–576.e16 (2017).
pubmed: 28753430
pmcid: 5667678
doi: 10.1016/j.cell.2017.06.010
Luebker, S. A. & Koepsell, S. A. Diverse mechanisms of BRAF inhibitor resistance in melanoma identified in clinical and preclinical studies. Front. Oncol. 9, 268 (2019).
pubmed: 31058079
pmcid: 6478763
doi: 10.3389/fonc.2019.00268
Rizos, H. et al. BRAF inhibitor resistance mechanisms in metastatic melanoma: spectrum and clinical impact. Clin. Cancer Res. 20, 1965–1977 (2014).
pubmed: 24463458
doi: 10.1158/1078-0432.CCR-13-3122
Ito, T. et al. Paralog knockout profiling identifies DUSP4 and DUSP6 as a digenic dependence in MAPK pathway-driven cancers. Nat. Genet. 53, 1664–1672 (2021).
pubmed: 34857952
doi: 10.1038/s41588-021-00967-z
Gutierrez-Prat N. et al. DUSP4 protects BRAF- and NRAS-mutant melanoma from oncogene overdose through modulation of MITF. Life Sci. Alliance 5, e202101235 (2022); https://www.life-science-alliance.org/content/5/9/e202101235
Cho, E., Lou, H. J., Kuruvilla, L., Calderwood, D. A. & Turk, B. E. PPP6C negatively regulates oncogenic ERK signaling through dephosphorylation of MEK. Cell Rep. 34, 108928 (2021).
pubmed: 33789117
pmcid: 8068315
doi: 10.1016/j.celrep.2021.108928
Ji, Z. et al. MITF modulates therapeutic resistance through EGFR signaling. J. Invest. Dermatol. 135, 1863–1872 (2015).
pubmed: 25789707
pmcid: 4466007
doi: 10.1038/jid.2015.105
Labrie, M., Brugge, J. S., Mills, G. B. & Zervantonakis, I. K. Therapy resistance: opportunities created by adaptive responses to targeted therapies in cancer. Nat. Rev. Cancer 22, 323–339 (2022).
pubmed: 35264777
pmcid: 9149051
doi: 10.1038/s41568-022-00454-5
Shaffer, S. M. et al. Rare cell variability and drug-induced reprogramming as a mode of cancer drug resistance. Nature 546, 431–435 (2017).
pubmed: 28607484
pmcid: 5542814
doi: 10.1038/nature22794
Su, Y. et al. Single-cell analysis resolves the cell state transition and signaling dynamics associated with melanoma drug-induced resistance. Proc. Natl Acad. Sci. USA 114, 13679–13684 (2017).
pubmed: 29229836
pmcid: 5748184
doi: 10.1073/pnas.1712064115
Nyberg, W. A. et al. The bromodomain protein TRIM28 controls the balance between growth and invasiveness in melanoma. EMBO Rep. 24, e54944 (2023).
pubmed: 36341538
doi: 10.15252/embr.202254944
Kavran, A. J. et al. Intermittent treatment of BRAF
pubmed: 35290123
pmcid: 8944661
doi: 10.1073/pnas.2113535119
Strobl, M. A. R. et al. Spatial structure impacts adaptive therapy by shaping intra-tumoral competition. Commun. Med. 2, 46 (2022).
pubmed: 35603284
pmcid: 9053239
doi: 10.1038/s43856-022-00110-x
Yu, H. A. et al. Phase 2 study of intermittent pulse dacomitinib in patients with advanced non-small cell lung cancers. Lung Cancer 112, 195–199 (2017).
pubmed: 29191595
doi: 10.1016/j.lungcan.2017.08.017
Killarney, S. T. et al. Executioner caspases restrict mitochondrial RNA-driven type I IFN induction during chemotherapy-induced apoptosis. Nat. Commun. 14, 1399 (2023).
pubmed: 36918588
pmcid: 10015073
doi: 10.1038/s41467-023-37146-z
Martz, C. A. et al. Systematic identification of signaling pathways with potential to confer anticancer drug resistance. Sci. Signal. 7, ra121 (2014).
pubmed: 25538079
pmcid: 4353587
doi: 10.1126/scisignal.aaa1877
Hart, T. et al. Evaluation and design of genome-wide CRISPR/SpCas9 knockout screens. G3 7, 2719–2727 (2017).
pubmed: 28655737
pmcid: 5555476
doi: 10.1534/g3.117.041277
Guzmán, C. et al. ColonyArea: an ImageJ plugin to automatically quantify colony formation in clonogenic assays. PLoS One 9, e92444, https://doi.org/10.1371/journal.pone.0092444 (2014).
doi: 10.1371/journal.pone.0092444
pubmed: 24647355
pmcid: 3960247
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517
pmcid: 1239896
doi: 10.1073/pnas.0506580102
Barbie, D. A. et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462, 108–112 (2009).
pubmed: 19847166
pmcid: 2783335
doi: 10.1038/nature08460
Reich, M. et al. GenePattern 2.0. Nat. Genet. 38, 500–501 (2006).
pubmed: 16642009
doi: 10.1038/ng0506-500
Bravo, R. R. et al. Hybrid Automata Library: a flexible platform for hybrid modeling with real-time visualization. PLoS Comput. Biol. 16, e1007635 (2020).
pubmed: 32155140
pmcid: 7105119
doi: 10.1371/journal.pcbi.1007635