Toward Minimal Residual Disease-Directed Therapy in Melanoma
Open accessAbstract
Many patients with advanced cancers achieve dramatic responses to a panoply of therapeutics yet retain minimal residual disease (MRD), which ultimately results in relapse. To gain insights into the biology of MRD, we applied single-cell RNA sequencing to malignant cells isolated from BRAF mutant patient-derived xenograft melanoma cohorts exposed to concurrent RAF/MEK-inhibition. We identified distinct drug-tolerant transcriptional states, varying combinations of which co-occurred within MRDs from PDXs and biopsies of patients on treatment. One of these exhibited a neural crest stem cell (NCSC) transcriptional program largely driven by the nuclear receptor RXRG. An RXR antagonist mitigated accumulation of NCSCs in MRD and delayed the development of resistance. These data identify NCSCs as key drivers of resistance and illustrate the therapeutic potential of MRD-directed therapy. They also highlight how gene regulatory network architecture reprogramming may be therapeutically exploited to limit cellular heterogeneity, a key driver of disease progression and therapy resistance.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In vivo models have shown similar drug-tolerant slow-cycling persister cells.
“In vivo models have shown similar drug-tolerant slow-cycling persister cells.”
From Emerging Insights into Targeted Therapy-Tolerant Persister Cells in Cancer (2021) · cites this paper as [48]
In melanoma, tumor cells treated with targeted therapy underwent a lineage transition to an undifferentiated mesenchymal cell state leading to drug tolerance and eventually resistance.
“In melanoma, tumor cells treated with targeted therapy underwent a lineage transition to an undifferentiated mesenchymal cell state leading to drug tolerance and eventually resistance [48,80,81].”
From Emerging Insights into Targeted Therapy-Tolerant Persister Cells in Cancer (2021) · cites this paper as [48]
Using the selective antagonist HX531 to target RXR signaling, a lower proportion of NCSC-like cells emerged upon MAPK inhibitor treatment, thus rendering melanomas more sensitive to treatment.
“Using the selective antagonist HX531 to target RXR signaling, a lower proportion of NCSC-like cells emerged upon MAPK inhibitor treatment, thus rendering melanomas more sensitive to treatment [48].”
From Emerging Insights into Targeted Therapy-Tolerant Persister Cells in Cancer (2021) · cites this paper as [48]
Applying single-cell RNA sequencing to BRAF-mutant patient-derived xenograft tumors treated with combination of RAF and ME inhibitors, Rambow et al. identified distinct drug-tolerant transcriptional states, including a neural crest stem cell-like (NCSC) transcriptional program largely driven by the nuclear receptor RXR.
“Applying single-cell RNA sequencing to BRAF-mutant patient-derived xenograft tumors treated with combination of RAF and ME inhibitors, Rambow et al. identified distinct drug-tolerant transcriptional states, including a neural crest stem cell-like (NCSC) transcriptional program largely driven by the nuclear receptor RXR [48].”
From Emerging Insights into Targeted Therapy-Tolerant Persister Cells in Cancer (2021) · cites this paper as [48]
Cites
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581 · see citing works
Verhaak, R. G. W., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., Miller, C. R., Ding, L., Golub, T., Mesirov, J. P., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.020 · Cited by 7,575 · see citing works
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314 · see citing works
Scenic: single-cell regulatory network inference and clustering.
Aibar, S., González-Blas, C. B., Moerman, T., Huynh-Thu, V. A., Imrichova, H., Hulselmans, G., Rambow, F., Marine, J.-C., Geurts, P., Aerts, J., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4463 · Cited by 6,520 · see citing works
Self-citationDissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq
Tirosh, I., Izar, B., Prakadan, S. M., Wadsworth, M. H., Treacy, D., Trombetta, J. J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. (2016) · Science · doi:10.1126/science.aad0501 · Cited by 4,944 · see citing works
Self-citationFull-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
A Chromatin-Mediated Reversible Drug-Tolerant State in Cancer Cell Subpopulations
Sharma, S. V., Lee, D. Y., Li, B., Quinlan, M. P., Takahashi, F., Maheswaran, S., McDermott, U., Azizian, N., Zou, L., Fischbach, M. A., et al. (2010) · Cell · doi:10.1016/j.cell.2010.02.027 · Cited by 2,770 · see citing works
McCarthy, D. J., Campbell, K. R., Lun, A. T. L., & Wills, Q. F. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btw777 · Cited by 1,852 · see citing works
A step-by-step workflow for low-level analysis of single-cell RNA-seq data with Bioconductor
Lun, A. T. L., McCarthy, D. J., & Marioni, J. C. (2016) · F1000Research · doi:10.12688/f1000research.9501.2 · Cited by 1,586 · see citing works
Bayesian approach to single-cell differential expression analysis
Kharchenko, P. V., Silberstein, L., & Scadden, D. T. (2014) · Nature Methods · doi:10.1038/nmeth.2967 · Cited by 1,348 · see citing works
Rare cell variability and drug-induced reprogramming as a mode of cancer drug resistance
Shaffer, S. M., Dunagin, M. C., Torborg, S. R., Torre, E. A., Emert, B., Krepler, C., Beqiri, M., Sproesser, K., Brafford, P. A., Xiao, M., et al. (2017) · Nature · doi:10.1038/nature22794 · Cited by 1,218 · see citing works
Nuclear Receptors, RXR, and the Big Bang
Evans, R. M., & Mangelsdorf, D. J. (2014) · Cell · doi:10.1016/j.cell.2014.03.012 · Cited by 1,200 · see citing works
The Genetic Landscape of Clinical Resistance to RAF Inhibition in Metastatic Melanoma
Allen, E. M. V., Wagle, N., Sucker, A., Treacy, D. J., Johannessen, C. M., Goetz, E. M., Place, C. S., Taylor-Weiner, A. N., Whittaker, S. R., Kryukov, G. V., et al. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0617 · Cited by 904 · see citing works
Oncogenic BRAF Regulates Oxidative Metabolism via PGC1α and MITF
Haq, R., Shoag, J., Andreu-Perez, P., Yokoyama, S., Edelman, H., Rowe, G. C., Frederick, D. T., Hurley, A. D., Nellore, A., Kung, A. L., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.003 · Cited by 818 · see citing works
Self-citationLlorens-Bobadilla, E., Zhao, S., Baser, A., Saiz-Castro, G., Zwadlo, K., & Martin-Villalba, A. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.07.002 · Cited by 778 · see citing works
<i>In vivo</i> Switching of Human Melanoma Cells between Proliferative and Invasive States
Hoek, K. S., Eichhoff, O. M., Schlegel, N. C., Döbbeling, U., Kobert, N., Schaerer, L., Hemmi, S., & Dummer, R. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-2491 · Cited by 743 · see citing works
Self-citationRoesch, A., Vultur, A., Bogeski, I., Wang, H., Zimmermann, K. M., Speicher, D., Körbel, C., Laschke, M. W., Gimotty, P. A., Philipp, S. E., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.05.003 · Cited by 670 · see citing works
<i>destiny</i> : diffusion maps for large-scale single-cell data in R
Angerer, P., Haghverdi, L., Büttner, M., Theis, F. J., Marr, C., & Buettner, F. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btv715 · Cited by 640 · see citing works
Low MITF/AXL ratio predicts early resistance to multiple targeted drugs in melanoma
Müller, J., Krijgsman, O., Tsoi, J., Robert, L., Hugo, W., Song, C., Kong, X., Possik, P. A., Cornelissen-Steijger, P. D. M., Foppen, M. H. G., et al. (2014) · Nature Communications · doi:10.1038/ncomms6712 · Cited by 639 · see citing works
Codega, P., Silva-Vargas, V., Paul, A., Maldonado-Soto, A. R., DeLeo, A. M., Pastrana, E., & Doetsch, F. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.039 · Cited by 634 · see citing works
Tsujikawa, T., Kumar, S., Borkar, R. N., Azimi, V., Thibault, G., Chang, Y. H., Balter, A. I., Kawashima, R., Choe, G. H., Sauer, D., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.037 · Cited by 555 · see citing works
Self-citationHoek, K. S., Schlegel, N. C., Brafford, P. A., Sucker, A., Ugurel, S., Kumar, R., Weber, B. L., Nathanson, K. L., Phillips, D. J., Herlyn, M., et al. (2006) · Pigment Cell Research · doi:10.1111/j.1600-0749.2006.00322.x · Cited by 554 · see citing works
Self-citationBRAF Inhibitor Resistance Mechanisms in Metastatic Melanoma: Spectrum and Clinical Impact
Rizos, H., Menzies, A. M., Pupo, G. M., Carlino, M. S., Fung, C., Hyman, J., Haydu, L. E., Mijatov, B., Becker, T. M., Boyd, S. C., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-3122 · Cited by 543 · see citing works
A Melanoma Cell State Distinction Influences Sensitivity to MAPK Pathway Inhibitors
Konieczkowski, D. J., Johannessen, C. M., Abudayyeh, O. O., Kim, J. W., Cooper, Z. A., Piris, A., Frederick, D. T., Barzily-Rokni, M., Straussman, R., Haq, R., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0424 · Cited by 526 · see citing works
Self-citationDecoding the regulatory landscape of melanoma reveals TEADS as regulators of the invasive cell state
Verfaillie, A., Imrichova, H., Atak, Z. K., Dewaele, M., Rambow, F., Hulselmans, G., Christiaens, V., Svetlichnyy, D., Luciani, F., Van den Mooter, L., et al. (2015) · Nature Communications · doi:10.1038/ncomms7683 · Cited by 489 · see citing works
Self-citationA melanocyte lineage program confers resistance to MAP kinase pathway inhibition
Johannessen, C. M., Johnson, L. A., Piccioni, F., Townes, A., Frederick, D. T., Donahue, M. K., Narayan, R., Flaherty, K. T., Wargo, J. A., Root, D. E., et al. (2013) · Nature · doi:10.1038/nature12688 · Cited by 452 · see citing works
Self-citationCharacterizing transcriptional heterogeneity through pathway and gene set overdispersion analysis
Fan, J., Salathia, N. S., Liu, R., Kaeser, G. E., Yung, Y. C., Herman, J. L., Kaper, F., Fan, J., Zhang, K., Chun, J. J. M., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3734 · Cited by 394 · see citing works
Long, G. V., Fung, C., Menzies, A. M., Pupo, G. M., Carlino, M. S., Hyman, J., Shahheydari, H., Tembe, V., Thompson, J. F., Saw, R. P., et al. (2014) · Nature Communications · doi:10.1038/ncomms6694 · Cited by 375 · see citing works
Genome-wide copy number analysis of single cells
Baslan, T., Kendall, J., Rodgers, L., Cox, H., Riggs, M., Stepansky, A., Troge, J. E., Ravi, K., Esposito, D., Lakshmi, B. V., et al. (2012) · Nature Protocols · doi:10.1038/nprot.2012.039 · Cited by 373 · see citing works
Pisco, A. O., & Huang, S. (2015) · British Journal of Cancer · doi:10.1038/bjc.2015.146 · Cited by 282 · see citing works
Smith, M. P., Brunton, H., Rowling, E. J., Ferguson, J., Arozarena, I., Miskolczi, Z., Lee, J. L., Girotti, M. R., Marais, R., Levesque, M. P., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.02.003 · Cited by 246 · see citing works
Self-citationFallahi‐Sichani, M., Becker, V., Izar, B., Baker, G. J., Lin, J., Boswell, S. A., Shah, P., Rotem, A., Garraway, L. A., & Sorger, P. K. (2017) · Molecular Systems Biology · doi:10.15252/msb.20166796 · Cited by 236 · see citing works
Boshuizen, J., Koopman, L. A., Krijgsman, O., Shahrabi, A., van den Heuvel, E. G., Ligtenberg, M. A., Vredevoogd, D. W., Kemper, K., Kuilman, T., Song, J.-Y., et al. (2018) · Nature Medicine · doi:10.1038/nm.4472 · Cited by 229 · see citing works
Su, Y., Wei, W., Robert, L., Xue, M., Tsoi, J., García-Díaz, Á., Moreno, B. H., Kim, J.-W., Ng, R. H., Lee, J. W., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712064115 · Cited by 226 · see citing works
Haq, R., Yokoyama, S., Hawryluk, E. B., Jönsson, G. B., Frederick, D. T., McHenry, K. T., PORTER, D. A., Tran, T.-N., Love, K. T., Langer, R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205575110 · Cited by 221 · see citing works
Self-citationWellbrock, C., & Arozarena, I. (2015) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12370 · Cited by 218 · see citing works
Phenotype Switching: Tumor Cell Plasticity as a Resistance Mechanism and Target for Therapy
Kemper, K., de Goeje, P. L., Peeper, D. S., & van Amerongen, R. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1174 · Cited by 216 · see citing works
Gopal, Y. N. V., Rizos, H., Chen, G., Deng, W., Frederick, D. T., Cooper, Z. A., Scolyer, R. A., Pupo, G. M., Komurov, K., Sehgal, V., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1392 · Cited by 203 · see citing works
Self-citationMechanisms of Disease: Cancer stem cells--targeting the evil twin
Trumpp, A., & Wiestler, O. D. (2008) · Nature Clinical Practice Oncology · doi:10.1038/ncponc1110 · Cited by 199 · see citing works
A stress-induced early innate response causes multidrug tolerance in melanoma
Menon, D. R., Das, S. K., Krepler, C., Vultur, A., Rinner, B., Schauer, S., Kashofer, K., Wagner, K., Zhang, G., Rad, E. B., et al. (2014) · Oncogene · doi:10.1038/onc.2014.372 · Cited by 171 · see citing works
Separation and parallel sequencing of the genomes and transcriptomes of single cells using G&T-seq
Macaulay, I. C., Teng, M. J., Haerty, W., Kumar, P., Ponting, C. P., & Voet, T. (2016) · Nature Protocols · doi:10.1038/nprot.2016.138 · Cited by 171 · see citing works
Self-citationTargeting minimal residual disease: a path to cure?
Luskin, M. R., Murakami, M. A., Manalis, S. R., & Weinstock, D. M. (2018) · Nature reviews. Cancer · doi:10.1038/nrc.2017.125 · Cited by 171 · see citing works
StemChecker: a web-based tool to discover and explore stemness signatures in gene sets
Pinto, J., Kalathur, R. K. R., Oliveira, D. V., Barata, T., Machado, R. S. R., Machado, S., Pacheco-Leyva, I., Duarte, I., & Futschik, M. E. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv529 · Cited by 126 · see citing works
MeV+R: using MeV as a graphical user interface for Bioconductor applications in microarray analysis
Chu, V. T., Gottardo, R., Raftery, A. E., et al. (2008) · Genome biology · doi:10.1186/gb-2008-9-7-r118 · Cited by 107 · see citing works
Effect of SMURF2 Targeting on Susceptibility to MEK Inhibitors in Melanoma
Smith, M. P., Ferguson, J., Arozarena, I., Hayward, R., Marais, R., Chapman, A., Hurlstone, A. F. L., & Wellbrock, C. (2012) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs471 · Cited by 106 · see citing works
Redmer, T., Welte, Y., Behrens, D., Fichtner, I., Przybilla, D., Wruck, W., Yaspo, M., Lehrach, H. R., Schäfer, R., & Regenbrecht, C. R. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092596 · Cited by 98 · see citing works
Retinoid X Receptor-Antagonistic Diazepinylbenzoic Acids.
Ebisawa, M., Umemiya, H., Ohta, K., Fukasawa, H., Kawachi, E., CHRISTOFFEL, G., Gronemeyer, H., Tsuji, M., Hashimoto, Y., SHUDO, K., et al. (1999) · Chemical and Pharmaceutical Bulletin · doi:10.1248/cpb.47.1778 · Cited by 87 · see citing works
MITF Modulates Therapeutic Resistance through EGFR Signaling
Ji, Z., Chen, Y. E., Kumar, R., Taylor, M., Njauw, C.-N. J., Miao, B., Frederick, D. T., Wargo, J. A., Flaherty, K. T., Jonsson, G. G., et al. (2015) · Journal of Investigative Dermatology · doi:10.1038/jid.2015.105 · Cited by 86 · see citing works
Self-citationTumor progression: Chance and necessity in Darwinian and Lamarckian somatic (mutationless) evolution
Huang, S. (2012) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2012.05.001 · Cited by 76 · see citing works
JUN dependency in distinct early and late BRAF inhibition adaptation states of melanoma
Titz, B., Lomova, A., Le, A., Hugo, W., Kong, X., ten Hoeve, J., Friedman, M., Shi, H., Moriceau, G., Song, C., et al. (2016) · Cell Discovery · doi:10.1038/celldisc.2016.28 · Cited by 68 · see citing works
Agarwal, P., Verzi, M. P., Nguyen, T. N., Hu, J., Ehlers, M. L., McCulley, D. J., Xu, S.-M., Dodou, E., Anderson, J. P., Wei, M. L., et al. (2011) · Development · doi:10.1242/dev.056804 · Cited by 59 · see citing works
ccmGDB: a database for cancer cell metabolism genes
Kim, P., Cheng, F., Zhao, J., & Zhao, Z. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1128 · Cited by 49 · see citing works
Erratum: A stress-induced early innate response causes multidrug tolerance in melanoma
Menon, D. R., Das, S. K., Krepler, C., et al. (2015) · Oncogene · doi:10.1038/onc.2014.432 · Cited by 49 · see citing works
Martino, V. B., Sabljic, T. F., Deschamps, P. A., et al. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.025262 · Cited by 34 · see citing works
Hu, J., Verzi, M. P., Robinson, A. S., Tang, P. L.-F., Hua, L. L., Xu, S.-M., Kwok, P., & Black, B. L. (2015) · Development · doi:10.1242/dev.126391 · Cited by 29 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Methods and applications for single-cell and spatial multi-omics
Vandereyken, K., Sifrim, A., Thienpont, B., & Voet, T. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00580-2 · Cited by 1,244 · see citing works
Self-citationHallmarks of transcriptional intratumour heterogeneity across a thousand tumours
Gavish, A., Tyler, M., Greenwald, A. C., Hoefflin, R., Simkin, D., Tschernichovsky, R., Galili Darnell, N., Somech, E., Barbolin, C., Antman, T., et al. (2023) · Nature · doi:10.1038/s41586-023-06130-4 · Cited by 556 · see citing works
Barkley, D., Moncada, R., Pour, M., Liberman, D. A., Dryg, I., Werba, G., Wang, W., Baron, M., Rao, A., Xia, B., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01141-9 · Cited by 532 · see citing works
Self-citationColorectal Cancer Cells Enter a Diapause-like DTP State to Survive Chemotherapy
Rehman, S. K., Haynes, J., Collignon, E., Brown, K. R., Wang, Y., Nixon, A. M. L., Bruce, J. P., Wintersinger, J. A., Singh Mer, A., Lo, E. B. L., et al. (2021) · Cell · doi:10.1016/j.cell.2020.11.018 · Cited by 495 · see citing works
Phenotype plasticity as enabler of melanoma progression and therapy resistance
Arozarena, I., & Wellbrock, C. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0154-4 · Cited by 381 · see citing works
Disease severity-specific neutrophil signatures in blood transcriptomes stratify COVID-19 patients
(DeCOI), G. C.-1. O. I., Aschenbrenner, A. C., Mouktaroudi, M., Krämer, B., Oestreich, M., Antonakos, N., Nuesch-Germano, M., Gkizeli, K., Bonaguro, L., Reusch, N., et al. (2021) · Genome Medicine · doi:10.1186/s13073-020-00823-5 · Cited by 255 · see citing works
Tumor cell plasticity in targeted therapy-induced resistance: Mechanisms and new strategies
Shi, Z.-D., Pang, K., Wu, Z.-X., Dong, Y., Hao, L., Qin, J.-X., Wang, W., Chen, Z.-S., & Han, C.-H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01383-x · Cited by 256 · see citing works
A TCF4-dependent gene regulatory network confers resistance to immunotherapy in melanoma
Pozniak, J., Pedri, D., Landeloos, E., Van Herck, Y., Antoranz, A., Vanwynsberghe, L., Nowosad, A., Roda, N., Makhzami, S., Bervoets, G., et al. (2024) · Cell · doi:10.1016/j.cell.2023.11.037 · Cited by 199 · see citing works
Self-citationEmerging Insights into Targeted Therapy-Tolerant Persister Cells in Cancer
Cabanos, H. F., & Hata, A. N. (2021) · Cancers · doi:10.3390/cancers13112666 · Cited by 189 · see citing works
Cancer drug-tolerant persister cells: from biological questions to clinical opportunities
Russo, M., Chen, M., Mariella, E., Peng, H., Rehman, S. K., Sancho, E., Sogari, A., Toh, T. S., Balaban, N. Q., Batlle, E., et al. (2024) · Nature Reviews Cancer · doi:10.1038/s41568-024-00737-z · Cited by 210 · see citing works
Self-citationRaman-guided subcellular pharmaco-metabolomics for metastatic melanoma cells
Du, J., Su, Y., Qian, C., Yuan, D., Miao, K., Lee, D., Ng, A. H. C., Wijker, R. S., Ribas, A., Levine, R. D., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18376-x · Cited by 171 · see citing works
Bai, X., Fisher, D. E., & Flaherty, K. T. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0204-6 · Cited by 107 · see citing works
Self-citationAllgayer, H., Mahapatra, S., Mishra, B., Swain, B., Saha, S., Khanra, S., Kumari, K., Panda, V. K., Malhotra, D., Patil, N. S., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02338-2 · Cited by 127 · see citing works
Fan, J., Lu, F., Qin, T., Peng, W., Zhuang, X., Li, Y., Hou, X., Fang, Z., Yang, Y., Guo, E., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01570-0 · Cited by 93 · see citing works
Diener, J., & Sommer, L. (2021) · Stem Cells Translational Medicine · doi:10.1002/sctm.20-0351 · Cited by 64 · see citing works
Varum, S., Baggiolini, A., Zurkirchen, L., Atak, Z. K., Cantù, C., Marzorati, E., Bossart, R., Wouters, J., Häusel, J., Tuncer, E., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.011 · Cited by 65 · see citing works
Self-citationMetabolic alterations mediated by STAT3 promotes drug persistence in CML
Patel, S. B., Nemkov, T., Stefanoni, D., Benavides, G. A., Bassal, M. A., Crown, B. L., Matkins, V. R., Camacho, V., Kuznetsova, V., Hoang, A. T., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01315-0 · Cited by 56 · see citing works
Epigenetic control of melanoma cell invasiveness by the stem cell factor SALL4
Diener, J., Baggiolini, A., Pernebrink, M., Dalcher, D., Lerra, L., Cheng, P. F., Varum, S., Häusel, J., Stierli, S., Treier, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25326-8 · Cited by 34 · see citing works
Self-citationThe AhR‐SRC axis as a therapeutic vulnerability in BRAFi‐resistant melanoma
Paris, A., Tardif, N., Baietti, F. M., Berra, C., Leclair, H. M., Leucci, E., Galibert, M., & Corre, S. (2022) · EMBO Molecular Medicine · doi:10.15252/emmm.202215677 · Cited by 26 · see citing works
Wu, S., Chen, D., & Snyder, M. P. (2022) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2021.102101 · Cited by 25 · see citing works
Secreted Apoe rewires melanoma cell state vulnerability to ferroptosis
More, S., Bonnereau, J., Wouters, D., Spotbeen, X., Karras, P., Rizzollo, F., Killian, T., Venken, T., Naulaerts, S., Vervoort, E., et al. (2024) · Science Advances · doi:10.1126/sciadv.adp6164 · Cited by 25 · see citing works
Self-citationEl Meouche, I., Jain, P., Jolly, M. K., & Capp, J.-P. (2024) · Translational Oncology · doi:10.1016/j.tranon.2024.102069 · Cited by 22 · see citing works
- Authors
- Rambow, F., Rogiers, A., Marin-Bejar, O., Aibar, S., Femel, J., Dewaele, M., Karras, P., Brown, D., Chang, Y. H., Debiec-Rychter, M., Adriaens, C., Radaelli, E., Wolter, P., Bechter, O., Dummer, R., Levesque, M., Piris, A., Frederick, D. T., Boland, G., Flaherty, K. T., van den Oord, J., Voet, T., Aerts, S., Lund, A. W., & Marine, J.-C.
- Affiliations
- VIB-KU Leuven Center for Cancer Biology (BE)
- VIB-KU Leuven Center for Brain & Disease Research (BE)
- Oregon Health & Science University (US)
- KU Leuven (BE)
- University of Pennsylvania (US)
- Universitair Ziekenhuis Leuven (BE)
- University Hospital Zurich (CH)
- Massachusetts General Hospital (US)
- Corresponding author
- Marine, Jean-Christophe
- ORCID
- Rambow, Florian
- Rogiers, Aljosja
- Aibar, Sara
- Femel, Julia
- Dewaele, Michael
- Karras, Panagiotis
- Brown, Daniel
- Chang, Young Hwan
- Adriaens, Carmen
- Radaelli, Enrico
- Bechter, Oliver
- Dummer, Reinhard
- Levesque, Mitchell
- Piris, Adriano
- Frederick, Dennie T.
- Boland, Genevieve
- Flaherty, Keith T.
- Voet, Thierry
- Aerts, Stein
- Lund, Amanda W.
- Marine, Jean-Christophe
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-08
- Volume
- 174
- Issue
- 4
- Pages
- 843-855.e19
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2884607428
- Cited by
- 771
- References
- 56
- Citations by year
- 2026: 90 · 2025: 96 · 2024: 87 · 2023: 124 · 2022: 98 · 2021: 115 · 2020: 96 · 2019: 53 · 2018: 10
- FWCI
- 24.36
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Lirias (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Omics/Marie Curie@VIB
- KUL GOA (14/012)
- VLK
- Interreg
- Fonds voor Wetenschappelijk Onderzoek Vlaanderen (G.0929.16N)
- Swedish Research Council
- OHSU Knight Cancer Center (NIH P30-CA069533)
- Department of Defense Peer Reviewed Cancer Research Program (W81XWH-15-1-0348)
- V Foundation for Cancer Research (V2015-024)
- Cancer Research Institute
- Melanoma Research Alliance
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Melanoma and MAPK Pathways
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- minimal residual disease, melanoma, BRAF mutation, drug resistance, neural crest stem cells, retinoid X receptor, single-cell RNA sequencing, patient-derived xenografts, transcriptional heterogeneity
- MeSH terms
- Animals, Female, Humans, Male, Melanoma, Mutation, Tumor Cells, Cultured, Biomarkers, Tumor, Neoplastic Stem Cells, Gene Expression Regulation, Neoplastic, Mice, SCID, Neoplasm, Residual, Drug Resistance, Neoplasm, Xenograft Model Antitumor Assays, Protein Kinase Inhibitors, Retinoid X Receptor gamma, MAP Kinase Kinase 1, Proto-Oncogene Proteins B-raf, Neural Stem Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
