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Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3

Ethan V. Abel, … , Paolo Fortina, Andrew E. Aplin

Ethan V. Abel, … , Paolo Fortina, Andrew E. Aplin

Published April 1, 2013
Citation Information: J Clin Invest. 2013;123(5):2155-2168. https://doi.org/10.1172/JCI65780.

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Protein Kinase A Signaling Inhibits Iridophore Differentiation in Zebrafish C Cooper, S Erickson, S Yin, T Moravec, B Peh, K Curran	Journal of Developmental Biology	2018
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Functional genomic characterization of a synthetic anti-HER3 antibody reveals a role for ubiquitination by RNF41 in the anti-proliferative response JP Turowec, EW Lau, X Wang, KR Brown, FA Fellouse, KK Jawanda, J Pan, J Moffat, SS Sidhu	The Journal of biological chemistry	2018
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The natural compound fucoidan from New Zealand Undaria pinnatifida synergizes with the ERBB inhibitor lapatinib enhancing melanoma growth inhibition V Thakur, J Lu, G Roscilli, L Aurisicchio, M Cappelletti, E Pavoni, WL White, B Bedogni	Oncotarget	2017
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Targeting mitochondrial biogenesis to overcome drug resistance to MAPK inhibitors Gao Zhang, Dennie Frederick, Lawrence Wu, Zhi Wei, Clemens Krepler, Satish Srinivasan, Young Chan Chae, Xiaowei Xu, Harry Choi, Elaida Dimwamwa, Omotayo Ope, Batool Shannan, Devraj Basu, Dongmei Zhang, Manti Guha, Min Xiao, Sergio Randell, Katrin Sproesser, Wei Xu, Jephrey Liu, Giorgos Karakousis, Lynn Schuchter, Tara C. Gangadhar, Ravi Amaravadi, Mengnan Gu, Caiyue Xu, Abheek Ghosh, Weiting Xu, Tian Tian, Jie Zhang, Shijie Zha, Qin Liu, Patricia Brafford, Ashani Weeraratna, Michael Davies, Jennifer Wargo, Narayan Avadhani, Yiling Lu, Gordon Mills, Dario C. Altieri, Keith Flaherty, Meenhard Herlyn	Journal of Clinical Investigation	2016
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FOXD3 Regulates Pluripotent Stem Cell Potential by Simultaneously Initiating and Repressing Enhancer Activity R Krishnakumar, AF Chen, MG Pantovich, M Danial, RJ Parchem, PA Labosky, R Blelloch	Cell Stem Cell	2016
Asparagine promotes cancer cell proliferation through use as an amino acid exchange factor AS Krall, S Xu, TG Graeber, D Braas, HR Christofk	Nature Communications	2016
MIG6 Is MEK Regulated and Affects EGF-Induced Migration in Mutant NRAS Melanoma HL Vu, S Rosenbaum, C Capparelli, TJ Purwin, MA Davies, AC Berger, AE Aplin	Journal of Investigative Dermatology	2016
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A Nexus Consisting of Beta-Catenin and Stat3 Attenuates BRAF Inhibitor Efficacy and Mediates Acquired Resistance to Vemurafenib T Sinnberg, E Makino, MA Krueger, A Velic, B Macek, U Rothbauer, N Groll, O Pötz, S Czemmel, H Niessner, F Meier, K Ikenberg, C Garbe, B Schittek	EBioMedicine	2016
Novobiocin Analogues That Inhibit the MAPK Pathway JA Hall, S Seedarala, H Zhao, G Garg, S Ghosh, BS Blagg	Journal of Medicinal Chemistry	2016
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RMEL3, a novel BRAF^V600E-associated long noncoding RNA, is required for MAPK and PI3K signaling in melanoma L Goedert, CG Pereira, J Roszik, JR Plaça, C Cardoso, G Chen, W Deng, VG Yennu-Nanda, WA Silva, MA Davies, EM Espreafico	Oncotarget	2016
Microphthalmia-associated transcription factor in melanoma development and MAP-kinase pathway targeted therapy C Wellbrock, I Arozarena	Pigment Cell & Melanoma Research	2015
Fibronectin induction abrogates the BRAF inhibitor response of BRAF V600E/PTEN-null melanoma cells IV Fedorenko, EV Abel, JM Koomen, B Fang, ER Wood, YA Chen, KJ Fisher, S Iyengar, KB Dahlman, JA Wargo, KT Flaherty, JA Sosman, VK Sondak, JL Messina, GT Gibney, KS Smalley	Oncogene	2015
Genetic Events That Limit the Efficacy of MEK and RTK Inhibitor Therapies in a Mouse Model of KRAS-Driven Pancreatic Cancer P Pettazzoni, A Viale, P Shah, A Carugo, H Ying, H Wang, G Genovese, S Seth, R Minelli, T Green, E Huang-Hobbs, D Corti, N Sanchez, L Nezi, M Marchesini, A Kapoor, W Yao, ME Francesco, A Petrocchi, AK Deem, K Scott, S Colla, GB Mills, JB Fleming, TP Heffernan, P Jones, C Toniatti, RA DePinho, GF Draetta	Cancer research	2015
Targeting HER3 by interfering with its Sec61-mediated cotranslational insertion into the endoplasmic reticulum A Ruiz-Saenz, M Sandhu, Y Carrasco, RL Maglathlin, J Taunton, MM Moasser	Oncogene	2015
NF-κB Regulation of c-FLIP Promotes TNFα-Mediated RAF Inhibitor Resistance in Melanoma Y Shao, K Le, H Cheng, AE Aplin	Journal of Investigative Dermatology	2015
The broad-spectrum receptor tyrosine kinase inhibitor dovitinib suppresses growth of BRAF -mutant melanoma cells in combination with other signaling pathway inhibitors CG Langdon, MA Held, JT Platt, K Meeth, P Iyidogan, R Mamillapalli, AB Koo, M Klein, Z Liu, MW Bosenberg, DF Stern	Pigment Cell & Melanoma Research	2015
ErbB3 upregulation by the HNSCC 3D microenvironment modulates cell survival and growth JO Humtsoe, E Pham, RJ Louie, DA Chan, RH Kramer	Oncogene	2015
Early decline in serum phospho-CSE1L levels in vemurafenib/sunitinib-treated melanoma and sorafenib/lapatinib-treated colorectal tumor xenografts WR Lee, SC Shen, YH Shih, CL Chou, JT Tseng, SY Chin, KH Liu, YC Chen, MC Jiang	Journal of Translational Medicine	2015
Downregulation of the Ubiquitin Ligase RNF125 Underlies Resistance of Melanoma Cells to BRAF Inhibitors via JAK1 Deregulation H Kim, DT Frederick, MP Levesque, ZA Cooper, Y Feng, C Krepler, L Brill, Y Samuels, NK Hayward, A Perlina, A Piris, T Zhang, R Halaban, MM Herlyn, KM Brown, JA Wargo, R Dummer, KT Flaherty, ZA Ronai	Cell Reports	2015
Paracrine Effect of NRG1 and HGF Drives Resistance to MEK Inhibitors in Metastatic Uveal Melanoma H Cheng, M Terai, K Kageyama, S Ozaki, PA McCue, T Sato, AE Aplin	Cancer research	2015
Converting biology into clinical benefit: lessons learned from BRAF inhibitors J McQuade, MA Davies	Melanoma Management	2015
BRAF Inhibition Generates a Host–Tumor Niche that Mediates Therapeutic Escape IV Fedorenko, JA Wargo, KT Flaherty, JL Messina, KS Smalley	Journal of Investigative Dermatology	2015
ErbB3-ErbB2 Complexes as a Therapeutic Target in a Subset of Wild-type BRAF/NRAS Cutaneous Melanomas C Capparelli, S Rosenbaum, LD Berman-Booty, A Salhi, N Gaborit, T Zhan, I Chervoneva, J Roszik, SE Woodman, MA Davies, YY Setiady, I Osman, Y Yarden, AE Aplin	Cancer research	2015
Fibroblast-derived Neuregulin 1 Promotes Compensatory ErbB3 Receptor Signaling in Mutant BRAF Melanoma C Capparelli, S Rosenbaum, AC Berger, AE Aplin	The Journal of biological chemistry	2015
Systems Analysis of Adaptive Responses to MAP Kinase Pathway Blockade in BRAF Mutant Melanoma BJ Capaldo, D Roller, MJ Axelrod, AF Koeppel, EF Petricoin, CL Slingluff, MJ Weber, AJ Mackey, D Gioeli, S Bekiranov, K Smalley	PloS one	2015
Dynamical modeling of uncertain interaction-based genomic networks DN Mohsenizadeh, J Hua, M Bittner, ER Dougherty	BMC bioinformatics	2015
Histone Modifications, Modifiers and Readers in Melanoma Resistance to Targeted and Immune Therapy S Gallagher, J Tiffen, P Hersey	Cancers	2015
Inhibition of ErbB3 by a monoclonal antibody that locks the extracellular domain in an inactive configuration S Lee, EB Greenlee, JR Amick, GF Ligon, JS Lillquist, EJ Natoli, Y Hadari, D Alvarado, J Schlessinger	Proceedings of the National Academy of Sciences	2015
MEK inhibitors and their potential in the treatment of advanced melanoma: the advantages of combination therapy E Maverakis, K Tran, M Cheng, A Mitra, H Ogawa, V Shi, L Olney, A Kloxin	Drug design, development and therapy	2015
Combinatorial drug screening and molecular profiling reveal diverse mechanisms of intrinsic and adaptive resistance to BRAF inhibition in V600E BRAF mutant melanomas Roller DG, Capaldo B, Bekiranov S, Mackey AJ, Conaway MR, Petricoin EF, Gioeli D, Weber MJ	Oncotarget	2015
Overcoming melanoma resistance to vemurafenib by targeting CCL2-induced miR-34a, miR-100 and miR-125b Vergani E, Di Guardo L, Dugo M, Rigoletto S, Tragni G, Ruggeri R, Perrone F, Tamborini E, Gloghini A, Arienti F, Vergani B, Deho P, De Cecco L, Vallacchi V, Frati P, Shahaj E, Villa A, Santinami M, De Braud F, Rivoltini L, Rodolfo M	Oncotarget	2015
A melanoma subtype with intrinsic resistance to BRAF inhibition identified by receptor tyrosine kinases gene-driven classification Dugo M, Nicolini G, Tragni G, Bersani I, Tomassetti A, Colonna V, Del Vecchio M, De Braud F, Canevari S, Anichini A, Sensi M	Oncotarget	2015
Targeting ER stress induced-autophagy overcomes BRAF inhibitor resistance in melanoma Xiao-hong Ma, Shengfu Piao, Souvik Dey, Quentin Mcafee, Giorgos Karakousis, Jessie Villanueva, Lori Hart, Samuel Levi, Janice Hu, Gao Zhang, Rossitza Lazova, Vincent Klump, John Pawelek, Xiaowei Xu, Wei Xu, Lynn Schuchter, Michael Davies, Meenhard Herlyn, Jeffrey Winkler, Constantinos Koumenis, Ravi Amaravadi	Journal of Clinical Investigation	2014
Change or die: Targeting adaptive signaling to kinase inhibition in cancer cells VW Rebecca, KS Smalley	Biochemical Pharmacology	2014
Targeting RAF kinases for cancer therapy: BRAF-mutated melanoma and beyond M Holderfield, MM Deuker, F McCormick, M McMahon	Nature Reviews Cancer	2014
Melanoma: oncogenic drivers and the immune system Niki Karachaliou, Sara Pilotto, Cristina Teixidó, Santiago Viteri, María González-Cao, Aldo Riso, Daniela Morales-Espinosa, Miguel Angel Molina, Imane Chaib, Mariacarmela Santarpia, Eduardo Richardet, Emilio Bria, Rafael Rosell	Annals of translational medicine
Targeting the complexity of Src signalling in the tumour microenvironment of pancreatic cancer: from mechanism to therapy A Parkin, J Man, P Timpson, M Pajic	The FEBS journal	2019
Towards combinatorial targeted therapy in melanoma: from pre-clinical evidence to clinical application (review) G Grazia, I Penna, V Perotti, A Anichini, E Tassi	International journal of oncology	2014
Identification of PLX4032-resistance mechanisms and implications for novel RAF inhibitors J Choi, SF Landrette, T Wang, P Evans, A Bacchiocchi, R Bjornson, E Cheng, AL Stiegler, S Gathiaka, O Acevedo, TJ Boggon, M Krauthammer, R Halaban, T Xu	Pigment Cell & Melanoma Research	2014
Linking SOX10 to a slow-growth resistance phenotype G Zhang, M Herlyn	Cell Research	2014
Ligand-associated ERBB2/3 activation confers acquired resistance to FGFR inhibition in FGFR3-dependent cancer cells J Wang, O Mikse, RG Liao, Y Li, L Tan, PA Janne, NS Gray, K Wong, PS Hammerman	Oncogene	2014
Adaptive resistance to RAF inhibitors in melanoma CH Kugel, AE Aplin	Pigment Cell & Melanoma Research	2014
Targeting of erbB3 receptor to overcome resistance in cancer treatment J Ma, H Lyu, J Huang, B Liu	Molecular Cancer	2014
Tumor heterogeneity and plasticity as elusive drivers for resistance to MAPK pathway inhibition in melanoma A Roesch	Oncogene	2014
ERBB3 is required for metastasis formation of melanoma cells S Tiwary, M Preziosi, PG Rothberg, N Zeitouni, N Corson, L Xu	Oncogenesis	2014
Molecular Pathways: HER3 Targeted Therapy K Gala, S Chandarlapaty	Clinical cancer research	2014
Ligand-Independent EPHA2 Signaling Drives the Adoption of a Targeted Therapy-Mediated Metastatic Melanoma Phenotype KH Paraiso, MD Thakur, B Fang, JM Koomen, IV Fedorenko, JK John, H Tsao, KT Flaherty, VK Sondak, JL Messina, EB Pasquale, A Villagra, UN Rao, JM Kirkwood, F Meier, S Sloot, GT Gibney, D Stuart, H Tawbi, KS Smalley	Cancer Discovery	2014
Inhibition of HSP90 by AT13387 Delays the Emergence of Resistance to BRAF Inhibitors and Overcomes Resistance to Dual BRAF and MEK Inhibition in Melanoma Models T Smyth, KH Paraiso, K Hearn, AM Rodriguez-Lopez, JM Munck, HE Haarberg, VK Sondak, NT Thompson, M Azab, JF Lyons, KS Smalley, NG Wallis	Molecular cancer therapeutics	2014
FOXD3 Modulates Migration through Direct Transcriptional Repression of TWIST1 in Melanoma MB Weiss, EV Abel, N Dadpey, AE Aplin	Molecular cancer research : MCR	2014
Function-Blocking ERBB3 Antibody Inhibits the Adaptive Response to RAF Inhibitor CH Kugel, EJ Hartsough, MA Davies, YY Setiady, AE Aplin	Cancer research	2014
Molecular Profiling of Patient-Matched Brain and Extracranial Melanoma Metastases Implicates the PI3K Pathway as a Therapeutic Target G Chen, N Chakravarti, K Aardalen, AJ Lazar, MT Tetzlaff, B Wubbenhorst, SB Kim, S Kopetz, AA Ledoux, YN Gopal, CG Pereira, W Deng, JS Lee, KL Nathanson, KD Aldape, VG Prieto, D Stuart, MA Davies	Clinical cancer research	2014
Evaluating Melanoma Drug Response and Therapeutic Escape with Quantitative Proteomics VW Rebecca, E Wood, IV Fedorenko, KH Paraiso, HE Haarberg, Y Chen, Y Xiang, A Sarnaik, GT Gibney, VK Sondak, JM Koomen, KS Smalley	Molecular & cellular proteomics : MCP	2014
Beneficial Effects of RAF Inhibitor in Mutant BRAF Splice Variant-Expressing Melanoma EJ Hartsough, KJ Basile, AE Aplin	Molecular cancer research : MCR	2014
Pan-erbB inhibition potentiates BRAF inhibitors for melanoma treatment: YK Ng, JY Lee, KM Supko, A Khan, SM Torres, M Berwick, J Ho, JM Kirkwood, JM Siegfried, LP Stabile	Melanoma Research	2014
Overcoming resistance to BRAF inhibition in BRAF-mutated metastatic melanoma Spagnolo F, Ghiorzo P, Queirolo P	Oncotarget	2014
ROCK1 is a potential combinatorial drug target for BRAF mutant melanoma Smit MA, Maddalo G, Greig K, Raaijmakers LM, Possik PA, van Breukelen B, Cappadona S, Heck AJ, Altelaar AM, Peeper DS	Molecular Systems Biology	2014
Pathways and therapeutic targets in melanoma Shtivelman E, Davies MA, Hwu P, Yang J, Lotem M, Oren M, Flaherty KT, Fisher DE	Oncotarget	2014
Activation of an early feedback survival loop involving phospho-ErbB3 is a general response of melanoma cells to RAF/MEK inhibition and is abrogated by anti-ErbB3 antibodies L Fattore, E Marra, ME Pisanu, A Noto, C de Vitis, F Belleudi, L Aurisicchio, R Mancini, MR Torrisi, PA Ascierto, G Ciliberto	Journal of Translational Medicine	2013
Targeted therapies in development for non-small cell lung cancer T Reungwetwattana, GK Dy	Journal of carcinogenesis	2013
Concurrent MEK2 Mutation and BRAF Amplification Confer Resistance to BRAF and MEK Inhibitors in Melanoma J Villanueva, JR Infante, C Krepler, P Reyes-Uribe, M Samanta, HY Chen, B Li, RK Swoboda, M Wilson, A Vultur, M Fukunaba-Kalabis, B Wubbenhorst, TY Chen, Q Liu, K Sproesser, DJ DeMarini, TM Gilmer, AM Martin, R Marmorstein, DC Schultz, DW Speicher, GC Karakousis, W Xu, RK Amaravadi, X Xu, LM Schuchter, M Herlyn, KL Nathanson	Cell Reports	2013
Resistance to RAF Inhibitors Revisited E Hartsough, Y Shao, AE Aplin	Journal of Investigative Dermatology	2013
Paradoxical oncogenesis--the long-term effects of BRAF inhibition in melanoma GT Gibney, JL Messina, IV Fedorenko, VK Sondak, KS Smalley	Nature Reviews Clinical Oncology	2013
Other targeted drugs in melanoma María González-Cao, Jordi Rodón, Niki Karachaliou, Jesús Sánchez, Mariacarmela Santarpia, Santiago Viteri, Sara Pilotto, Cristina Teixidó, Aldo Riso, Rafael Rosell	Annals of translational medicine
HER-3: hub for escape mechanisms E Capone, PR Prasetyanti, G Sala	Aging	2015
Combination of antibodies directed against different ErbB3 surface epitopes prevents the establishment of resistance to BRAF/MEK inhibitors in melanoma D Malpicci, E Marra, F Belleudi, A Noto, CD Vitis, ME Pisanu, P Coluccia, R Camerlingo, G Roscilli, A Ribas, AD Napoli, MR Torrisi, L Aurisicchio, PA Ascierto, R Mancini, G Ciliberto, L Fattore	Oncotarget	2015
ErbB-3 activation by NRG-1β sustains growth and promotes vemurafenib resistance in BRAF-V600E colon cancer stem cells (CSCs) PR Prasetyanti, E Capone, D Barcaroli, D DAgostino, S Volpe, A Benfante, S Hooff, V Iacobelli, C Rossi, S Iacobelli, JP Medema, VD Laurenzi, G Sala	Oncotarget	2015
ERBB activation modulates sensitivity to MEK1/2 inhibition in a subset of driver-negative melanoma KE Hutchinson, DB Johnson, AS Johnson, V Sanchez, M Kuba, P Lu, X Chen, MC Kelley, Q Wang, Z Zhao, M Kris, MF Berger, JA Sosman, W Pao	Oncotarget	2015
MicroRNAs in melanoma development and resistance to target therapy L Fattore, S Costantini, D Malpicci, CF Ruggiero, PA Ascierto, CM Croce, R Mancini, G Ciliberto	Oncotarget	2015
EV20, a Novel Anti-ErbB-3 Humanized Antibody, Promotes ErbB-3 Down-Regulation and Inhibits Tumor Growth In Vivo. Sala G, Rapposelli IG, Ghasemi R, Piccolo E, Traini S, Capone E, Rossi C, Pelliccia A, Di Risio A, D'Egidio M, Tinari N, Muraro R, Iacobelli S	Translational oncology	2013

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