. 2020 Oct; 12(10):.
doi: 10.3390/cancers12102870.

Tumor Microenvironment: Implications in Melanoma Resistance to Targeted Therapy and Immunotherapy

Italia Falcone 1 Fabiana Conciatori 1 Chiara Bazzichetto 1 Gianluigi Ferretti 1 Francesco Cognetti 1 Ludovica Ciuffreda 2 Michele Milella 3 
  • PMID: 33036192
  •     180 References
  •     19 citations


Antitumor therapies have made great strides in recent decades. Chemotherapy, aggressive and unable to discriminate cancer from healthy cells, has given way to personalized treatments that, recognizing and blocking specific molecular targets, have paved the way for targeted and effective therapies. Melanoma was one of the first tumor types to benefit from this new care frontier by introducing specific inhibitors for v-Raf murine sarcoma viral oncogene homolog B (BRAF), mitogen-activated protein kinase (MEK), v-kit Hardy-Zuckerman 4 feline sarcoma viral oncogene homolog (KIT), and, recently, immunotherapy. However, despite the progress made in the melanoma treatment, primary and/or acquired drug resistance remains an unresolved problem. The molecular dynamics that promote this phenomenon are very complex but several studies have shown that the tumor microenvironment (TME) plays, certainly, a key role. In this review, we will describe the new melanoma treatment approaches and we will analyze the mechanisms by which TME promotes resistance to targeted therapy and immunotherapy.

Keywords: immunotherapy; melanoma; targeted therapy; therapeutic resistance; tumor microenvironment.

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Nature, 2010 Feb 25; 464(7287). PMID: 20179705    Free PMC article.
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Myeloid Cells and Related Chronic Inflammatory Factors as Novel Predictive Markers in Melanoma Treatment with Ipilimumab.
Christoffer Gebhardt, Alexandra Sevko, +10 authors, Viktor Umansky.
Clin Cancer Res, 2015 Aug 21; 21(24). PMID: 26289067
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PTEN as a Prognostic/Predictive Biomarker in Cancer: An Unfulfilled Promise?
Chiara Bazzichetto, Fabiana Conciatori, +5 authors, Ludovica Ciuffreda.
Cancers (Basel), 2019 Mar 31; 11(4). PMID: 30925702    Free PMC article.
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Jean S Marshall, Richard Warrington, Wade Watson, Harold L Kim.
Allergy Asthma Clin Immunol, 2018 Sep 29; 14(Suppl 2). PMID: 30263032    Free PMC article.
PD-1 and PD-L1 antibodies for melanoma.
Katy K Tsai, Inés Zarzoso, Adil I Daud.
Hum Vaccin Immunother, 2015 Jan 28; 10(11). PMID: 25625924    Free PMC article.
Association of Pembrolizumab With Tumor Response and Survival Among Patients With Advanced Melanoma.
Antoni Ribas, Omid Hamid, +25 authors, Caroline Robert.
JAMA, 2016 Apr 20; 315(15). PMID: 27092830
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Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF.
Sonja J Heidorn, Carla Milagre, +8 authors, Richard Marais.
Cell, 2010 Feb 10; 140(2). PMID: 20141835    Free PMC article.
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Tertiary lymphoid structures improve immunotherapy and survival in melanoma.
Rita Cabrita, Martin Lauss, +22 authors, Göran Jönsson.
Nature, 2020 Jan 17; 577(7791). PMID: 31942071
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Delphine Morales, Florian Lombart, +7 authors, Muriel Vayssade.
Tissue Eng Part A, 2018 Dec 07; 25(15-16). PMID: 30501565
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Richard V Parry, Jens M Chemnitz, +6 authors, James L Riley.
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Jedd D Wolchok, Vanna Chiarion-Sileni, +30 authors, James Larkin.
N Engl J Med, 2017 Sep 12; 377(14). PMID: 28889792    Free PMC article.
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Rajasekharan Somasundaram, Gao Zhang, +50 authors, Stephan N Wagner.
Nat Commun, 2017 Sep 21; 8(1). PMID: 28928360    Free PMC article.
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Rodabe N Amaria, Sangeetha M Reddy, +42 authors, Jennifer A Wargo.
Nat Med, 2018 Oct 10; 24(11). PMID: 30297909    Free PMC article.
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Udupi A Ramagopal, Weifeng Liu, +10 authors, Steven C Almo.
Proc Natl Acad Sci U S A, 2017 May 10; 114(21). PMID: 28484017    Free PMC article.
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Loise M Francisco, Peter T Sage, Arlene H Sharpe.
Immunol Rev, 2010 Jul 20; 236. PMID: 20636820    Free PMC article.
Highly Cited. Review.
Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma.
James Larkin, Vanna Chiarion-Sileni, +28 authors, Jedd D Wolchok.
N Engl J Med, 2015 Jun 02; 373(1). PMID: 26027431    Free PMC article.
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Iwona Lugowska, Pawel Teterycz, Piotr Rutkowski.
Contemp Oncol (Pozn), 2018 Apr 10; 22(1A). PMID: 29628796    Free PMC article.
Encorafenib plus binimetinib versus vemurafenib or encorafenib in patients with BRAF-mutant melanoma (COLUMBUS): a multicentre, open-label, randomised phase 3 trial.
Reinhard Dummer, Paolo A Ascierto, +17 authors, Keith T Flaherty.
Lancet Oncol, 2018 Mar 27; 19(5). PMID: 29573941
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Li Wu, Aleksandar Dakic.
Cell Mol Immunol, 2005 Oct 11; 1(2). PMID: 16212897
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Nature, 2010 Feb 05; 464(7287). PMID: 20130576
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Targeting ERK, an Achilles' Heel of the MAPK pathway, in cancer therapy.
Feifei Liu, Xiaotong Yang, Meiyu Geng, Min Huang.
Acta Pharm Sin B, 2018 Aug 16; 8(4). PMID: 30109180    Free PMC article.
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Dragging ras back in the ring.
Andrew G Stephen, Dominic Esposito, Rachel K Bagni, Frank McCormick.
Cancer Cell, 2014 Mar 22; 25(3). PMID: 24651010
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Inhibitory Receptors and Pathways of Lymphocytes: The Role of PD-1 in Treg Development and Their Involvement in Autoimmunity Onset and Cancer Progression.
Elena Gianchecchi, Alessandra Fierabracci.
Front Immunol, 2018 Nov 06; 9. PMID: 30386337    Free PMC article.
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Prognostic value of tumor-infiltrating FoxP3+ regulatory T cells in cancers: a systematic review and meta-analysis.
Bin Shang, Yao Liu, Shu-juan Jiang, Yi Liu.
Sci Rep, 2015 Oct 16; 5. PMID: 26462617    Free PMC article.
Highly Cited. Systematic Review.
Suppression of BRAF(V599E) in human melanoma abrogates transformation.
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Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma.
Ryosuke Hino, Kenji Kabashima, +5 authors, Yoshiki Tokura.
Cancer, 2010 Feb 10; 116(7). PMID: 20143437
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FOXD3 Regulates VISTA Expression in Melanoma.
Sheera R Rosenbaum, Meghan Knecht, +11 authors, Andrew E Aplin.
Cell Rep, 2020 Jan 16; 30(2). PMID: 31940493    Free PMC article.
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Dabrafenib plus trametinib versus dabrafenib monotherapy in patients with metastatic BRAF V600E/K-mutant melanoma: long-term survival and safety analysis of a phase 3 study.
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Ann Oncol, 2017 May 06; 28(7). PMID: 28475671    Free PMC article.
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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
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Cancer-associated fibroblasts promote M2 polarization of macrophages in pancreatic ductal adenocarcinoma.
Aibin Zhang, Yigang Qian, +5 authors, Shusen Zheng.
Cancer Med, 2017 Jan 18; 6(2). PMID: 28097809    Free PMC article.
Expression of ID4 protein in breast cancer cells induces reprogramming of tumour-associated macrophages.
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Breast Cancer Res, 2018 Jun 21; 20(1). PMID: 29921315    Free PMC article.
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Norio Kubo, Kenichiro Araki, Hiroyuki Kuwano, Ken Shirabe.
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FOXP3+ T regulatory lymphocytes in primary melanoma are associated with BRAF mutation but not with response to BRAF inhibitor.
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Pathology, 2015 Aug 27; 47(6). PMID: 26308130
Melanoma induces immunosuppression by up-regulating FOXP3(+) regulatory T cells.
Joel Baumgartner, Cara Wilson, +3 authors, Martin McCarter.
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BMB Rep, 2017 Sep 01; 50(12). PMID: 28855026    Free PMC article.
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Carmen Alvarez-Dominguez, Ricardo Calderón-Gonzalez, +5 authors, Fernando Rivera.
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Weiyi Peng, Jie Qing Chen, +41 authors, Patrick Hwu.
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KIT as an Oncogenic Driver in Melanoma: An Update on Clinical Development.
Da Meng, Richard D Carvajal.
Am J Clin Dermatol, 2019 Feb 02; 20(3). PMID: 30707374
Glycocalyx-Mimicking Nanoparticles Improve Anti-PD-L1 Cancer Immunotherapy through Reversion of Tumor-Associated Macrophages.
Yufei Zhang, Libin Wu, +4 authors, Guosong Chen.
Biomacromolecules, 2018 Apr 11; 19(6). PMID: 29634251
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Paola Savoia, Paolo Fava, Filippo Casoni, Ottavio Cremona.
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Activation of cancer-associated fibroblasts is required for tumor neovascularization in a murine model of melanoma.
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Matrix Biol, 2018 Jun 10; 74. PMID: 29885461
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N Engl J Med, 2015 Apr 22; 372(26). PMID: 25891173
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Fibronectin induction abrogates the BRAF inhibitor response of BRAF V600E/PTEN-null melanoma cells.
I V Fedorenko, E V Abel, +13 authors, K S M Smalley.
Oncogene, 2015 Jun 16; 35(10). PMID: 26073081    Free PMC article.
MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAF mutations: a non-randomised, open-label phase 2 study.
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Lancet Oncol, 2013 Feb 19; 14(3). PMID: 23414587
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Lindsey Broussard, Amanda Howland, +4 authors, Peter I Song.
Chonnam Med J, 2018 Oct 06; 54(3). PMID: 30288368    Free PMC article.
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Highly Cited. Review.
PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer.
Takahiro Kamada, Yosuke Togashi, +13 authors, Hiroyoshi Nishikawa.
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VISTA expression on tumor-infiltrating inflammatory cells in primary cutaneous melanoma correlates with poor disease-specific survival.
Lawrence F Kuklinski, Shaofeng Yan, +6 authors, Marc S Ernstoff.
Cancer Immunol Immunother, 2018 May 09; 67(7). PMID: 29737375
Dendritic Cell Plasticity in Tumor-Conditioned Skin: CD14(+) Cells at the Cross-Roads of Immune Activation and Suppression.
Rieneke van de Ven, Jelle J Lindenberg, Dinja Oosterhoff, Tanja D de Gruijl.
Front Immunol, 2013 Dec 11; 4. PMID: 24324467    Free PMC article.
Intravital imaging reveals how BRAF inhibition generates drug-tolerant microenvironments with high integrin β1/FAK signaling.
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Preclinical Development of Ipilimumab and Nivolumab Combination Immunotherapy: Mouse Tumor Models, In Vitro Functional Studies, and Cynomolgus Macaque Toxicology.
Mark J Selby, John J Engelhardt, +11 authors, Alan J Korman.
PLoS One, 2016 Sep 10; 11(9). PMID: 27610613    Free PMC article.
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Zhaoduan Liang, Yanyan Li, +8 authors, Yi Li.
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Joel Sunshine, Janis M Taube.
Curr Opin Pharmacol, 2015 Jun 07; 23. PMID: 26047524    Free PMC article.
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Sergei I Grivennikov, Florian R Greten, Michael Karin.
Cell, 2010 Mar 23; 140(6). PMID: 20303878    Free PMC article.
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NFAT1 enhances the effects of tumor-associated macrophages on promoting malignant melanoma growth and metastasis.
Hao Liu, Liping Yang, Min Qi, Jianglin Zhang.
Biosci Rep, 2018 Nov 22; 38(6). PMID: 30459241    Free PMC article.
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Manoela Tiago, Edson Mendes de Oliveira, +7 authors, Silvya Stuchi Maria-Engler.
Tissue Eng Part A, 2014 Feb 20; 20(17-18). PMID: 24548268    Free PMC article.
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Cancer Immunol Immunother, 2015 Jul 24; 64(11). PMID: 26201938
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N Engl J Med, 2014 Sep 30; 371(20). PMID: 25265492
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Long term survival with cytotoxic T lymphocyte-associated antigen 4 blockade using tremelimumab.
Zeynep Eroglu, Dae Won Kim, +9 authors, Antoni Ribas.
Eur J Cancer, 2015 Sep 15; 51(17). PMID: 26364516    Free PMC article.
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Yifan Zhou, Natalie Slone, +6 authors, Stephanie S Watowich.
J Immunother Cancer, 2020 Apr 11; 8(1). PMID: 32273347    Free PMC article.
Non-conventional Inhibitory CD4+Foxp3-PD-1hi T Cells as a Biomarker of Immune Checkpoint Blockade Activity.
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Cancer Cell, 2018 Jun 13; 33(6). PMID: 29894689    Free PMC article.
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Simultaneous blocking of IL-6 and IL-8 is sufficient to fully inhibit CAF-induced human melanoma cell invasiveness.
Njainday Pulo Jobe, Daniel Rösel, +5 authors, Jan Brábek.
Histochem Cell Biol, 2016 Apr 23; 146(2). PMID: 27102177
A Mini-Review for Cancer Immunotherapy: Molecular Understanding of PD-1/PD-L1 Pathway & Translational Blockade of Immune Checkpoints.
Yongshu Li, Fangfei Li, +4 authors, Ge Zhang.
Int J Mol Sci, 2016 Jul 22; 17(7). PMID: 27438833    Free PMC article.
Highly Cited. Review.
GSK1120212 (JTP-74057) is an inhibitor of MEK activity and activation with favorable pharmacokinetic properties for sustained in vivo pathway inhibition.
Aidan G Gilmartin, Maureen R Bleam, +11 authors, Sylvie G Laquerre.
Clin Cancer Res, 2011 Jan 20; 17(5). PMID: 21245089
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αvβ3-integrin regulates PD-L1 expression and is involved in cancer immune evasion.
Andrea Vannini, Valerio Leoni, +5 authors, Tatiana Gianni.
Proc Natl Acad Sci U S A, 2019 Sep 19; 116(40). PMID: 31527243    Free PMC article.
Tumor Necrosis Factor Receptor-1 (p55) Deficiency Attenuates Tumor Growth and Intratumoral Angiogenesis and Stimulates CD8+ T Cell Function in Melanoma.
Yamila I Rodriguez, Ludmila E Campos, +6 authors, Sergio E Alvarez.
Cells, 2020 Nov 19; 9(11). PMID: 33202705    Free PMC article.
MEK inhibitors for the treatment of non-small cell lung cancer.
Jing Han, Yang Liu, +3 authors, Qiming Wang.
J Hematol Oncol, 2021 Jan 07; 14(1). PMID: 33402199    Free PMC article.
SEMAPHORINS and their receptors: focus on the crosstalk between melanoma and hypoxia.
Elisabetta Valentini, Marta Di Martile, Donatella Del Bufalo, Simona D'Aguanno.
J Exp Clin Cancer Res, 2021 Apr 17; 40(1). PMID: 33858502    Free PMC article.
Precision Medicine and Melanoma: Multi-Omics Approaches to Monitoring the Immunotherapy Response.
Fabio Valenti, Italia Falcone, +9 authors, Antonino Guerrisi.
Int J Mol Sci, 2021 May 01; 22(8). PMID: 33917181    Free PMC article.
Prognostic Role of Plasma PD-1, PD-L1, pan-BTN3As and BTN3A1 in Patients Affected by Metastatic Gastrointestinal Stromal Tumors: Can Immune Checkpoints Act as a Sentinel for Short-Term Survival?
Daniele Fanale, Lorena Incorvaia, +8 authors, Viviana Bazan.
Cancers (Basel), 2021 May 01; 13(9). PMID: 33925671    Free PMC article.
Cutaneous Melanoma Classification: The Importance of High-Throughput Genomic Technologies.
Cristian Scatena, Daniela Murtas, Sara Tomei.
Front Oncol, 2021 Jun 15; 11. PMID: 34123788    Free PMC article.
Integrated Analysis of the Transcriptome Profile Reveals the Potential Roles Played by Long Noncoding RNAs in Immunotherapy for Sarcoma.
Boran Pang, Yongqiang Hao.
Front Oncol, 2021 Jun 29; 11. PMID: 34178688    Free PMC article.
Progression of melanoma is suppressed by targeting all transforming growth factor‑β isoforms with an Fc chimeric receptor.
Shingo Kodama, Katarzyna Α Podyma-Inoue, +8 authors, Tetsuro Watabe.
Oncol Rep, 2021 Jul 24; 46(3). PMID: 34296292    Free PMC article.
Gelsolin Contributes to the Motility of A375 Melanoma Cells and This Activity Is Mediated by the Fibrous Extracellular Matrix Protein Profile.
Ewa Mazurkiewicz, Aleksandra Makowiecka, +3 authors, Antonina Joanna Mazur.
Cells, 2021 Aug 28; 10(8). PMID: 34440617    Free PMC article.
Interrogating Epigenome toward Personalized Approach in Cutaneous Melanoma.
Elena-Georgiana Dobre, Carolina Constantin, Marieta Costache, Monica Neagu.
J Pers Med, 2021 Sep 29; 11(9). PMID: 34575678    Free PMC article.
Prognostic Value of Interleukin-32 Expression and Its Correlation with the Infiltration of Natural Killer Cells in Cutaneous Melanoma.
Ji Young Kang, Kyung Eun Kim.
J Clin Med, 2021 Oct 24; 10(20). PMID: 34682815    Free PMC article.
Predictive Value of Baseline [18F]FDG PET/CT for Response to Systemic Therapy in Patients with Advanced Melanoma.
Virginia Liberini, Marco Rubatto, +11 authors, Désirée Deandreis.
J Clin Med, 2021 Nov 14; 10(21). PMID: 34768517    Free PMC article.
The Challenging Melanoma Landscape: From Early Drug Discovery to Clinical Approval.
Mariana Matias, Jacinta O Pinho, +3 authors, Maria Manuela Gaspar.
Cells, 2021 Nov 28; 10(11). PMID: 34831311    Free PMC article.
Magnetic nanoparticles in theranostics of malignant melanoma.
Maxim Shevtsov, Susanne Kaesler, +2 authors, Tilo Biedermann.
EJNMMI Res, 2021 Dec 15; 11(1). PMID: 34905138    Free PMC article.
Genomic and Transcriptomic Underpinnings of Melanoma Genesis, Progression, and Metastasis.
Olga S Cherepakhin, Zsolt B Argenyi, Ata S Moshiri.
Cancers (Basel), 2022 Jan 12; 14(1). PMID: 35008286    Free PMC article.
Editorial on Special Issue "Advances and Novel Treatment Options in Metastatic Melanoma".
Alessandra Carè, Donatella Del Bufalo, Antonio Facchiano.
Cancers (Basel), 2022 Feb 16; 14(3). PMID: 35158974    Free PMC article.
Exosomes produced by melanoma cells significantly influence the biological properties of normal and cancer-associated fibroblasts.
Karolína Strnadová, Lucie Pfeiferová, +13 authors, Lukáš Lacina.
Histochem Cell Biol, 2021 Nov 28; 157(2). PMID: 34837514    Free PMC article.
Extracellular Vesicles Derived from Acidified Metastatic Melanoma Cells Stimulate Growth, Migration, and Stemness of Normal Keratinocytes.
Maxim L Bychkov, Artem V Kirichenko, +5 authors, Ekaterina N Lyukmanova.
Biomedicines, 2022 Mar 26; 10(3). PMID: 35327461    Free PMC article.
Nobiletin Induces Ferroptosis in Human Skin Melanoma Cells Through the GSK3β-Mediated Keap1/Nrf2/HO-1 Signalling Pathway.
Senling Feng, Yongheng Zhou, +8 authors, Baoying Liang.
Front Genet, 2022 Mar 31; 13. PMID: 35350242    Free PMC article.