Review
. 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 
Affiliations
  • PMID: 33036192
  •     180 References
  •     19 citations

Abstract

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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Binimetinib versus dacarbazine in patients with advanced NRAS-mutant melanoma (NEMO): a multicentre, open-label, randomised, phase 3 trial.
Reinhard Dummer, Dirk Schadendorf, +21 authors, Keith Flaherty.
Lancet Oncol, 2017 Mar 13; 18(4). PMID: 28284557
Highly Cited.
RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF.
Poulikos I Poulikakos, Chao Zhang, +2 authors, Neal Rosen.
Nature, 2010 Feb 25; 464(7287). PMID: 20179705    Free PMC article.
Highly Cited.
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
Highly Cited.
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.
Highly Cited. Review.
An introduction to immunology and immunopathology.
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.
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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.
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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
Highly Cited.
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.
Highly Cited.
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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3D Coculture Models Underline Metastatic Melanoma Cell Sensitivity to Vemurafenib.
Delphine Morales, Florian Lombart, +7 authors, Muriel Vayssade.
Tissue Eng Part A, 2018 Dec 07; 25(15-16). PMID: 30501565
CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms.
Richard V Parry, Jens M Chemnitz, +6 authors, James L Riley.
Mol Cell Biol, 2005 Oct 18; 25(21). PMID: 16227604    Free PMC article.
Highly Cited.
Overall Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma.
Jedd D Wolchok, Vanna Chiarion-Sileni, +30 authors, James Larkin.
N Engl J Med, 2017 Sep 12; 377(14). PMID: 28889792    Free PMC article.
Highly Cited.
Tumor-associated B-cells induce tumor heterogeneity and therapy resistance.
Rajasekharan Somasundaram, Gao Zhang, +50 authors, Stephan N Wagner.
Nat Commun, 2017 Sep 21; 8(1). PMID: 28928360    Free PMC article.
Neoadjuvant immune checkpoint blockade in high-risk resectable melanoma.
Rodabe N Amaria, Sangeetha M Reddy, +42 authors, Jennifer A Wargo.
Nat Med, 2018 Oct 10; 24(11). PMID: 30297909    Free PMC article.
Highly Cited.
Structural basis for cancer immunotherapy by the first-in-class checkpoint inhibitor ipilimumab.
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.
The PD-1 pathway in tolerance and autoimmunity.
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.
Highly Cited.
Immunotherapy of melanoma.
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
Highly Cited.
Development of dendritic cell system.
Li Wu, Aleksandar Dakic.
Cell Mol Immunol, 2005 Oct 11; 1(2). PMID: 16212897
Review.
RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth.
Georgia Hatzivassiliou, Kyung Song, +18 authors, Shiva Malek.
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.
Highly Cited. Review.
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
Highly Cited. Review.
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.
Highly Cited. Review.
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.
Sunil R Hingorani, Michael A Jacobetz, +2 authors, David A Tuveson.
Cancer Res, 2003 Sep 23; 63(17). PMID: 14500344
Highly Cited.
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.
The immune microenvironment confers resistance to MAPK pathway inhibitors through macrophage-derived TNFα.
Michael P Smith, Berta Sanchez-Laorden, +10 authors, Claudia Wellbrock.
Cancer Discov, 2014 Sep 27; 4(10). PMID: 25256614    Free PMC article.
Highly Cited.
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.
G V Long, K T Flaherty, +28 authors, J-J Grob.
Ann Oncol, 2017 May 06; 28(7). PMID: 28475671    Free PMC article.
Highly Cited.
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.
Sara Donzelli, Elisa Milano, +12 authors, Giulia Fontemaggi.
Breast Cancer Res, 2018 Jun 21; 20(1). PMID: 29921315    Free PMC article.
Cancer-associated fibroblasts in hepatocellular carcinoma.
Norio Kubo, Kenichiro Araki, Hiroyuki Kuwano, Ken Shirabe.
World J Gastroenterol, 2016 Aug 30; 22(30). PMID: 27570421    Free PMC article.
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FOXP3+ T regulatory lymphocytes in primary melanoma are associated with BRAF mutation but not with response to BRAF inhibitor.
Connull Leslie, Samantha E Bowyer, +5 authors, Michael Millward.
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.
J Surg Res, 2007 Jun 19; 141(1). PMID: 17574040    Free PMC article.
Fibronectin expression is upregulated by PI-3K/Akt activation in tamoxifen-resistant breast cancer cells.
Daeun You, Seung Pil Jung, +3 authors, Sangmin Kim.
BMB Rep, 2017 Sep 01; 50(12). PMID: 28855026    Free PMC article.
Dendritic cell therapy in melanoma.
Carmen Alvarez-Dominguez, Ricardo Calderón-Gonzalez, +5 authors, Fernando Rivera.
Ann Transl Med, 2017 Nov 09; 5(19). PMID: 29114544    Free PMC article.
Review.
Loss of PTEN Promotes Resistance to T Cell-Mediated Immunotherapy.
Weiyi Peng, Jie Qing Chen, +41 authors, Patrick Hwu.
Cancer Discov, 2015 Dec 10; 6(2). PMID: 26645196    Free PMC article.
Highly Cited.
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
Review.
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
Targeting the ERK Signaling Pathway in Melanoma.
Paola Savoia, Paolo Fava, Filippo Casoni, Ottavio Cremona.
Int J Mol Sci, 2019 Apr 03; 20(6). PMID: 30934534    Free PMC article.
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The blockade of immune checkpoints in cancer immunotherapy.
Drew M Pardoll.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437870    Free PMC article.
Highly Cited. Review.
Activation of cancer-associated fibroblasts is required for tumor neovascularization in a murine model of melanoma.
James Hutchenreuther, Krista Vincent, +9 authors, Andrew Leask.
Matrix Biol, 2018 Jun 10; 74. PMID: 29885461
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I Cornil, D Theodorescu, +3 authors, R S Kerbel.
Proc Natl Acad Sci U S A, 1991 Jul 15; 88(14). PMID: 2068080    Free PMC article.
Pembrolizumab versus Ipilimumab in Advanced Melanoma.
Caroline Robert, Jacob Schachter, +20 authors, KEYNOTE-006 investigators.
N Engl J Med, 2015 Apr 22; 372(26). PMID: 25891173
Highly Cited.
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.
Paolo A Ascierto, Dirk Schadendorf, +12 authors, Reinhard Dummer.
Lancet Oncol, 2013 Feb 19; 14(3). PMID: 23414587
Highly Cited.
Melanoma Cell Death Mechanisms.
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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Immunotherapy in melanoma: Recent advances and future directions.
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Eur J Surg Oncol, 2016 Oct 23; 43(3). PMID: 27769635
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.
Proc Natl Acad Sci U S A, 2019 Apr 28; 116(20). PMID: 31028147    Free PMC article.
Highly Cited.
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.
Review.
Intravital imaging reveals how BRAF inhibition generates drug-tolerant microenvironments with high integrin β1/FAK signaling.
Eishu Hirata, Maria Romina Girotti, +6 authors, Erik Sahai.
Cancer Cell, 2015 Apr 16; 27(4). PMID: 25873177    Free PMC article.
Highly Cited.
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.
Highly Cited.
High-affinity human programmed death-1 ligand-1 variant promotes redirected T cells to kill tumor cells.
Zhaoduan Liang, Yanyan Li, +8 authors, Yi Li.
Cancer Lett, 2019 Jan 25; 447. PMID: 30677447
Tumor microenvironment and therapeutic response.
Ting Wu, Yun Dai.
Cancer Lett, 2016 Feb 05; 387. PMID: 26845449
Highly Cited. Review.
PD-1/PD-L1 inhibitors.
Joel Sunshine, Janis M Taube.
Curr Opin Pharmacol, 2015 Jun 07; 23. PMID: 26047524    Free PMC article.
Highly Cited. Review.
Immunity, inflammation, and cancer.
Sergei I Grivennikov, Florian R Greten, Michael Karin.
Cell, 2010 Mar 23; 140(6). PMID: 20303878    Free PMC article.
Highly Cited. Review.
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.
Fibroblasts protect melanoma cells from the cytotoxic effects of doxorubicin.
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.
Constitutively active GSK3β as a means to bolster dendritic cell functionality in the face of tumour-mediated immune suppression.
Marta López González, Dinja Oosterhoff, +17 authors, Tanja D De Gruijl.
Oncoimmunology, 2019 Oct 28; 8(10). PMID: 31646076    Free PMC article.
Immunosuppressive activity of cancer-associated fibroblasts in head and neck squamous cell carcinoma.
Hideyuki Takahashi, Koichi Sakakura, +4 authors, Kazuaki Chikamatsu.
Cancer Immunol Immunother, 2015 Jul 24; 64(11). PMID: 26201938
MEK inhibitors for the treatment of NRAS mutant melanoma.
Saro Sarkisian, Diwakar Davar.
Drug Des Devel Ther, 2018 Aug 30; 12. PMID: 30154648    Free PMC article.
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Despina Handolias, Renato Salemi, +6 authors, Grant A McArthur.
Pigment Cell Melanoma Res, 2010 Jan 22; 23(2). PMID: 20088873
BRAF Inhibition Stimulates Melanoma-Associated Macrophages to Drive Tumor Growth.
Tao Wang, Min Xiao, +19 authors, Russel E Kaufman.
Clin Cancer Res, 2015 Jan 27; 21(7). PMID: 25617424    Free PMC article.
Combined BRAF and MEK inhibition versus BRAF inhibition alone in melanoma.
Georgina V Long, Daniil Stroyakovskiy, +32 authors, Keith Flaherty.
N Engl J Med, 2014 Sep 30; 371(20). PMID: 25265492
Highly Cited.
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.
Vaccine efficacy against primary and metastatic cancer with in vitro-generated CD103+ conventional dendritic cells.
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.
Roberta Zappasodi, Sadna Budhu, +13 authors, Jedd D Wolchok.
Cancer Cell, 2018 Jun 13; 33(6). PMID: 29894689    Free PMC article.
Highly Cited.
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
Highly Cited.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.