Recent advances in tyrosine kinase inhibitors VEGFR 1-3 for the treatment of advanced metastatic melanoma

References

• Salven P, Heikkilä P, Joensuu H. Enhanced expression of vascular endothelial growth factor in metastatic melanoma. Br J Cancer. 1997;76(7):930–934. doi: 10.1038/bjc.1997.486
   PubMed Web of Science ®Google Scholar
• Demirkesen C, Büyükpinarbaşili N, Ramazanoğlu R, et al. The correlation of angiogenesis with metastasis in primary cutaneous melanoma: a comparative analysis of microvessel density, expression of vascular endothelial growth factor and basic fibroblastic growth factor. Pathology. 2006 Apr;38(2):132–137.
   PubMed Web of Science ®Google Scholar
• Ugurel S, Rappl G, Tilgen W, et al. Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol. 2001 Jan 15;19(2):577–583. doi: 10.1200/JCO.2001.19.2.577
   PubMed Web of Science ®Google Scholar
• Graells J, Vinyals A, Figueras A, et al. Overproduction of VEGF concomitantly expressed with its receptors promotes growth and survival of melanoma cells through MAPK and PI3K signaling. J Invest Dermatol. 2004 Dec;123(6):1151–1161.
   PubMed Web of Science ®Google Scholar
• Oku T, Tjuvajev JG, Miyagawa T, et al. Tumor growth modulation by sense and antisense vascular endothelial growth factor gene expression: effects on angiogenesis, vascular permeability, blood volume, blood flow, fluorodeoxyglucose uptake, and proliferation of human melanoma intracerebral xenografts. Cancer Res. 1998 Sep 15;58(18):4185–4192.
   PubMed Web of Science ®Google Scholar
• Karkkainen MJ, Petrova TV. Vascular endothelial growth factor receptors in the regulation of angiogenesis and lymphangiogenesis. Oncogene. 2000 Nov 20;19(49):5598–5605. doi: 10.1038/sj.onc.1203855
   PubMed Web of Science ®Google Scholar
• Zhu JW, Ni YJ, Tong XY, et al. Activation of VEGF receptors in response to UVB promotes cell proliferation and melanogenesis of normal human melanocytes. Exp Cell Res. 2020 Feb 15;387(2):111798. doi: 10.1016/j.yexcr.2019.111798
   PubMed Web of Science ®Google Scholar
• Rajabi P, Neshat A, Mokhtari M, et al. The role of VEGF in melanoma progression. J Res Med Sci. 2012 Jun;17(6):534–539.
   PubMed Web of Science ®Google Scholar
• Ni C-s, Sun B-C, Dong X-Y, et al. Promoting melanoma growth and metastasis by enhancing VEGF expression [journal article]. Contemporary Oncology/Współczesna Onkologia. 2012;6(6):526–531. doi: 10.5114/wo.2012.32486
   Google Scholar
• Soubrane C, Mouawad R, Rixe O, et al. Soluble VEGF and its receptors (1 and 2) in metastatic malignant melanoma patients: relationship with survival. J Clin Oncol. 2005;23(16_suppl):7541–. doi: 10.1200/jco.2005.23.16_suppl.7541
   Web of Science ®Google Scholar
• Lacal PM, Atzori MG, Ruffini F, et al. Targeting the vascular endothelial growth factor receptor-1 by the monoclonal antibody D16F7 to increase the activity of immune checkpoint inhibitors against cutaneous melanoma. Pharmacol Res. 2020 Sep;159:104957. doi: 10.1016/j.phrs.2020.104957
   PubMed Web of Science ®Google Scholar
• Atzori MG, Ceci C, Ruffini F, et al. Role of VEGFR-1 in melanoma acquired resistance to the BRAF inhibitor vemurafenib. J Cell Mol Med. 2020 Jan;24(1):465–475.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med. 2007 Jan 11;356(2):115–124. doi: 10.1056/NEJMoa065044
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Hessel C, Halabi S, et al. Cabozantinib versus sunitinib as initial therapy for metastatic renal cell carcinoma of intermediate or poor risk (Alliance A031203 CABOSUN randomised trial): progression-free survival by independent review and overall survival update. Eur J Cancer. 2018 May;94:115–125. doi: 10.1016/j.ejca.2018.02.012
   PubMed Web of Science ®Google Scholar
• Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008 Jul 24;359(4):378–390. doi: 10.1056/NEJMoa0708857
   PubMed Web of Science ®Google Scholar
• Hauschild A, Agarwala SS, Trefzer U, et al. Results of a phase III, randomized, placebo-controlled study of sorafenib in combination with carboplatin and paclitaxel as second-line treatment in patients with unresectable stage III or stage IV melanoma. J Clin Oncol. 2009 Jun 10;27(17):2823–2830. doi: 10.1200/JCO.2007.15.7636
   PubMed Web of Science ®Google Scholar
• Fruehauf J, Lutzky J, McDermott D, et al. Multicenter, phase II study of axitinib, a selective second-generation inhibitor of vascular endothelial growth factor receptors 1, 2, and 3, in patients with metastatic melanoma. Clin Cancer Res. 2011 Dec 1;17(23):7462–7469. doi: 10.1158/1078-0432.CCR-11-0534
   PubMed Web of Science ®Google Scholar
• Huinen ZR, Huijbers EJM, van Beijnum JR, et al. Anti-angiogenic agents - overcoming tumour endothelial cell anergy and improving immunotherapy outcomes. Nat Rev Clin Oncol. 2021 Aug;18(8):527–540.
   PubMed Web of Science ®Google Scholar
• van Not OJ, de Meza MM, van den Eertwegh AJM, et al. Response to immune checkpoint inhibitors in acral melanoma: a nationwide cohort study. Eur J Cancer. 2022 May;167:70–80. doi: 10.1016/j.ejca.2022.02.026
   PubMed Web of Science ®Google Scholar
• Bhave P, Ahmed T, Lo SN, et al. Efficacy of anti-PD-1 and ipilimumab alone or in combination in acral melanoma. J Immunother Cancer. 2022 Jul;10(7):e004668.
   PubMed Web of Science ®Google Scholar
• Li H, Kuang X, Liang L, et al. The beneficial role of sunitinib in tumor immune surveillance by regulating tumor PD-L1. Adv Sci. 2021;8(2):2001596. doi: 10.1002/advs.202001596
   Web of Science ®Google Scholar
• Sutent FDA approval history [cited 2024 Mar 31]. Available from: https://www.drugs.com/history/sutent.html
   Google Scholar
• Wishart DS, Knox C, Guo AC, et al. Drugbank: a comprehensive resource for in silico drug discovery and exploration. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D668–72. 16381955. [cited 2024 Mar 31]. Available from: https://go.drugbank.com/drugs/DB01268
   PubMed Web of Science ®Google Scholar
• Wu RY, Kong PF, Xia LP, et al. Regorafenib promotes antitumor immunity via inhibiting PD-L1 and IDO1 expression in melanoma. Clin Cancer Res. 2019 Jul 15;25(14):4530–4541. doi: 10.1158/1078-0432.CCR-18-2840
   PubMed Web of Science ®Google Scholar
• Tran TT, Caulfield J, Zhang L, et al. Lenvatinib or anti-VEGF in combination with anti-PD-1 differentially augments antitumor activity in melanoma. JCI Insight. 2023 Apr 10;8(7). doi: 10.1172/jci.insight.157347
   Web of Science ®Google Scholar
• Gungabeesoon J, Gort-Freitas NA, Kiss M, et al. A neutrophil response linked to tumor control in immunotherapy. Cell. 2023 Mar 30;186(7):1448–64.e20. doi: 10.1016/j.cell.2023.02.032
   PubMed Web of Science ®Google Scholar
• Taylor MH, Lee CH, Makker V, et al. Phase IB/II trial of lenvatinib plus pembrolizumab in patients with advanced renal cell carcinoma, endometrial cancer, and other selected advanced solid tumors. J Clin Oncol. 2020 Apr 10;38(11):1154–1163. doi: 10.1200/JCO.19.01598
   PubMed Web of Science ®Google Scholar
• Arance A, de la Cruz-Merino L, Petrella TM, et al. Phase II LEAP-004 study of lenvatinib plus pembrolizumab for melanoma with confirmed progression on a programmed cell death protein-1 or programmed death ligand 1 inhibitor given as monotherapy or in combination. J Clin Oncol. 2023 Jan 1;41(1):75–85. doi: 10.1200/JCO.22.00221
   PubMed Web of Science ®Google Scholar
• Merck and eisai provide update on phase 3 trials of KEYTRUDA® (pembrolizumab) plus LENVIMA® (lenvatinib) in certain patients with advanced melanoma (LEAP-003) and metastatic colorectal cancer (LEAP-017) MERCK. [cited 2023 Dec 11]. Available from: https://www.merck.com/news/merck-and-eisai-provide-update-on-phase-3-trials-of-keytruda-pembrolizumab-plus-lenvima-lenvatinib-in-certain-patients-with-advanced-melanoma-leap-003-and-metastatic-colorectal-cance/
   Google Scholar
• Stoff R, Asher N, Laks S, et al. Real world evidence of Lenvatinib + anti PD-1 as an advanced line for metastatic melanoma. Front Oncol. 2023;13:1180988. doi: 10.3389/fonc.2023.1180988
   PubMed Web of Science ®Google Scholar
• Stewart J, Cabometyx FDA approval history. 2021 [cited 2024 Mar 31]. Available from: https://www.drugs.com/history/cabometyx.html
   Google Scholar
• Gibney GT, Pecora AL, Rapisuwon S, et al. Interim analysis of a phase II study of nivolumab/ipilimumab plus cabozantinib in patients with unresectable advanced melanoma. J Clin Oncol. 2023;41(16_suppl):9563–. doi: 10.1200/JCO.2023.41.16_suppl.9563
   Google Scholar
• Inlyta FDA approval history. [cited 2024 Mar 31]. Available from: https://www.drugs.com/history/inlyta.html
   Google Scholar
• Algazi AP, Cha E, Ortiz-Urda SM, et al. The combination of axitinib followed by paclitaxel/carboplatin yields extended survival in advanced BRAF wild-type melanoma: results of a clinical/correlative prospective phase II clinical trial. Br J Cancer. 2015 Apr 14;112(8):1326–1331. doi: 10.1038/bjc.2014.541
   PubMed Web of Science ®Google Scholar
• Block MS, Suman VJ, Nevala WK, et al. A phase I trial of nab-paclitaxel/bevacizumab (AB160) nano-immunoconjugate therapy for unresectable stage IV malignant melanoma (MM): MC1371 (NCT02020707). J Clin Oncol. 2020;38(15_suppl):e22020–e. doi: 10.1200/JCO.2020.38.15_suppl.e22020
   Web of Science ®Google Scholar
• Takeda T, Tsubaki M, Kato N, et al. Sorafenib treatment of metastatic melanoma with c-Kit aberration reduces tumor growth and promotes survival. Oncol Lett. 2021 Dec;22(6):827.
   PubMed Web of Science ®Google Scholar
• Kim KH, Jung M, Lee HJ, et al. A phase II study on the efficacy of regorafenib in treating patients with c-KIT-mutated metastatic malignant melanoma that progressed after previous treatment (KCSG-UN-14-13). Eur J Cancer. 2023 Nov;193:113312. doi: 10.1016/j.ejca.2023.113312
   PubMed Web of Science ®Google Scholar
• Hayward NK, Wilmott JS, Waddell N, et al. Whole-genome landscapes of major melanoma subtypes. Nature. 2017 May 11;545(7653):175–180. doi: 10.1038/nature22071
   PubMed Web of Science ®Google Scholar
• Newell F, Johansson PA, Wilmott JS, et al. Comparative genomics provides etiologic and biological insight into melanoma subtypes. Cancer Discov. 2022 Dec 2;12(12):2856–2879. doi: 10.1158/2159-8290.CD-22-0603
   PubMed Web of Science ®Google Scholar
• Fujisawa Y, Yoshikawa S, Minagawa A, et al. Clinical and histopathological characteristics and survival analysis of 4594 Japanese patients with melanoma. Cancer Med. 2019 May;8(5):2146–2156.
   PubMed Web of Science ®Google Scholar
• Wang X, Wu X, Yang Y, et al. Apatinib combined with camrelizumab in advanced acral melanoma patients: an open-label, single-arm phase 2 trial. Eur J Cancer. 2023 Mar;182:57–65. doi: 10.1016/j.ejca.2022.12.027
   PubMed Web of Science ®Google Scholar
• Zhou L, Yang Y, Si L, et al. Phase II study of apatinib combined with temozolomide in patients with advanced melanoma after failure of immunotherapy. Melanoma Res. 2022 Jun 1;32(3):142–149. doi: 10.1097/CMR.0000000000000809
   PubMed Web of Science ®Google Scholar
• Mao L, Lian B, Li C, et al. Camrelizumab plus apatinib and temozolomide as first-line treatment in patients with advanced acral melanoma: the CAP 03 phase 2 nonrandomized clinical trial. JAMA Oncol. 2023 Aug 1;9(8):1099–1107. doi: 10.1001/jamaoncol.2023.1363
   PubMed Web of Science ®Google Scholar
• Furney SJ, Turajlic S, Stamp G, et al. Genome sequencing of mucosal melanomas reveals that they are driven by distinct mechanisms from cutaneous melanoma. J Pathol. 2013 Jul;230(3):261–269.
   PubMed Web of Science ®Google Scholar
• Curtin JA, Busam K, Pinkel D, et al. Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol. 2006 Sep 10;24(26):4340–4346. doi: 10.1200/JCO.2006.06.2984
   PubMed Web of Science ®Google Scholar
• Kim HS, Jung M, Kang HN, et al. Oncogenic BRAF fusions in mucosal melanomas activate the MAPK pathway and are sensitive to MEK/PI3K inhibition or MEK/CDK4/6 inhibition. Oncogene. 2017 Jun 8;36(23):3334–3345. doi: 10.1038/onc.2016.486
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015 Jan 22;372(4):320–330. doi: 10.1056/NEJMoa1412082
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015 Jul 2;373(1):23–34. doi: 10.1056/NEJMoa1504030
   PubMed Web of Science ®Google Scholar
• Robert C, Schachter J, Long GV, et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med. 2015 Jun 25;372(26):2521–2532. doi: 10.1056/NEJMoa1503093
   PubMed Web of Science ®Google Scholar
• Stewart J, Avastin FDA approval history. 2021 [cited 2023 Nov 26]. Available from: https://www.drugs.com/history/avastin.html
   Google Scholar
• Yan X, Sheng X, Chi Z, et al. Randomized phase ii study of bevacizumab in combination with carboplatin plus paclitaxel in patients with previously untreated advanced mucosal melanoma. J Clin Oncol. 2021 Mar 10;39(8):881–889. doi: 10.1200/JCO.20.00902
   PubMed Web of Science ®Google Scholar
• Mao L, Fang M, Chen Y, et al. Atezolizumab plus bevacizumab in patients with unresectable or metastatic mucosal melanoma: a multicenter, open-label, single-arm phase ii study. Clin Cancer Res. 2022 Nov 1;28(21):4642–4648. doi: 10.1158/1078-0432.CCR-22-1528
   PubMed Web of Science ®Google Scholar
• Li S, Wu X, Yan X, et al. Toripalimab plus axitinib in patients with metastatic mucosal melanoma: 3-year survival update and biomarker analysis. J Immunother Cancer. 2022 Feb;10(2):e004036.
   PubMed Web of Science ®Google Scholar
• Cui C, Lian B, Sheng X, et al. Toripalimab plus axitinib versus toripalimab or axitinib alone in patients with treatment-naive unresectable or metastatic mucosal melanoma: Interim results from a randomized, controlled, phase II trial. J Clin Oncol. 2022;40(16_suppl):9512–. doi: 10.1200/JCO.2022.40.16_suppl.9512.
   Google Scholar
• Tang B, Mo J, Yan X, et al. Real-world efficacy and safety of axitinib in combination with anti-programmed cell death-1 antibody for advanced mucosal melanoma. Eur J Cancer. 2021 Oct;156:83–92. doi: 10.1016/j.ejca.2021.07.018
   PubMed Web of Science ®Google Scholar
• Lian B, Li Z, Wu N, et al. Phase II clinical trial of neoadjuvant anti-PD-1 (Toripalimab) combined with axitinib in resectable mucosal melanoma. Ann Oncol. 2023 Nov 11;35(2):211–220. doi: 10.1016/j.annonc.2023.10.793
   PubMed Web of Science ®Google Scholar
• Bai X, Li M, Chen Y, et al. Updated safety and efficacy results from the phase I study of either LBL-007 (an anti-LAG-3 antibody) in combination with toripalimab (an anti-PD-1 antibody) or LBL-007 in combination with toripalimab and axitinib in patients with advanced melanoma. J Clin Oncol. 2023;41(16_suppl):9541–. doi: 10.1200/JCO.2023.41.16_suppl.9541
   Web of Science ®Google Scholar
• Luke JJ, Olson DJ, Allred JB, et al. Randomized phase ii trial and tumor mutational spectrum analysis from cabozantinib versus chemotherapy in metastatic uveal melanoma (Alliance A091201). Clin Cancer Res. 2020 Feb 15;26(4):804–811. doi: 10.1158/1078-0432.CCR-19-1223
   PubMed Web of Science ®Google Scholar
• Daud A, Kluger HM, Kurzrock R, et al. Phase II randomised discontinuation trial of the MET/VEGF receptor inhibitor cabozantinib in metastatic melanoma. Br J Cancer. 2017 Feb 14;116(4):432–440. doi: 10.1038/bjc.2016.419
   PubMed Web of Science ®Google Scholar
• Rodrigues M, Saint-Ghislain M, Ramtohul T, et al. PLUME: a single-arm phase II trial evaluating the combination of pembrolizumab and lenvatinib in metastatic uveal melanoma (mUM) patients (pts) previously treated or not with tebentafusp. J Clin Oncol. 2023;41(16_suppl):TPS9613–TPS. doi: 10.1200/JCO.2023.41.16_suppl.TPS9613
   Web of Science ®Google Scholar
• Mannsåker TA, Hoang T, Aasen SN, et al. Cabozantinib is effective in melanoma brain metastasis cell lines and affects key signaling pathways. Int J Mol Sci. 2021 Nov 14;22(22):12296. doi: 10.3390/ijms222212296
   PubMed Web of Science ®Google Scholar
• Burton E, Honaker V, Milton D, et al. 1085O Atezolizumab, bevacizumab, and cobimetinib (TACo) in patients (pts) with PD1 refractory melanoma brain metastases (MBM). Ann Oncol. 2023;34:S652–S3. doi: 10.1016/j.annonc.2023.09.2219
   Google Scholar
• Stivarga FDA approval history. [cited 2024 Mar 31]. Available from: https://www.drugs.com/history/stivarga.html
   Google Scholar
• Dirven I, Vander Mijnsbrugge AS, Tijtgat J, et al. 1136P regorafenib combined with BRAF-/MEK-inhibitors for the treatment of refractory melanoma brain metastases. Ann Oncol. 2023;34:S681. doi: 10.1016/j.annonc.2023.09.2270
   PubMed Web of Science ®Google Scholar
• Dirven I, Mijnsbrugge A-S, Vounckx M, et al. Combination of regorafenib with BRAF-/MEK-inhibitors for the treatment of patients with refractory melanoma brain metastases. J Clin Oncol. 2023;41(16_suppl):e14003–e. doi: 10.1200/JCO.2023.41.16_suppl.e14003
   Web of Science ®Google Scholar
• Bowyer S, Prithviraj P, Lorigan P, et al. Efficacy and toxicity of treatment with the anti-CTLA-4 antibody ipilimumab in patients with metastatic melanoma after prior anti-PD-1 therapy. Br J Cancer. 2016 May 10;114(10):1084–1089. doi: 10.1038/bjc.2016.107
   PubMed Web of Science ®Google Scholar
• Zimmer L, Apuri S, Eroglu Z, et al. Ipilimumab alone or in combination with nivolumab after progression on anti-PD-1 therapy in advanced melanoma. Eur J Cancer. 2017 Apr;75:47–55. doi: 10.1016/j.ejca.2017.01.009
   PubMed Web of Science ®Google Scholar
• Cybulska-Stopa B, Rogala P, Czarnecka AM, et al. Efficacy of ipilimumab after anti-PD-1 therapy in sequential treatment of metastatic melanoma patients - real world evidence. Adv Med Sci. 2020 Sep;65(2):316–323.
   PubMed Web of Science ®Google Scholar
• Vanderwalde AM, Moon J, Kendra K, et al. Abstract CT013: S1616: Ipilimumab plus nivolumab versus ipilimumab alone in patients with metastatic or unresectable melanoma that did not respond to anti-PD-1 therapy. Cancer Res. 2022;82(12_Supplement):CT013–CT. doi: 10.1158/1538-7445.AM2022-CT013
   Web of Science ®Google Scholar
• Silva IPD, Ahmed T, Lo S, et al. Ipilimumab (IPI) alone or in combination with anti-PD-1 (IPI+PD1) in patients (pts) with metastatic melanoma (MM) resistant to PD1 monotherapy. J Clin Oncol. 2020;38(15_suppl):10005–. doi: 10.1200/JCO.2020.38.15_suppl.10005
   Web of Science ®Google Scholar
• Pires da Silva I, Ahmed T, Reijers ILM, et al. Ipilimumab alone or ipilimumab plus anti-PD-1 therapy in patients with metastatic melanoma resistant to anti-PD-(L)1 monotherapy: a multicentre, retrospective, cohort study. The Lancet Oncology. 2021 Jun;22(6):836–847.
   PubMedGoogle Scholar
• Zeng F, Li Y, Meng Y. et al. BET inhibitors synergize with sunitinib in melanoma through GDF15 suppression. Exp Mol Med. 2023 Feb;55(2):364–376.
   PubMed Web of Science ®Google Scholar
• Shorstova T, Foulkes WD, Witcher M. Achieving clinical success with BET inhibitors as anti-cancer agents. Br J Cancer. 2021 Apr;124(9):1478–1490. doi: 10.1038/s41416-021-01321-0
   PubMed Web of Science ®Google Scholar
• Cotto-Rios XM, Agianian B, Gitego N, et al. Inhibitors of BRAF dimers using an allosteric site. Nat Commun. 2020 Sep 01;11(1):4370. doi: 10.1038/s41467-020-18123-2
   PubMed Web of Science ®Google Scholar
• Barnwal A, Das S, Bhattacharyya J. Repurposing ponatinib as a PD-L1 inhibitor revealed by drug repurposing screening and validation by in vitro and in vivo experiments. ACS Pharmacol Transl Sci. 2023 Feb 10;6(2):281–289.
   PubMedGoogle Scholar
• Tang F, Li S, Liu D, et al. Sorafenib sensitizes melanoma cells to vemurafenib through ferroptosis. Transl Cancer Res TCR. 2020 Mar;9(3):1584–1593.
   PubMed Web of Science ®Google Scholar
• Shoushtari AN, Wagstaff J, Ascierto PA, et al. CheckMate 067: long-term outcomes in patients with mucosal melanoma. J Clin Oncol. 2020;38(15_suppl):10019–. doi: 10.1200/JCO.2020.38.15_suppl.10019
   Google Scholar