1,390
Views
1
CrossRef citations to date
0
Altmetric
Original research

Lag-3 expression and clinical outcomes in metastatic melanoma patients treated with combination anti-lag-3 + anti-PD-1-based immunotherapies

, , , , , , , , ORCID Icon & show all
Article: 2261248 | Received 16 Apr 2023, Accepted 17 Sep 2023, Published online: 04 Oct 2023

References

  • Burnell SEA, Capitani L, MacLachlan BJ, Mason GH, Gallimore AM, Godkin A. Seven mysteries of LAG-3: a multi-faceted immune receptor of increasing complexity. Immunol Adv. 2022;2(1):ltab025. doi:10.1093/immadv/ltab025.
  • Ascierto PA, Lipson EJ, Dummer R, Larkin J, Long GV, Sanborn RE, Chiarion-Sileni V, Dréno B, Dalle S, Schadendorf D, et al. Nivolumab and relatlimab in patients with advanced melanoma that had progressed on anti–programmed death-1/Programmed death ligand 1 therapy: results from the Phase I/IIa RELATIVITY-020 trial. J Clin Oncol. 2023;41(15):2724–10. JCO.22.02072. doi:10.1200/JCO.22.02072.
  • Tawbi HA, Schadendorf D, Lipson EJ, Ascierto PA, Matamala L, Castillo Gutiérrez E, Rutkowski P, Gogas HJ, Lao CD, De Menezes JJ, et al. Relatlimab and nivolumab versus nivolumab in untreated advanced melanoma. N Engl J Med. 2022;386(1):24–34. doi:10.1056/NEJMoa2109970.
  • Long GV, Stephen HF, Lipson EJ, Schadendorf D, Ascierto PA, Matamala L, Salman P, Castillo Gutiérrez E, Rutkowski P, Gogas HJ, et al. Overall survival and response with Nivolumab and relatlimab in advanced melanoma. NEJM Evidence. 2023;2(4):EVIDoa2200239. doi:10.1056/EVIDoa2200239.
  • Winstead E. Opdualag becomes first FDA-Approved immunotherapy to target LAG-3. National Cancer Institute at the National Institutes of Health; 2022 [accessed Dec 12].
  • Machiraju D, Wiecken M, Lang N, Hülsmeyer I, Roth J, Schank TE, Eurich R, Halama N, Enk A, Hassel JC. Soluble immune checkpoints and T-cell subsets in blood as biomarkers for resistance to immunotherapy in melanoma patients. Oncoimmunology. 2021;10(1):1926762. doi:10.1080/2162402x.2021.1926762.
  • Shen R, Postow MA, Adamow M, Arora A, Hannum M, Maher C, Wong P, Curran MA, Hollmann TJ, Jia L, et al. LAG-3 expression on peripheral blood cells identifies patients with poorer outcomes after immune checkpoint blockade. Sci Transl Med. 2021;13(608). doi:10.1126/scitranslmed.abf5107
  • Ohmura H, Yamaguchi K, Hanamura F, Ito M, Makiyama A, Uchino K, Shimokawa H, Tamura S, Esaki T, Mitsugi K, et al. OX40 and LAG3 are associated with better prognosis in advanced gastric cancer patients treated with anti-programmed death-1 antibody. Br J Cancer. 2020;122(10):1507–1517. doi:10.1038/s41416-020-0810-1.
  • Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228–247. doi:10.1016/j.ejca.2008.10.026.
  • Azimi F, Scolyer RA, Rumcheva P, Moncrieff M, Murali R, McCarthy SW, Saw RP, Thompson JF. Tumor-infiltrating lymphocyte grade is an Independent predictor of sentinel lymph node status and survival in patients with cutaneous melanoma. J Clin Oncol. 2012;30(21):2678–2683. doi:10.1200/JCO.2011.37.8539.
  • Johnson L, McCune B, Locke D, Hedvat C, Wojcik JB, Schroyer C, Yan J, Johnson K, Sanders-Cliette A, Samala S, et al. Development of a LAG-3 immunohistochemistry assay for melanoma. J Clin Pathol. 2022. jclinpath-2022-208254. doi:10.1136/jclinpath-2022-208254.
  • Pistillo MP, Carosio R, Grillo F, Fontana V, Mastracci L, Morabito A, Banelli B, Tanda E, Cecchi F, Dozin B, et al. Phenotypic characterization of tumor CTLA-4 expression in melanoma tissues and its possible role in clinical response to ipilimumab. Cl Immunol. 2020;215:108428. doi:10.1016/j.clim.2020.108428.
  • Daud AI, Wolchok JD, Robert C, Hwu W-J, Weber JS, Ribas A, Hodi FS, Joshua AM, Kefford R, Hersey P, et al. Programmed death-ligand 1 expression and response to the anti–programmed death 1 antibody pembrolizumab in melanoma. J Clin Oncol. 2016;34(34):4102–4109. doi:10.1200/JCO.2016.67.2477.
  • Gide TN, Quek C, Menzies AM, Tasker AT, Shang P, Holst J, Madore J, Lim SY, Velickovic R, Wongchenko M, et al. Distinct immune cell populations define response to anti-PD-1 monotherapy and anti-PD-1/Anti-CTLA-4 combined therapy. Cancer Cell. 2019;35(2):238–255.e236. doi:10.1016/j.ccell.2019.01.003.
  • Placke J-M, Soun C, Bottek J, Herbst R, Terheyden P, Utikal J, Pföhler C, Ulrich J, Kreuter A, Pfeiffer C, et al. Digital Quantification of tumor PD-L1 predicts outcome of PD-1-Based immune checkpoint therapy in metastatic melanoma [original research]. Front Oncol. 2021;11:11. doi:10.3389/fonc.2021.741993.
  • Madore J, Vilain RE, Menzies AM, Kakavand H, Wilmott JS, Hyman J, Yearley JH, Kefford RF, Thompson JF, Long GV, et al. PD-L1 expression in melanoma shows marked heterogeneity within and between patients: implications for anti-PD-1/PD-L1 clinical trials. Pigment Cell Melanoma Res. 2015;28(3):245–253. doi:10.1111/pcmr.12340.
  • Carlino MS, Long GV, Schadendorf D, Robert C, Ribas A, Richtig E, Nyakas M, Caglevic C, Tarhini A, Blank C, et al. Outcomes by line of therapy and programmed death ligand 1 expression in patients with advanced melanoma treated with pembrolizumab or ipilimumab in KEYNOTE-006: a randomised clinical trial. Eur J Cancer. 2018;101:236–243. doi:10.1016/j.ejca.2018.06.034.
  • Larkin J, Chiarion-Sileni V, Gonzalez R, Grob J-J, Rutkowski P, Lao CD, Cowey CL, Schadendorf D, Wagstaff J, Dummer R, et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2019;381(16):1535–1546. doi:10.1056/NEJMoa1910836.
  • Rozeman EA, Hoefsmit EP, Reijers ILM, Saw RPM, Versluis JM, Krijgsman O, Dimitriadis P, Sikorska K, van de Wiel BA, Eriksson H, et al. Survival and biomarker analyses from the OpACIN-neo and OpACIN neoadjuvant immunotherapy trials in stage III melanoma. Nat Med. 2021;27(2):256–263. doi:10.1038/s41591-020-01211-7.
  • Rozeman EA, Menzies AM, van Akkooi ACJ, Adhikari C, Bierman C, van de Wiel BA, Scolyer RA, Krijgsman O, Sikorska K, Eriksson H, et al. Identification of the optimal combination dosing schedule of neoadjuvant ipilimumab plus nivolumab in macroscopic stage III melanoma (OpACIN-neo): a multicentre, phase 2, randomised, controlled trial. Lancet Oncol. 2019;20(7):948–960. doi:10.1016/S1470-2045(19)30151-2.
  • Amaria RN, Postow M, Burton EM, Tezlaff MT, Ross MI, Torres-Cabala C, Glitza IC, Duan F, Milton DR, Busam K, et al. Neoadjuvant relatlimab and nivolumab in resectable melanoma. Nature. 2022;611(7934):155–160. doi:10.1038/s41586-022-05368-8.
  • Robert C, Schadendorf D, Long GV, Ascierto P, Intagliata S, Meier F, van der Veldt AAM, Ribas A, Weber JS, Stenson L, et al. 1084P PLATForM: descriptive analysis from a randomised, phase II study of novel spartalizumab combinations in previously treated unresectable/metastatic melanoma. Ann Oncol. 2021;32:S898. doi:10.1016/j.annonc.2021.08.1469.
  • Zhang Y, Liu YD, Luo YL, Liu BL, Huang QT, Wang F, Zhong Q. Prognostic value of lymphocyte activation gene-3 (LAG-3) expression in esophageal squamous cell carcinoma. J Cancer. 2018;9(22):4287–4293. doi:10.7150/jca.26949.
  • Rhyner Agocs G, Assarzadegan N, Kirsch R, Dawson H, Galván JA, Lugli A, Zlobec I, Berger MD. LAG-3 expression predicts outcome in stage II colon Cancer. J Pers Med. 2021;11(8):749. doi:10.3390/jpm11080749.
  • He Y, Yu H, Rozeboom L, Rivard CJ, Ellison K, Dziadziuszko R, Suda K, Ren S, Wu C, Hou L, et al. LAG-3 protein expression in non–small cell lung Cancer and its relationship with PD-1/PD-L1 and tumor-infiltrating lymphocytes. J Thorac Oncol. 2017;12(5):814–823. doi:10.1016/j.jtho.2017.01.019.
  • Wang M, Du Q, Jin J, Wei Y, Lu Y, Li Q. LAG3 and its emerging role in cancer immunotherapy. Clin Transl Med. 2021;11(3):e365. doi:10.1002/ctm2.365.
  • Garcia Cruz D, Giri RR, Gamiotea Turro D, Balsbaugh JL, Adler AJ, Rodriguez A. Lymphocyte activation gene-3 regulates dendritic cell metabolic programming and T cell priming function. J Immunol. 2021;207(9):2374–2384. doi:10.4049/jimmunol.2001188.
  • Workman CJ, Wang Y, El Kasmi KC, Pardoll DM, Murray PJ, Drake CG, Vignali DAA. LAG-3 regulates plasmacytoid dendritic cell Homeostasis1. J Immunol. 2009;182(4):1885–1891. doi:10.4049/jimmunol.0800185.
  • Camisaschi C, De Filippo A, Beretta V, Vergani B, Villa A, Vergani E, Santinami M, Cabras AD, Arienti F, Triebel F, et al. Alternative activation of human plasmacytoid DCs in vitro and in melanoma lesions: involvement of LAG-3. J Invest Dermatol. 2014;134(7):1893–1902. doi:10.1038/jid.2014.29.
  • Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol. 2011;29(1):163–183. doi:10.1146/annurev-immunol-031210-101345.