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Original research

Digital spatial profiling of melanoma shows CD95 expression in immune cells is associated with resistance to immunotherapy

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Article: 2260618 | Received 16 Mar 2023, Accepted 14 Sep 2023, Published online: 27 Sep 2023

References

  • Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, McDermott D, Linette GP, Meyer N, Giguere JK, Agarwala SS, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015;372(21):2006–10. doi:10.1056/NEJMoa1414428.
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti–PD-1 antibody in Cancer. N Engl J Med. 2012;366(26):2443–2454. doi:10.1056/NEJMoa1200690.
  • Wolchok JD, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob JJ, Cowey CL, Lao CD, Wagstaff J, Schadendorf D, Ferrucci PF, et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2017;377(14):1345–1356. doi:10.1056/NEJMoa1709684.
  • Weber JS, D’Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, Hoeller C, Khushalani NI, Miller WH, Lao CD, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015;16(4):375–384. doi:10.1016/S1470-2045(15)70076-8.
  • Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373(1):23–34. doi:10.1056/NEJMoa1504030.
  • Merritt CR, Ong GT, Church SE, Barker K, Danaher P, Geiss G, Hoang M, Jung J, Liang Y, McKay-Fleisch J, et al. Multiplex digital spatial profiling of proteins and RNA in fixed tissue. Nat Biotechnol. 2020;38(5):586–599. doi:10.1038/s41587-020-0472-9.
  • Toki MI, Merritt CR, Wong PF, Smithy JW, Kluger HM, Syrigos KN, Ong GT, Warren SE, Beechem JM, Rimm DL. High-plex predictive marker Discovery for melanoma immunotherapy–treated patients using Digital spatial profiling. Clin Cancer Res. 2019;25(18):5503–5512. doi:10.1158/1078-0432.CCR-19-0104.
  • Camp RL, Charette LA, Rimm DL. Validation of tissue microarray technology in breast carcinoma. Lab Invest. 2000;80(12):1943–1949. doi:10.1038/labinvest.3780204.
  • Martinez-Morilla S, Villarroel-Espindola F, Wong PF, Toki MI, Aung TN, Pelekanou V, Bourke-Martin B, Schalper KA, Kluger HM, Rimm DL. Biomarker Discovery in patients with immunotherapy-treated melanoma with imaging mass cytometry. Clin Cancer Res. 2021;27(7):1987–1996. doi:10.1158/1078-0432.CCR-20-3340.
  • 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.
  • Zugazagoitia J, Gupta S, Liu Y, Fuhrman K, Gettinger S, Herbst RS, Schalper KA, Rimm DL. Biomarkers associated with beneficial PD-1 checkpoint blockade in non–Small cell lung Cancer (NSCLC) identified using high-plex Digital spatial profiling. Clin Cancer Res. 2020;26(16):4360–4368. doi:10.1158/1078-0432.CCR-20-0175.
  • Wong PF, Wei W, Smithy JW, Acs B, Toki MI, Blenman KRM, Zelterman D, Kluger HM, Rimm DL. Multiplex Quantitative analysis of tumor-Infiltrating Lymphocytes and immunotherapy outcome in metastatic melanoma. Clin Cancer Res. 2019;25(8):2442–2449. doi:10.1158/1078-0432.CCR-18-2652.
  • Liu Y, Zugazagoitia J, Ahmed FS, Henick BS, Gettinger SN, Herbst RS, Schalper KA, Rimm DL. Immune cell PD-L1 colocalizes with macrophages and is associated with outcome in PD-1 pathway blockade therapy. Clin Cancer Res. 2020;26(4):970–977. doi:10.1158/1078-0432.CCR-19-1040.
  • Neumeister VM, Anagnostou V, Siddiqui S, England AM, Zarrella ER, Vassilakopoulou M, Parisi F, Kluger Y, Hicks DG, Rimm DL. Quantitative assessment of effect of preanalytic cold ischemic time on protein expression in breast cancer tissues. J Natl Cancer Inst. 2012;104(23):1815–1824. doi:10.1093/jnci/djs438.
  • Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568–571. doi:10.1038/nature13954.
  • Edwards J, Wilmott JS, Madore J, Gide TN, Quek C, Tasker A, Ferguson A, Chen J, Hewavisenti R, Hersey P, et al. CD103+ tumor-resident CD8+ T cells are associated with improved survival in immunotherapy-naïve melanoma patients and expand significantly during anti–PD-1 treatment. Clin Cancer Res. 2018;24(13):3036–3045. doi:10.1158/1078-0432.CCR-17-2257.
  • Gide TN, Silva IP, Quek C, Ahmed T, Menzies AM, Carlino MS, Saw RPM, Thompson JF, Batten M, Long GV, et al. Close proximity of immune and tumor cells underlies response to anti-PD-1 based therapies in metastatic melanoma patients. Oncoimmunology. 2020;9(1):1659093. doi:10.1080/2162402X.2019.1659093.
  • Halse H, Colebatch AJ, Petrone P, Henderson MA, Mills JK, Snow H, Westwood JA, Sandhu S, Raleigh JM, Behren A, et al. Multiplex immunohistochemistry accurately defines the immune context of metastatic melanoma. Scie Rep. 2018;8(1):11158. doi:10.1038/s41598-018-28944-3.
  • Toki MI, Cecchi F, Hembrough T, Syrigos KN, Rimm DL. Proof of the quantitative potential of immunofluorescence by mass spectrometry. Lab Invest. 2017;97(3):329–334. doi:10.1038/labinvest.2016.148.
  • Camp RL, Chung GG, Rimm DL. Automated subcellular localization and quantification of protein expression in tissue microarrays. Nat Med. 2002;8(11):1323–1327. doi:10.1038/nm791.
  • Eton O, Legha SS, Moon TE, Buzaid AC, Papadopoulos NE, Plager C, Burgess AM, Bedikian AY, Ring S, Dong Q, et al. Prognostic factors for survival of patients treated systemically for disseminated melanoma. J Clin Oncol. 1998;16(3):1103–1111. doi:10.1200/JCO.1998.16.3.1103.
  • Manola J, Atkins M, Ibrahim J, Kirkwood J. Prognostic factors in metastatic melanoma: a pooled analysis of Eastern Cooperative Oncology group trials. J Clin Oncol. 2000;18(22):3782–3793. doi:10.1200/JCO.2000.18.22.3782.
  • Joosse A, Collette S, Suciu S, Nijsten T, Patel PM, Keilholz U, Eggermont AMM, Coebergh JWW, de Vries E. Sex is an independent prognostic indicator for survival and relapse/progression-free survival in metastasized stage III to IV melanoma: a pooled analysis of five European organisation for research and treatment of cancer randomized controlled trials. J Clin Oncol. 2013;31(18):2337–2346. doi:10.1200/JCO.2012.44.5031.
  • Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116(2):205–219. doi:10.1016/S0092-8674(04)00046-7.
  • MacNeil T, Vathiotis IA, Martinez-Morilla S, Yaghoobi V, Zugazagoitia J, Liu Y, Rimm DL. Antibody validation for protein expression on tissue slides: a protocol for immunohistochemistry. Biotechniques. 2020;69(6):460–468. doi:10.2144/btn-2020-0095.
  • Xiao W, Du N, Huang T, Guo J, Mo X, Yuan T, Chen Y, Ye T, Xu C, Wang W, et al. TP53 mutation as potential negative predictor for response of anti-CTLA-4 therapy in metastatic melanoma. EBioMedicine. 2018;32:119–124. doi:10.1016/j.ebiom.2018.05.019.
  • Martinez-Morilla S, McGuire J, Gaule P, Moore L, Acs B, Cougot D, Gown AM, Yaziji H, Wang W-L, Cartun RW, et al. Quantitative assessment of PD-L1 as an analyte in immunohistochemistry diagnostic assays using a standardized cell line tissue microarray. Lab Invest. 2019;100(1):4–15. doi:10.1038/s41374-019-0295-9.
  • Sompuram SR, Torlakovic EE, ‘t Hart, T Hart NA K, Bogen SA, ‘t Hart NA. Quantitative comparison of PD-L1 IHC assays against NIST standard reference material 1934. Mod Pathol. 2021;34(12):2242. doi:10.1038/s41379-021-00898-4.
  • Rimm DL, Han G, Taube JM, Yi ES, Bridge JA, Flieder DB, Homer R, West WW, Wu H, Roden AC, et al. A prospective, multi-institutional, pathologist-based assessment of 4 immunohistochemistry assays for PD-L1 expression in non–small cell lung Cancer. JAMA Oncol. 2017;3(8):1051–1058. doi:10.1001/jamaoncol.2017.0013.
  • Hirsch FR, McElhinny A, Stanforth D, Ranger-Moore J, Jansson M, Kulangara K, Richardson W, Towne P, Hanks D, Vennapusa B, et al. PD-L1 immunohistochemistry assays for lung Cancer: results from phase 1 of the blueprint PD-L1 IHC assay comparison project. J Thorac Oncol. 2017;12(2):208–222. doi:10.1016/j.jtho.2016.11.2228.
  • Daud AI, Wolchok JD, Robert C, Hwu WJ, 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.
  • Doroshow DB, Sanmamed MF, Hastings K, Politi K, Rimm DL, Chen L, Melero I, Schalper KA, Herbst RS. Immunotherapy in non–small cell lung Cancer: facts and hopes. Clin Cancer Res. 2019;25(15):4592–4602. doi:10.1158/1078-0432.CCR-18-1538.
  • Peter ME, Hadji A, Murmann AE, Brockway S, Putzbach W, Pattanayak A, Ceppi P. The role of CD95 and CD95 ligand in cancer. Cell Death Differ. 2015;22(4):549–559. doi:10.1038/cdd.2015.3.
  • Richards DM, Merz C, Gieffers C, Krendyukov A. CD95L and anti-tumor immune response: Current understanding and New evidence. Cancer Manag Res. 2021;13:2477–2482. doi:10.2147/CMAR.S297499.
  • Teodorczyk M, Kleber S, Wollny D, Sefrin JP, Aykut B, Mateos A, Herhaus P, Sancho-Martinez I, Hill O, Gieffers C, et al. CD95 promotes metastatic spread via Sck in pancreatic ductal adenocarcinoma. Cell Death Differ. 2015;22(7):1192–1202. doi:10.1038/cdd.2014.217.
  • Ma Y, Liu H, Tu-Rapp H, Thiesen HJ, Ibrahim SM, Cole SM, Pope RM. Fas ligation on macrophages enhances IL-1R1–toll-like receptor 4 signaling and promotes chronic inflammation. Nat Immunol. 2004;5(4):380–387. doi:10.1038/ni1054.
  • Wang D, DuBois RN. Immunosuppression associated with chronic inflammation in the tumor microenvironment. Carcinogenesis. 2015;36(10):1085–1093. doi:10.1093/carcin/bgv123.
  • Xiang X, Wang J, Lu D, Xu X. Targeting tumor-associated macrophages to synergize tumor immunotherapy. Signal Transduct Target Ther. 2021;6(1):75. doi:10.1038/s41392-021-00484-9.
  • Ogino S, Galon J, Fuchs CS, Dranoff G. Cancer immunology–analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011;8:711–719. doi:10.1038/nrclinonc.2011.122.
  • Giesen C, Wang HA, Schapiro D, Zivanovic N, Jacobs A, Hattendorf B, Schüffler PJ, Grolimund D, Buhmann JM, Brandt S, et al. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat Methods. 2014;11(4):417–422. doi:10.1038/nmeth.2869.
  • Angelo M, Bendall SC, Finck R, Hale MB, Hitzman C, Borowsky AD, Levenson RM, Lowe JB, Liu SD, Zhao S, et al. Multiplexed ion beam imaging of human breast tumors. Nat Med. 2014;20(4):436–442. doi:10.1038/nm.3488.