Antibody dependent cell-mediated cytotoxicity selection pressure induces diverse mechanisms of resistance

References

• Martinelli E, Ciardiello D, Martini G, Troiani T, Cardone C, Vitiello PP, Normanno N, Rachiglio AM, Maiello E, Latiano T, et al. Implementing anti-epidermal growth factor receptor (EGFR) therapy in metastatic colorectal cancer: challenges and future perspectives. Ann Oncol. 2020;31(1):30–19. doi:10.1016/j.annonc.2019.10.007.
   PubMed Web of Science ®Google Scholar
• Granados-García M, Aguilar-Ponce JL, Maldonado-Magos F, De La Garza-Salazar JG. Advanced squamous cell carcinoma of the head and neck: the Current role of Cetuximab. Orl. 2017;78(6):320–333. doi:10.1159/000455891.
   Google Scholar
• Maximiano S, Magalhães P, Guerreiro MP, Morgado M. Trastuzumab in the treatment of breast cancer. BioDrugs. 2016;30(2):75–86. doi:10.1007/s40259-016-0162-9.
   PubMed Web of Science ®Google Scholar
• Boku N. HER2-positive gastric cancer. Gastric Cancer. 2014;17(1):1–12. doi:10.1007/s10120-013-0252-z.
   PubMed Web of Science ®Google Scholar
• Benavente S, Huang S, Armstrong EA, Chi A, Hsu KT, Wheeler DL, Harari PM. Establishment and characterization of a model of acquired resistance to epidermal growth factor receptor targeting agents in human cancer cells. Clin Cancer Res. 2009;15(5):1585–1592. doi:10.1158/1078-0432.CCR-08-2068.
   PubMed Web of Science ®Google Scholar
• Swain SM, Miles D, Kim SB, Im Y-H, Im S-A, Semiglazov V, Ciruelos E, Schneeweiss A, Loi S, Monturus E, et al. Pertuzumab, trastuzumab, and docetaxel for HER2-positive metastatic breast cancer (CLEOPATRA): end-of-study results from a double-blind, randomised, placebo-controlled, phase 3 study. Lancet Oncol. 2020;21(4):519–530. doi:10.1016/S1470-2045(19)30863-0.
   PubMed Web of Science ®Google Scholar
• Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, Laccabue D, Zerbini A, Camisa R, Bisagni G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/ neu –positive metastatic breast cancer. J Clin Oncol. 2008;26(11):1789–1796. doi:10.1200/JCO.2007.14.8957.
   PubMed Web of Science ®Google Scholar
• Bibeau F, Lopez-Crapez E, Di Fiore F, Thezenas S, Ychou M, Blanchard F, Lamy A, Penault-Llorca F, Frébourg T, Michel P, et al. Impact of fcγRIIa-fcγRIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol. 2009;27(7):1122–1129. doi:10.1200/JCO.2008.18.0463.
   PubMed Web of Science ®Google Scholar
• Hubert P, Heitzmann A, Viel S, Nicolas A, Sastre-Garau X, Oppezzo P, Pritsch O, Osinaga E, Amigorena S. Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res. 2011;71(15):5134–5143. doi:10.1158/0008-5472.CAN-10-4222.
   PubMed Web of Science ®Google Scholar
• Arnould L, Gelly M, Penault-Llorca F, Benoit L, Bonnetain F, Migeon C, Cabaret V, Fermeaux V, Bertheau P, Garnier J, et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism? Br J Cancer. 2006;94(2):259–267. doi:10.1038/sj.bjc.6602930.
   PubMed Web of Science ®Google Scholar
• Monteverde M, Milano G, Strola G, Maffi M, Lattanzio L, Vivenza D, Tonissi F, Merlano M, Nigro CL. The relevance of ADCC for EGFR targeting: a review of the literature and a clinically-applicable method of assessment in patients. Crit Rev Oncol Hematol. 2015;95(2):179–190. doi:10.1016/j.critrevonc.2015.02.014.
   PubMed Web of Science ®Google Scholar
• Overdijk MB, Verploegen S, van den Brakel JH, Lammerts van Bueren JJ, Vink T, van de Winkel JG, Parren PW, Bleeker WK. Epidermal growth factor receptor (EGFR) antibody-induced antibody-dependent cellular cytotoxicity plays a Prominent role in Inhibiting Tumorigenesis, even of tumor cells insensitive to EGFR signaling inhibition. J Immunol. 2011;187(6):3383–3390. doi:10.4049/jimmunol.1003926.
   PubMed Web of Science ®Google Scholar
• Capuano C, Pighi C, Battella S, De Federicis D, Galandrini R, Palmieri G. Harnessing cd16-mediated nk cell functions to enhance therapeutic efficacy of tumor-targeting mabs. Cancers Basel. 2021;13(10):1–24. doi:10.3390/cancers13102500.
   Web of Science ®Google Scholar
• Braig F, Kriegs M, Voigtlaender M, Habel B, Grob T, Biskup K, Blanchard V, Sack M, Thalhammer A, Ben Batalla I, et al. Cetuximab resistance in head and neck cancer is mediated by EGFR-K521 polymorphism. Cancer Res. 2017;77(5):1188–1199. doi:10.1158/0008-5472.CAN-16-0754.
   PubMed Web of Science ®Google Scholar
• Brand TM, Iida M, Wheeler DL. Molecular mechanisms of resistance to the EGFR monoclonal antibody cetuximab. Cancer Biol Ther. 2011;11(9):777–792. doi:10.4161/cbt.11.9.15050.
   PubMed Web of Science ®Google Scholar
• Kawaguchi Y, Kono K, Mizukami Y, Mimura K, Fujii H. Mechanisms of escape from trastuzumab-mediated ADCC in esophageal squamous cell carcinoma: relation to susceptibility to perforin-granzyme. Anticancer Res. 2009;29(6):2137–2146.
   PubMed Web of Science ®Google Scholar
• Evans MK, Sauer SJ, Nath S, Robinson TJ, Morse MA, Devi GR. X-linked inhibitor of apoptosis protein mediates tumor cell resistance to antibody-dependent cellular cytotoxicity. Cell Death Disease. 2016;7(1):e2073. doi:10.1038/cddis.2015.412.
   PubMedGoogle Scholar
• Nishie M, Suzuki E, Hattori M, Kawaguch K, Kataoka TR, Hirata M, Pu F, Kotake T, Tsuda M, Yamaguchi A, et al. Downregulated ATP6V1B1 expression acidifies the intracellular environment of cancer cells leading to resistance to antibody-dependent cellular cytotoxicity. Cancer Immunol Immun. 2021;70(3):817–830. doi:10.1007/s00262-020-02732-3.
   PubMed Web of Science ®Google Scholar
• Zahavi D, AlDeghaither D, O’Connell A, Weiner LM. Enhancing antibody-dependent cell-mediated cytotoxicity: a strategy for improving antibody-based immunotherapy. Antib Ther. 2018;1(1):7–12. doi:10.1093/abt/tby002.
   PubMedGoogle Scholar
• Murray JC, Aldeghaither D, Wang S, Nasto RE, Jablonski SA, Tang Y, Weiner LM. C-abl modulates tumor cell sensitivity to antibody-dependent cellular cytotoxicity. Cancer Immunol Res. 2014;2(12):1186–1198. doi:10.1158/2326-6066.CIR-14-0083.
   PubMed Web of Science ®Google Scholar
• Aldeghaither DS, Zahavi DJ, Murray JC, Fertig EJ, Graham GT, Zhang Y-W, O’Connell A, Ma J, Jablonski SA, Weiner LM, et al. A mechanism of resistance to antibody-targeted immune attack. Cancer Immunol Res. 2019;7(2):230–243. doi:10.1158/2326-6066.cir-18-0266.
   PubMed Web of Science ®Google Scholar
• Chung KY, Shia J, Kemeny NE, Shah M, Schwartz GK, Tse A, Hamilton A, Pan D, Schrag D, Schwartz L, et al. Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J Clin Oncol. 2005;23(9):1803–1810. doi:10.1200/JCO.2005.08.037.
   PubMed Web of Science ®Google Scholar
• Seo Y, Ishii Y, Ochiai H, Fukuda K, Akimoto S, Hayashida T, Okabayashi K, Tsuruta M, Hasegawa H, Kitagawa Y, et al. Cetuximab-mediated ADCC activity is correlated with the cell surface expression level of EGFR but not with the KRAS/BRAF mutational status in colorectal cancer. Oncol Rep. 2014;31(5):2115–2122. doi:10.3892/or.2014.3077.
   PubMed Web of Science ®Google Scholar
• Okada Y, Kimura T, Nakagawa T, Okamoto K, Fukuya A, Goji T, Fujimoto S, Sogabe M, Miyamoto H, Muguruma N, et al. EGFR downregulation after anti-EGFR therapy predicts the antitumor effect in colorectal cancer. Mol Cancer Res. 2017;15(10):1445–1454. doi:10.1158/1541-7786.MCR-16-0383.
   PubMed Web of Science ®Google Scholar
• Kim JW, Kim JH, Im SA, Kim YJ, Han H-S, Kim J-S, Lee K-H, Kim T-Y, Han S-W, Jeon YK, et al. HER2/CEP17 ratio and HER2 immunohistochemistry predict clinical outcome after first-line trastuzumab plus taxane chemotherapy in patients with HER2 fluorescence in situ hybridization-positive metastatic breast cancer. Cancer Chemother Pharmacol. 2013;72(1):109–115. doi:10.1007/s00280-013-2174-1.
   PubMed Web of Science ®Google Scholar
• Ferris RL, Jaffee EM, Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J Clin Oncol. 2010;28(28):4390–4399. doi:10.1200/JCO.2009.27.6360.
   PubMed Web of Science ®Google Scholar
• Sforza V, Martinelli E, Ciardiello F, Gambardella V, Napolitano S, Martini G, della Corte C, Cardone C, Ferrara ML, Reginelli A, et al. Mechanisms of resistance to anti-epidermal growth factor receptor inhibitors in metastatic colorectal cancer. World J Gastroenterol. 2016;22(28):6345–6361. doi:10.3748/wjg.v22.i28.6345.
   PubMed Web of Science ®Google Scholar
• Vu T, Claret FX. Trastuzumab: updated mechanisms of action and resistance in breast cancer. Front Oncol. 2012;2:62. doi:10.3389/fonc.2012.00062.
   PubMedGoogle Scholar
• Terry S, Savagner P, Ortiz-Cuaran S, Mahjoubi L, Saintigny P, Thiery JP, Chouaib S. New insights into the role of EMT in tumor immune escape. Mol Oncol. 2017;11(7):824–846. doi:10.1002/1878-0261.12093.
   PubMed Web of Science ®Google Scholar
• Schmitz S, Bindea G, Albu RI, Mlecnik B, Machiels JP. Cetuximab promotes epithelial to mesenchymal transition and cancer associated fibroblasts in patients with head and neck cancer. Oncotarget. 2015;6(33):34288–34299. doi:10.18632/oncotarget.5924.
   PubMedGoogle Scholar
• MacFawn I, Wilson H, Selth LA, Leighton I, Serebriiskii I, Bleackley RC, Elzamzamy O, Farris J, Pifer PM, Richer J, et al. Grainyhead-like-2 confers NK-sensitivity through interactions with epigenetic modifiers. Mol Immunol. 2019;105:137–149. doi:10.1016/j.molimm.2018.11.006.
   PubMed Web of Science ®Google Scholar
• Prager I, Watzl C. Mechanisms of natural killer cell-mediated cellular cytotoxicity. J Leukoc Biol. 2019;105(6):1319–1329. doi:10.1002/JLB.MR0718-269R.
   PubMed Web of Science ®Google Scholar
• Aliño SF, Unda FJ, Perez-Yarza G, Cañavate ML. Are laminin binding sites on tumor cell surface involved in the indomethacin-induced sensitivity to natural cytotoxic cells? Biol Cell. 1989;66(3):255–261. doi:10.1111/j.1768-322X.1989.tb00842.x.
   PubMed Web of Science ®Google Scholar
• Filatova NA, Tyuryaeva II, Ivanov VA. Recognition and lysis by natural killers of tumor cells with participation of laminin. Cell Tissue Biol. 2008;2(1):38–44. doi:10.1134/S1990519X08010069.
   Google Scholar
• Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8(9):713–725. Published online 2008. doi:10.1038/nri2381.
   PubMed Web of Science ®Google Scholar
• MORITA S, YOSHIKADO R, GODA S. CD54 contributes for NK cells cytotoxicity. J Oral Tissue Engine. 2009;6(3):194–200. doi:10.11223/jarde.6.194.
   Google Scholar
• Tazawa K, Koutsogiannaki S, Chamberlain M, Yuki K. The effect of different anesthetics on tumor cytotoxicity by natural killer cells. Toxicol Lett. 2017;266:23–31. doi:10.1016/j.toxlet.2016.12.007.
   PubMed Web of Science ®Google Scholar
• Cooley S, Burns LJ, Repka T, Miller JS. Natural killer cell cytotoxicity of breast cancer targets is enhanced by two distinct mechanisms of antibody-dependent cellular cytotoxicity against LFA-3 and HER2/neu. Exp Hematol. 1999;27(10):1533–1541. doi:10.1016/S0301-472X(99)00089-2.
   PubMed Web of Science ®Google Scholar
• Khodarev NN, Roizman B, Weichselbaum RR. Molecular pathways: Interferon/Stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin Cancer Res. 2012;18(11):3015–3021. doi:10.1158/1078-0432.CCR-11-3225.
   PubMed Web of Science ®Google Scholar
• Kominsky SL, Hobeika AC, Lake FA, Torres BA, Johnson HM. Down-regulation of neu/HER-2 by interferon-gamma in prostate cancer cells. Cancer Res. 2000;60:3904–3908. Published online 2000.
   PubMedGoogle Scholar
• Oliveras-Ferraros C, Vazquez-Martin A, Queralt B, Adrados M, Ortiz R, Cufí S, Hernández-Yagüe X, Guardeño R, Báez L, Martin-Castillo B, et al. Interferon/STAT1 and neuregulin signaling pathways are exploratory biomarkers of cetuximab (Erbitux®) efficacy in KRAS wild-type squamous carcinomas: a pathway-based analysis of whole human-genome microarray data from cetuximab-adapted tumor cell-line models. Int J Oncol. 2011;39(6):1455–1479. doi:10.3892/ijo.2011.1155.
   PubMed Web of Science ®Google Scholar
• Cifaldi L, Prencipe G, Caiello I, Bracaglia C, Locatelli F, De Benedetti F, Strippoli R. Inhibition of natural killer cell cytotoxicity by interleukin-6: implications for the pathogenesis of macrophage activation syndrome. Arthri Rheumatol. 2015;67(11):3037–3046. doi:10.1002/art.39295.
   PubMed Web of Science ®Google Scholar
• Benci JL, Xu B, Qiu Y, Wu TJ, Dada H, Twyman-Saint Victor C, Cucolo L, Lee DSM, Pauken KE, Huang AC, et al. Tumor interferon signaling regulates a multigenic resistance program to immune checkpoint blockade. Cell. 2016;167(6):1540–1554.e12. doi:10.1016/j.cell.2016.11.022.
   PubMed Web of Science ®Google Scholar
• Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature. 2005;436(7054):1186–1190. doi:10.1038/nature03884.
   PubMed Web of Science ®Google Scholar
• Brzostek-Racine S, Gordon C, Van Scoy S, Reich NC. The DNA damage response induces IFN. J Immunol. 2011;187(10):5336–5345. doi:10.4049/jimmunol.1100040.
   PubMed Web of Science ®Google Scholar
• Zerfas BL, Maresh ME, Trader DJ. The immunoproteasome: an emerging target in cancer and autoimmune and neurological disorders. J Med Chem. 2020;63(5):1841–1858. doi:10.1021/acs.jmedchem.9b01226.
   PubMed Web of Science ®Google Scholar
• Shoji T, Kikuchi E, Kikuchi J, Takashima Y, Furuta M, Takahashi H, Tsuji K, Maeda M, Kinoshita I, Dosaka-Akita H, et al. Evaluating the immunoproteasome as a potential therapeutic target in cisplatin-resistant small cell and non-small cell lung cancer. Cancer Chemother Pharmacol. 2020;85(5):843–853. doi:10.1007/s00280-020-04061-9.
   PubMed Web of Science ®Google Scholar
• Leblanc O, Vacher S, Lecerf C, Jeannot E, Klijanienko J, Berger F, Hoffmann C, Calugaru V, Badois N, Chilles A, et al. Biomarkers of cetuximab resistance in patients with head and neck squamous cell carcinoma. Cancer Biol Med. 2020;17(1):208–217. doi:10.20892/j.issn.2095-3941.2019.0153.
   PubMed Web of Science ®Google Scholar
• Kreutzfeldt J, Rozeboom B, Dey N, De P. The trastuzumab era: current and upcoming targeted HER2+ breast cancer therapies. Am J Cancer Res. 2020;10(4):1045–1067.
   PubMed Web of Science ®Google Scholar
• Verhoeven Y, Tilborghs S, Jacobs J, De Waele J, Quatannens D, Deben C, Prenen H, Pauwels P, Trinh XB, Wouters A, et al. The potential and controversy of targeting STAT family members in cancer. Semin Cancer Biol. 2020;60(October):41–56. doi:10.1016/j.semcancer.2019.10.002.
   PubMedGoogle Scholar
• Wolf DM, Yau C, Wulfkuhle J, Brown-Swigart L, Gallagher RI, Lee PRE, Zhu Z, Magbanua MJ, Sayaman R, O’Grady N, et al. Redefining breast cancer subtypes to guide treatment prioritization and maximize response: predictive biomarkers across 10 cancer therapies. Cancer Cell. 2022;40(6):609–623.e6. doi:10.1016/j.ccell.2022.05.005.
   PubMed Web of Science ®Google Scholar
• Kalaora S, Lee JS, Barnea E, Levy R, Greenberg P, Alon M, Yagel G, Bar Eli G, Oren R, Peri A, et al. Immunoproteasome expression is associated with better prognosis and response to checkpoint therapies in melanoma. Nat Commun. 2020;11(1):1–12. doi:10.1038/s41467-020-14639-9.
   PubMed Web of Science ®Google Scholar
• Tabernero J, Pfeiffer P, Cervantes A. Administration of cetuximab every 2 weeks in the treatment of metastatic colorectal cancer: an effective, more convenient alternative to weekly administration? Oncologist. 2008;13(2):113–119. doi:10.1634/theoncologist.2007-0201.
   PubMed Web of Science ®Google Scholar
• Rimawi MF, Wiechmann LS, Wang YC, Huang C, Migliaccio I, Wu M-F, Gutierrez C, Hilsenbeck SG, Arpino G, Massarweh S, et al. Reduced dose and intermittent treatment with Lapatinib and trastuzumab for potent blockade of the HER pathway in HER2/neu -overexpressing breast tumor xenografts. Clin Cancer Res. 2011;17(6):1351–1361. doi:10.1158/1078-0432.CCR-10-1905.
   PubMed Web of Science ®Google Scholar
• Zhang C, Oberoi P, Oelsner S, Waldmann A, Lindner A, Tonn T, Wels WS. Chimeric antigen receptor-engineered NK-92 cells: an off-the-shelf cellular therapeutic for targeted elimination of cancer cells and induction of protective antitumor immunity. Front Immunol. 2017. 8(533). doi:10.3389/fimmu.2017.00533.
   Google Scholar
• Giles AJ, Hao S, Padget M, Song H, Zhang W, Lynes J, Sanchez V, Liu Y, Jung J, Cao X, et al. Efficient ADCC killing of meningioma by avelumab and a high-affinity natural killer cell line, haNK. JCI Insight. 2019;4(20):1–12. doi:10.1172/jci.insight.130688.
   Web of Science ®Google Scholar
• Somanchi SS, Senyukov VV, Denman CJ, Lee DA. Expansion, purification, and functional assessment of human peripheral blood NK cells. J Visualized Exp. 2011;48. doi:10.3791/2540-v
   Google Scholar
• Zhang YW, Jones TL, Martin SE, Caplen NJ, Pommier Y. Implication of checkpoint kinase-dependent up-regulation of ribonucleotide reductase R2 in DNA damage response. J Biol Chem. 2009;284(27):18085–18095. doi:10.1074/jbc.M109.003020.
   PubMed Web of Science ®Google Scholar
• Pjaweletz CP, Charboneau L, Bichsel VE, Simone NL, Chen T, Gillespie JW, Emmert-Buck MR, Roth MJ, Petricoin III EF, Liotta LA, et al. Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene. 2001;20(16):1981–1989. doi:10.1038/sj.onc.1204265.
   PubMed Web of Science ®Google Scholar
• Pierobon M, VanMeter AJ, Moroni N, Galdi F, Petricoin EF. Reverse-phase protein microarrays. Mol Prof: Meth And Prot. 2012;215–235. doi:10.1007/978-1-60327-216-2_14.
   Google Scholar
• Einspahr JG, Calvert V, Alberts DS, Curiel-Lewandrowski C, Warneke J, Krouse R, Stratton SP, Liotta L, Longo C, Pellicani G, et al. Functional protein pathway activation mapping of the progression of normal skin to squamous cell carcinoma. Cancer Prev Res. 2012;5(3):403–413. doi:10.1158/1940-6207.CAPR-11-0427.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–D613. doi:10.1093/nar/gky1131.
   PubMed Web of Science ®Google Scholar
• Granja JM, Corces MR, Pierce SE, Bagdatli ST, Choudhry H, Chang HY, Greenleaf WJ. ArchR is a scalable software package for integrative single-cell chromatin accessibility analysis. Nat Genet. 2021;53(3):403–411. doi:10.1038/s41588-021-00790-6.
   PubMed Web of Science ®Google Scholar