Molecular alterations in claudin 18 suppressed and non-suppressed gastric adenocarcinomas to guide targeted therapies

References

• Kendrick P, Kelly YO, Baumann MM, Compton K, Blacker BF, Daoud F, Li Z, Mouhanna F, Nassereldine H, Schmidt C. et al. The burden of stomach cancer mortality by county, race, and ethnicity in the USA, 2000–2019: a systematic analysis of health disparities. Lancet Reg Health Am. 2023;24:100547. doi:10.1016/j.lana.2023.100547 PMID: 37600165; PMCID: PMC10435837.
   PubMedGoogle Scholar
• Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17–15. doi: 10.3322/caac.21763 PMID: 36633525.
   PubMed Web of Science ®Google Scholar
• Shitara K, Ajani JA, Moehler M, Garrido M, Gallardo C, Shen L, Yamaguchi K, Wyrwicz L, Skoczylas T, Bragagnoli AC. et al. Nivolumab plus chemotherapy or ipilimumab in gastro-oesophageal cancer. Nature. 2022;603(7903):942–948. doi:10.1038/s41586-022-04508-4 PMID: 35322232; PMCID: PMC8967713.
   PubMed Web of Science ®Google Scholar
• Janjigian YY, Kawazoe A, Yañez P, Li N, Lonardi S, Kolesnik O, Barajas O, Bai Y, Shen L, Tang Y. et al. The KEYNOTE-811 trial of dual PD-1 and HER2 blockade in HER2-positive gastric cancer. Nature. 2021;600(7890):727–730. doi:10.1038/s41586-021-04161-3 PMID: 34912120; PMCID: PMC8959470.
   PubMed Web of Science ®Google Scholar
• Kwon M, An M, Klempner SJ, Lee H, Kim KM, Sa JK, Cho HJ, Hong JY, Lee T, Min YW. et al. Determinants of response and intrinsic resistance to PD-1 blockade in microsatellite instability-high gastric cancer. Cancer Discov. 2021;11(9):2168–2185. doi: 10.1158/2159-8290.CD-21-0219 PMID: 33846173.
   PubMed Web of Science ®Google Scholar
• Fontana E, Smyth EC. Dissecting response and resistance to anti-PD-1 therapy in Microsatellite-Unstable Gastric cancer. Cancer Discov. 2021;11(9):2126–2128. doi: 10.1158/2159-8290.CD-21-0857 PMID: 34479973.
   PubMed Web of Science ®Google Scholar
• Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T. et al. ToGA trial investigators. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010;376(9742):687–697. doi:10.1016/S0140-6736(10)61121-X PMID: 20728210.
   PubMed Web of Science ®Google Scholar
• Mitani S, Kawakami H. Emerging targeted therapies for HER2 positive gastric cancer that can overcome trastuzumab resistance. Cancers Basel. 2020;12(2):400. doi:10.3390/cancers12020400 PMID: 32050652; PMCID: PMC7072407.
   PubMed Web of Science ®Google Scholar
• Shah MA, Kennedy EB, Alarcon-Rozas AE, Alcindor T, Bartley AN, Malowany AB, Bhadkamkar NA, Deighton DC, Janjigian Y, Karippot A. et al. Immunotherapy and targeted therapy for advanced gastroesophageal cancer: ASCO guideline. J Clin Oncol. 2023;41(7):1470–1491. doi:10.1200/JCO.22.02331 PMID: 36603169.
   PubMed Web of Science ®Google Scholar
• Shitara K, Bang YJ, Iwasa S, Sugimoto N, Ryu MH, Sakai D, Chung HC, Kawakami H, Yabusaki H, Lee J. et al. DESTINY-Gastric01 investigators. Trastuzumab deruxtecan in Previously treated HER2-positive gastric cancer. N Engl J Med. 2020;382(25):2419–2430. doi:10.1056/NEJMoa2004413 PMID: 32469182.
   PubMed Web of Science ®Google Scholar
• Wong MT, Singhi AD, Larson BK, Huynh CAT, Balzer BL, Burch M, Dhall D, Gangi A, Gong J, Guindi M. et al. Claudin-18. Arch Pathol Lab Med. 2022;147(5):559–567. doi:10.5858/arpa.2021-0428-OA PMID: 35976638.
   PubMedGoogle Scholar
• Derks S, vanLaarhoven HWM. Spotlight on GLOW. Cell Rep Med. 2023;4(10):101233. doi:10.1016/j.xcrm.2023.101233 PMID: 37852180; PMCID: PMC10591046.
   PubMedGoogle Scholar
• Shah MA, Shitara K, Ajani JA, Bang YJ, Enzinger P, Ilson D, Lordick F, Van Cutsem E, Gallego Plazas J, Huang J. et al. Zolbetuximab plus CAPOX in CLDN18.2-positive gastric or gastroesophageal junction adenocarcinoma: the randomized, phase 3 GLOW trial. Nat Med. 2023;29(8):2133–2141. doi:10.1038/s41591-023-02465-7 PMID: 37524953; PMCID: PMC10427418.
   PubMed Web of Science ®Google Scholar
• Shitara K, Lordick F, Bang YJ, Enzinger P, Ilson D, Shah MA, Van Cutsem E, Xu RH, Aprile G, Xu J. et al. Zolbetuximab plus mFOLFOX6 in patients with CLDN18.2-positive, HER2-negative, untreated, locally advanced unresectable or metastatic gastric or gastro-oesophageal junction adenocarcinoma (SPOTLIGHT): a multicentre, randomised, double-blind, phase 3 trial. Lancet. 2023;401(10389):1655–1668. doi:10.1016/S0140-6736(23)00620-7 PMID: 37068504.
   PubMed Web of Science ®Google Scholar
• Depotte L, Palle J, Rasola C, Broudin C, VA A, Mariani A, Zaanan A. New developments and standard of care in the management of advanced gastric cancer. Clin Res Hepatol Gastroenterol. 2024;48(1):102245. doi: 10.1016/j.clinre.2023.102245 PMID: 37952913.
   PubMed Web of Science ®Google Scholar
• Niimi T, Nagashima K, Ward JM, Minoo P, Zimonjic DB, Popescu NC, Kimura S. Claudin-18, a novel downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor, encodes lung- and stomach-specific isoforms through alternative splicing. Mol Cell Biol. 2001;21(21):7380–7390. doi: 10.1128/MCB.21.21.7380-7390.2001 PMID: 11585919; PMCID: PMC99911.
   PubMed Web of Science ®Google Scholar
• Kyuno D, Takasawa A, Takasawa K, Ono Y, Aoyama T, Magara K, Nakamori Y, Takemasa I, Osanai M. Claudin-18.2 as a therapeutic target in cancers: cumulative findings from basic research and clinical trials. Tissue Barriers. 2022;10(1):1967080. doi:10.1080/21688370.2021.1967080 PMID: 34486479; PMCID: PMC8794250.
   PubMed Web of Science ®Google Scholar
• Hashimoto I, Oshima T. Claudins and Gastric cancer: an overview. Cancers Basel. 2022;14(2):290. doi:10.3390/cancers14020290 PMID: 35053454; PMCID: PMC8773541.
   PubMed Web of Science ®Google Scholar
• Yano K, Imaeda T, Niimi T. Transcriptional activation of the human claudin-18 gene promoter through two AP-1 motifs in PMA-stimulated MKN45 gastric cancer cells. Am J Physiol Gastrointest Liver Physiol. 2008;294(1):G336–G343. doi: 10.1152/ajpgi.00328.2007 PMID: 18032479.
   PubMed Web of Science ®Google Scholar
• Cao W, Xing H, Li Y, Tian W, Song Y, Jiang Z, Yu J. Claudin18.2 is a novel molecular biomarker for tumor-targeted immunotherapy. Biomark Res. 2022;10(1):38. doi:10.1186/s40364-022-00385-1 PMID: 35642043; PMCID: PMC9153115.
   PubMed Web of Science ®Google Scholar
• Türeci Ӧ, Mitnacht-Kraus R, Wöll S, Yamada T, Sahin U. Characterization of zolbetuximab in pancreatic cancer models. Oncoimmunology. 2018;8(1):e1523096. doi: 10.1080/2162402X.2018.1523096 PMID: 30546962; PMCID: PMC6287799.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513(7517):202–209. doi:10.1038/nature13480 PMID: 25079317; PMCID: PMC4170219.
   PubMed Web of Science ®Google Scholar
• Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 2011;12:323. doi:10.1186/1471-2105-12-323 PMID: 21816040; PMCID: PMC3163565.
   PubMed Web of Science ®Google Scholar
• Carter SL, Cibulskis K, Helman E, McKenna A, Shen H, Zack T, Laird PW, Onofrio RC, Winckler W, Weir BA. et al. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol. 2012;30(5):413–421. doi:10.1038/nbt.2203 PMID: 22544022; PMCID: PMC4383288.
   PubMed Web of Science ®Google Scholar
• Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E. et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–404. doi:10.1158/2159-8290.CD-12-0095 PMID: 22588877; PMCID: PMC3956037.
   PubMed Web of Science ®Google Scholar
• Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E. et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioportal. Sci Signal. 2013;6(269):l1. doi:10.1126/scisignal.2004088 PMID: 23550210; PMCID: PMC4160307.
   Web of Science ®Google Scholar
• Chakravarty D, Gao J, Phillips SM, Kundra R, Zhang H, Wang J, Rudolph JE, Yaeger R, Soumerai T, Nissan MH. et al. OncoKB: a precision oncology knowledge base. JCO Precis Oncol. 2017;2017(1):1–16. doi: 10.1200/PO.17.00011 PMID: 28890946; PMCID: PMC5586540.
   Google Scholar
• Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Å S, Kampf C, Sjöstedt E, Asplund A. et al. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419. doi: 10.1126/science.1260419 PMID: 25613900.
   PubMed Web of Science ®Google Scholar
• Meylan P, Dreos R, Ambrosini G, Groux R, Bucher P. EPD in 2020: enhanced data visualization and extension to ncRNA promoters. Nucleic Acids Res. 2020;48(D1):D65–D69. doi: 10.1093/nar/gkz1014 PMID: 31680159; PMCID: PMC7145694.
   PubMed Web of Science ®Google Scholar
• Khan A, Fornes O, Stigliani A, Gheorghe M, Castro-Mondragon JA, van der Lee R, Bessy A, Chèneby J, Kulkarni SR, Tan G. et al. JASPAR 2018: update of the open-access database of transcription factor binding profiles and its web framework. Nucleic Acids Res. 2018;46(D1):D260–D266. doi:10.1093/nar/gkx1126 PMID: 29140473; PMCID: PMC5753243.
   PubMed Web of Science ®Google Scholar
• Pellino A, Brignola S, Riello E, Niero M, Murgioni S, Guido M, Nappo F, Businello G, Sbaraglia M, Bergamo F. et al. Association of CLDN18 protein expression with clinicopathological features and prognosis in advanced gastric and gastroesophageal junction adenocarcinomas. J Pers Med. 2021;11(11):1095. doi:10.3390/jpm11111095 PMID: 34834447; PMCID: PMC8624955.
   PubMed Web of Science ®Google Scholar
• Jia K, Chen Y, Sun Y, Hu Y, Jiao L, Ma J, Yuan J, Qi C, Li Y, Gong J. et al. Multiplex immunohistochemistry defines the tumor immune microenvironment and immunotherapeutic outcome in CLDN18.2-positive gastric cancer. BMC Med. 2022;20(1):223. doi:10.1186/s12916-022-02421-1 PMID: 35811317; PMCID: PMC9272556.
   PubMed Web of Science ®Google Scholar
• Klempner SJ, Janjigian YY, Wainberg ZA. Claudin18.Who? Examining biomarker overlap and outcomes in claudin18.2-positive gastroesophageal adenocarcinomas. ESMO Open. 2023;8(2):100778. doi:10.1016/j.esmoop.2022.100778 PMID: 36791669; PMCID: PMC9958250.
   PubMed Web of Science ®Google Scholar
• Nateri AS, Spencer-Dene B, Behrens A. Interaction of phosphorylated c-jun with TCF4 regulates intestinal cancer development. Nature. 2005;437(7056):281–285. doi:10.1038/nature03914 PMID: 16007074.
   PubMed Web of Science ®Google Scholar
• Hankey W, Chen Z, Bergman MJ, Fernandez MO, Hancioglu B, Lan X, Jegga AG, Zhang J, Jin VX, Aronow BJ. et al. Chromatin-associated APC regulates gene expression in collaboration with canonical WNT signaling and AP-1. Oncotarget. 2018;9(58):31214–31230. doi:10.18632/oncotarget.25781 PMID: 30131849; PMCID: PMC6101278.
   PubMedGoogle Scholar
• Zhu Y, Yan C, Wang X, Xu Z, Lv J, Xu X, Yu W, Zhou M, Yue L. Pan-cancer analysis of ARID family members as novel biomarkers for immune checkpoint inhibitor therapy. Cancer Biol Ther. 2022;23(1):104–111. doi:10.1080/15384047.2021.2011643 PMID: 35239432; PMCID: PMC8896200.
   PubMed Web of Science ®Google Scholar
• Okamura R, Kato S, Lee S, Jimenez RE, Sicklick JK, Kurzrock R. ARID1A alterations function as a biomarker for longer progression-free survival after anti-PD-1/PD-L1 immunotherapy. J Immunother Cancer. 2020;8(1):e000438. doi:10.1136/jitc-2019-000438 PMID: 32111729; PMCID: PMC7057434.
   PubMed Web of Science ®Google Scholar
• Kubota Y, Kawazoe A, Mishima S, Nakamura Y, Kotani D, Kuboki Y, Bando H, Kojima T, Doi T, Yoshino T. et al. Comprehensive clinical and molecular characterization of claudin 18.2 expression in advanced gastric or gastroesophageal junction cancer. ESMO Open. 2023;8(1):100762. doi: 10.1016/j.esmoop.2022.100762 PMID: 36610262; PMCID: PMC10024138.
   PubMed Web of Science ®Google Scholar
• Pereira MA, Ramos MFKP, Dias AR, Cardili L, Ribeiro RRE, de Castria TB, Zilberstein B, Nahas SC, U R Jr, de Mello ES. RhoA, Claudin 18, and c-MET in Gastric cancer: clinicopathological characteristics and prognostic significance in curative resected patients. Med Sci (Basel). 2021;10(1):4. doi:10.3390/medsci10010004 PMID: 35076580; PMCID: PMC8788521.
   PubMedGoogle Scholar
• Wang C, Wang Y, Chen J, Wang Y, Pang C, Liang C, Yuan L, Ma Y. CLDN18.2 expression and its impact on prognosis and the immune microenvironment in gastric cancer. BMC Gastroenterol. 2023;23(1):283. doi:10.1186/s12876-023-02924-y PMID: 37582713; PMCID: PMC10428652.
   PubMed Web of Science ®Google Scholar
• Li J, Zhang Y, Hu D, Gong T, Xu R, Gao J. Analysis of the expression and genetic alteration of CLDN18 in gastric cancer. Aging (Albany NY). 2020;12(14):14271–14284. doi:10.18632/aging.103457 PMID: 32668412; PMCID: PMC7425459.
   PubMedGoogle Scholar
• Nishijima TF, Kardos J, Chai S, Smith CC, Bortone DS, Selitsky SR, Parker JS, Sanoff HK, Lee MS, Vincent BG. Molecular and clinical characterization of a Claudin-Low Subtype of Gastric cancer. JCO Precis Oncol. 2017;1:1–10. doi:10.1200/PO.17.00047 PMID: 35172495.
   PubMed Web of Science ®Google Scholar
• Kardos J, Chai S, Mose LE, Selitsky SR, Krishnan B, Saito R, Iglesia MD, Milowsky MI, Parker JS, Kim WY. et al. Claudin-low bladder tumors are immune infiltrated and actively immune suppressed. JCI Insight. 2016;1(3):e85902. doi:10.1172/jci.insight.85902 PMID: 27699256; PMCID: PMC5033914.
   PubMed Web of Science ®Google Scholar
• Voutsadakis IA. Ubiquitination and the Ubiquitin-Proteasome System as regulators of transcription and transcription factors in epithelial mesenchymal transition of cancer. Tumour Biol. 2012;33(4):897–910. doi: 10.1007/s13277-012-0355-x PMID: 22399444.
   PubMedGoogle Scholar
• Ishigami S, Natsugoe S, Nakajo A, Arigami T, Kitazono M, Okumura H, Matsumoto M, Uchikado Y, Setoyama T, Sasaki K. et al. HLA-class I expression in gastric cancer. J Surg Oncol. 2008;97(7):605–608. doi:10.1002/jso.21029 PMID: 18459158.
   PubMed Web of Science ®Google Scholar
• Klempner SJ, Lee KW, Shitara K, Metges JP, Lonardi S, Ilson DH, Fazio N, Kim TY, Bai LY, Moran D. et al. ILUSTRO: phase II multicohort trial of Zolbetuximab in patients with advanced or metastatic claudin 18.2-positive gastric or gastroesophageal junction adenocarcinoma. Clin Cancer Res. 2023;29(19):3882–3891. doi:10.1158/1078-0432.CCR-23-0204 PMID: 37490286; PMCID: PMC10543966.
   PubMed Web of Science ®Google Scholar