Silencing Glypican-1 enhances the antitumor effects of Pictilisib via downregulating PI3K/Akt/ERK signaling in chemo-resistant esophageal adenocarcinoma

References

• Uhlenhopp DJ, Then EO, Sunkara T, Gaduputi V. Epidemiology of esophageal cancer: update in global trends, etiology and risk factors. Clin J Gastroenterol. 2020;13(6):1010–21. 2020/12/01. doi:10.1007/s12328-020-01237-x.
   PubMed Web of Science ®Google Scholar
• Neishaboori N, Wadhwa R, Nogueras-González GM, Elimova E, Shiozaki H, Sudo K, Charalampakis N, Hiremath A, Lee JH, Bhutani MS, et al. Distribution of resistant esophageal adenocarcinoma in the resected specimens of clinical stage iii patients after chemoradiation: its clinical implications. Oncology. 2015;89(2):65–69. doi:10.1159/000371889.
   PubMed Web of Science ®Google Scholar
• Mandard AM, Dalibard F, Mandard JC, Marnay J, Henry-Amar M, Petiot J-F, Roussel A, Jacob J-H, Segol P, Samama G, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer. 1994 Jun 1;73(11):2680–2686. doi:10.1002/1097-0142(19940601)73:11<2680:AID-CNCR2820731105>3.0.CO;2-C.
   PubMed Web of Science ®Google Scholar
• Fiocca R, Mastracci L, Lugaresi M, Grillo F, D’Errico A, Malvi D, Spaggiari P, Tomezzoli A, Albarello L, Ristimäki A, et al. The prognostic impact of histology in esophageal and esophago-gastric junction adenocarcinoma. Cancers. 2021;13(20):5211. doi:10.3390/cancers13205211.
   PubMed Web of Science ®Google Scholar
• van Nistelrooij AMJ, van Marion R, Koppert LB, van Nistelrooij AMJ, van Marion R, Biermann K, Spaander MCW, Tilanus HW, van Lanschot JJB, Wijnhoven BPL, et al. Molecular clonality analysis of esophageal adenocarcinoma by multiregion sequencing of tumor samples. BMC Res Notes. 2017;10(1):144. 2017/04/04. doi:10.1186/s13104-017-2456-5.
   PubMedGoogle Scholar
• Samuels Y, Waldman T. Oncogenic mutations of PIK3CA in human cancers. Curr Top Microbiol Immunol. 2010;347:21–41. doi:10.1007/82_2010_68.
   PubMed Web of Science ®Google Scholar
• Tasioudi KE, Sakellariou S, Levidou G, Theodorou D, Michalopoulos NV, Patsouris E, Korkolopoulou P, Saetta AA. Immunohistochemical and molecular analysis of PI3K/AKT/mTOR pathway in esophageal carcinoma. APMIS. 2015;123(8):639–647. doi:10.1111/apm.12398.
   PubMed Web of Science ®Google Scholar
• Wang W-F, Xie Y, Zhou Z-H, Qin Z-H, Wu J-C, He J-K. PIK3CA hypomethylation plays a key role in activation of the PI3K/AKT pathway in esophageal cancer in Chinese patients. Acta Pharmacol Sin. 2013;34(12):1560–1567. 2013/12/01. doi:10.1038/aps.2013.163.
   PubMed Web of Science ®Google Scholar
• Janku F, Yap TA, Meric-Bernstam F. Targeting the PI3K pathway in cancer: are we making headway? Nat Rev Clin Oncol. 2018 May;15(5):273–291. doi:10.1038/nrclinonc.2018.28.
   PubMed Web of Science ®Google Scholar
• Vansteenkiste JF, Canon JL, De Braud F, Grossi F, De Pas T, Gray JE, Su W-C, Felip E, Yoshioka H, Gridelli C, et al. Safety and efficacy of buparlisib (BKM120) in patients with PI3K pathway-activated non-small cell lung cancer: results from the phase II BASALT-1study. J Thorac Oncol. 2015 Sep;10(9):1319–1327. doi:10.1097/jto.0000000000000607.
   PubMed Web of Science ®Google Scholar
• Bedard PL, Tabernero J, Janku F, Wainberg ZA, Paz-Ares L, Vansteenkiste J, Van Cutsem E, Pérez-García J, Stathis A, Britten CD, et al. A phase Ib dose-escalation study of the oral pan-PI3K inhibitor buparlisib (BKM120) in combination with the oral MEK1/2 inhibitor trametinib (GSK1120212) in patients with selected advanced solid tumors. Clin Cancer Res. Feb 15 2015;21(4):730–738. doi:10.1158/1078-0432.Ccr-14-1814.
   PubMed Web of Science ®Google Scholar
• Hong DS, Bowles DW, Falchook GS, Messersmith WA, George GC, O’Bryant CL, Vo ACH, Klucher K, Herbst RS, Eckhardt SG, et al. A multicenter phase I trial of PX-866, an oral irreversible phosphatidylinositol 3-kinase inhibitor, in patients with advanced solid tumors. Clin Cancer Res. Aug 1 2012;18(15):4173–4182. doi:10.1158/1078-0432.Ccr-12-0714.
   PubMed Web of Science ®Google Scholar
• Sarker D, Ang JE, Baird R, Kristeleit R, Shah K, Moreno V, Clarke PA, Raynaud FI, Levy G, Ware JA, et al. First-in-human phase i study of pictilisib (GDC-0941), a potent pan–class i phosphatidylinositol-3-Kinase (PI3K) inhibitor, in patients with advanced solid tumors. Clin Cancer Res. Jan 1 2015;21(1):77–86. doi:10.1158/1078-0432.Ccr-14-0947.
   PubMed Web of Science ®Google Scholar
• Vuylsteke P, Huizing M, Petrakova K, Roylance R, Laing R, Chan S, Abell F, Gendreau S, Rooney I, Apt D, et al. Pictilisib PI3Kinase inhibitor (a phosphatidylinositol 3-kinase [PI3K] inhibitor) plus paclitaxel for the treatment of hormone receptor-positive, HER2-negative, locally recurrent, or metastatic breast cancer: interim analysis of the multicentre, placebo-controlled, phase II randomised PEGGY study. Ann Oncol. 2016 Nov;27(11):2059–2066. doi:10.1093/annonc/mdw320.
   PubMed Web of Science ®Google Scholar
• Janku F, Hong DS, Fu S, Piha-Paul S, Naing A, Falchook G, Tsimberidou A, Stepanek V, Moulder S, Lee J&, et al. Assessing PIK3CA and PTEN in early-phase trials with PI3K/AKT/mTOR inhibitors. Cell Rep. Jan 30 2014;6(2):377–387. doi:10.1016/j.celrep.2013.12.035.
   PubMed Web of Science ®Google Scholar
• Chappell WH, Steelman LS, Long JM, Kempf RC, Abrams SL, Franklin RA, Bäsecke J, Stivala F, Donia M, Fagone P, et al. Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget. 2011 Mar;2(3):135–164. doi:10.18632/oncotarget.240.
   PubMedGoogle Scholar
• Gagliato D, Gonzalez-Angulo AM. Targeting multiple pathways in breast cancer. Breast Cancer Manag. 2014;3(1):87–101. doi:10.2217/bmt.13.66.
   Google Scholar
• Pratap A, Li A, Westbrook L, Gergen AK, Mitra S, Chauhan A, Cheng L, Weyant MJ, McCarter M, Wani S, et al. Glypican 1 promotes proliferation and migration in esophagogastric adenocarcinoma via activating AKT/GSK/β-catenin pathway. J Gastrointest Oncol. 2022 Oct;13(5):2082–2104. doi:10.21037/jgo-22-240.
   PubMed Web of Science ®Google Scholar
• Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. Jul 1 2011;3(7):a004952–a004952. doi:10.1101/cshperspect.a004952.
   PubMed Web of Science ®Google Scholar
• Aikawa T, Whipple CA, Lopez ME, Gunn J, Young A, Lander AD, Korc M. Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J Clin Invest. 2008 Jan;118(1):89–99. doi:10.1172/jci32412.
   PubMed Web of Science ®Google Scholar
• Matsuda K, Maruyama H, Guo F, Kleeff J, Itakura J, Matsumoto Y, Lander AD, Korc M. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. Jul 15 2001;61(14):5562–5569.
   PubMed Web of Science ®Google Scholar
• Hara H, Takahashi T, Serada S, Fujimoto M, Ohkawara T, Nakatsuka R, Harada E, Nishigaki T, Takahashi Y, Nojima S, et al. Overexpression of glypican-1 implicates poor prognosis and their chemoresistance in oesophageal squamous cell carcinoma. Br J Cancer. Jun 28 2016;115(1):66–75. doi:10.1038/bjc.2016.183.
   PubMed Web of Science ®Google Scholar
• Saito T, Sugiyama K, Hama S, Yamasaki F, Takayasu T, Nosaka R, Onishi S, Muragaki Y, Kawamata T, Kurisu K, et al. High expression of glypican-1 predicts dissemination and poor prognosis in glioblastomas. World Neurosurg. 2017 Sep;105:282–288. doi:10.1016/j.wneu.2017.05.165.
   PubMed Web of Science ®Google Scholar
• Duan L, Hu XQ, Feng DY, Lei SY, Hu GH. GPC-1 may serve as a predictor of perineural invasion and a prognosticator of survival in pancreatic cancer. Asian J Surg. 2013 Jan;36(1):7–12. doi:10.1016/j.asjsur.2012.08.001.
   PubMed Web of Science ®Google Scholar
• Yokota K, Serada S, Tsujii S, Toya K, Takahashi T, Matsunaga T, Fujimoto M, Uemura S, Namikawa T, Murakami I, et al. Anti-glypican-1 antibody–drug conjugate as potential therapy against tumor cells and tumor vasculature for glypican-1–positive cholangiocarcinoma. Mol Cancer Ther. 2021;20(9):1713–1722. doi:10.1158/1535-7163.Mct-21-0015.
   PubMed Web of Science ®Google Scholar
• Tsujii S, Serada S, Fujimoto M, Uemura S, Namikawa T, Nomura T, Murakami I, Hanazaki K, Naka T. Glypican-1 is a novel target for stroma and tumor cell dual-targeting antibody–drug conjugates in pancreatic cancer. Mol Cancer Ther. 2021;20(12):2495–2505. doi:10.1158/1535-7163.Mct-21-0335.
   PubMed Web of Science ®Google Scholar
• Ajani JA, D’Amico TA, Bentrem DJ, Chao J, Corvera C, Das P, Denlinger CS, Enzinger PC, Fanta P, Farjah F, et al. Esophageal and esophagogastric junction cancers, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. Jul 1 2019;17(7):855–883. doi:10.6004/jnccn.2019.0033.
   PubMed Web of Science ®Google Scholar
• Salem ME, Puccini A, Xiu J, Raghavan D, Lenz H-J, Korn WM, Shields AF, Philip PA, Marshall JL, Goldberg RM, et al. Comparative molecular analyses of esophageal squamous cell carcinoma, esophageal adenocarcinoma, and gastric adenocarcinoma. Oncologist. 2018;23(11):1319–1327. doi:10.1634/theoncologist.2018-0143.
   PubMed Web of Science ®Google Scholar
• Miller HE, Bishop AJR. Correlation AnalyzeR: functional predictions from gene co-expression correlations. BMC Bioinform. 2021;22(1):206. 2021/04/20. doi:10.1186/s12859-021-04130-7.
   PubMed Web of Science ®Google Scholar
• Sathe A, Chalaud G, Oppolzer I, Wong KY, von Busch M, Schmid SC, Tong Z, Retz M, Gschwend JE, Schulz WA, et al. Parallel PI3K, AKT and mTOR inhibition is required to control feedback loops that limit tumor therapy. PLoS One. 2018;13(1):e0190854. doi:10.1371/journal.pone.0190854.
   PubMed Web of Science ®Google Scholar
• Fumarola C, Bonelli MA, Petronini PG, Alfieri RR. Targeting PI3K/AKT/mTOR pathway in non small cell lung cancer. Biochem Pharmacol. Aug 1 2014;90(3):197–207. doi:10.1016/j.bcp.2014.05.011.
   PubMed Web of Science ®Google Scholar
• Song M, Bode AM, Dong Z, Lee M-H. AKT as a therapeutic target for cancer. Cancer Res. 2019;79(6):1019–1031. doi:10.1158/0008-5472.Can-18-2738.
   PubMed Web of Science ®Google Scholar
• Castel P, Toska E, Zumsteg ZS, Carmona FJ, Elkabets M, Bosch A, Scaltriti M. Rationale-based therapeutic combinations with PI3K inhibitors in cancer treatment. Mol Cell Oncol. 2014 Jul-Sep;1(3):e963447. doi:10.4161/23723548.2014.963447.
   PubMedGoogle Scholar
• Wang S, Qiu Y, Bai B. The expression, regulation, and biomarker potential of glypican-1 in cancer. Front Oncol. 2019;9:614. doi:10.3389/fonc.2019.00614.
   PubMed Web of Science ®Google Scholar
• Pan J, Ho M. Role of glypican-1 in regulating multiple cellular signaling pathways. Am J Physiol Cell Physiol. Nov 1 2021;321(5):C846–c858. doi:10.1152/ajpcell.00290.2021.
   PubMed Web of Science ®Google Scholar
• Lu F, Chen S, Shi W, Su X, Wu H, Liu M, Montazeri Aliabadi H. GPC1 promotes the growth and migration of colorectal cancer cells through regulating the TGF-β1/SMAD2 signaling pathway. PLoS One. 2022;17(6):e0269094. doi:10.1371/journal.pone.0269094.
   PubMed Web of Science ®Google Scholar
• Jeong SJ, Dasgupta A, Jung KJ, Um J-H, Burke A, Park HU, Brady JN. PI3K/AKT inhibition induces caspase-dependent apoptosis in HTLV-1-transformed cells. Virology. Jan 20 2008;370(2):264–272. doi:10.1016/j.virol.2007.09.003.
   PubMed Web of Science ®Google Scholar
• Khalafi S, Zhu S, Khurana R, Lohse I, Giordano S, Corso S, Al-Ali H, Brothers SP, Wahlestedt C, Schürer S, et al., A novel strategy for combination of clofarabine and pictilisib is synergistic in gastric cancer, Transl Oncol. 2022;15(1):101260. 01/1/2022. doi:10.1016/j.tranon.2021.101260.
   PubMed Web of Science ®Google Scholar
• Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014 Mar;15(3):178–196. doi:10.1038/nrm3758.
   PubMed Web of Science ®Google Scholar