GPR50 Promotes Hepatocellular Carcinoma Progression via the Notch Signaling Pathway through Direct Interaction with ADAM17

Bray, 2018, Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries, CA Cancer J. Clin., 68, 394, 10.3322/caac.21492 Kabbach, 2015, Hepatobiliary Tumors: Update on Diagnosis and Management, J. Clin. Transl. Hepatol., 3, 169, 10.14218/JCTH.2015.00012 Chu, 2015, Update in management of hepatocellular carcinoma in Eastern population, World J. Hepatol., 7, 1562, 10.4254/wjh.v7.i11.1562 Shao, 2015, Treatment efficacy differences of sorafenib for advanced hepatocellular carcinoma: a meta-analysis of randomized clinical trials, Oncology, 88, 345, 10.1159/000369559 Kitano, 2012, Outcome and survival analysis of pulmonary metastasectomy for hepatocellular carcinoma, Eur. J. Cardiothorac. Surg., 41, 376, 10.1016/j.ejcts.2011.05.052 Li, 2011, Risk factors, prognosis, and management of early and late intrahepatic recurrence after resection of primary clear cell carcinoma of the liver, Ann. Surg. Oncol., 18, 1955, 10.1245/s10434-010-1540-z Rask-Andersen, 2011, Trends in the exploitation of novel drug targets, Nat. Rev. Drug Discov., 10, 579, 10.1038/nrd3478 Spiegelberg, 2007, Roles of G-protein-coupled receptor signaling in cancer biology and gene transcription, Curr. Opin. Genet. Dev., 17, 40, 10.1016/j.gde.2006.12.002 Thomas, 2006, Cross-talk between G protein-coupled receptor and epidermal growth factor receptor signaling pathways contributes to growth and invasion of head and neck squamous cell carcinoma, Cancer Res., 66, 11831, 10.1158/0008-5472.CAN-06-2876 Ahmad, 2015, Hunting for the function of orphan GPCRs - beyond the search for the endogenous ligand, Br. J. Pharmacol., 172, 3212, 10.1111/bph.12942 Levoye, 2006, Do orphan G-protein-coupled receptors have ligand-independent functions? New insights from receptor heterodimers, EMBO Rep., 7, 1094, 10.1038/sj.embor.7400838 Rezgaoui, 2006, The neuropeptide head activator is a high-affinity ligand for the orphan G-protein-coupled receptor GPR37, J. Cell Sci., 119, 542, 10.1242/jcs.02766 Ito, 2009, Anatomical and histological profiling of orphan G-protein-coupled receptor expression in gastrointestinal tract of C57BL/6J mice, Cell Tissue Res., 338, 257, 10.1007/s00441-009-0859-x Khalil, 2016, GPCR Signaling Mediates Tumor Metastasis via PI3Kβ, Cancer Res., 76, 2944, 10.1158/0008-5472.CAN-15-1675 Herr, 2012, Potential use of G protein-coupled receptor-blocking monoclonal antibodies as therapeutic agents for cancers, Int. Rev. Cell Mol. Biol., 297, 45, 10.1016/B978-0-12-394308-8.00002-9 Dorsam, 2007, G-protein-coupled receptors and cancer, Nat. Rev. Cancer, 7, 79, 10.1038/nrc2069 Tang, 2013, GPR116, an adhesion G-protein-coupled receptor, promotes breast cancer metastasis via the Gαq-p63RhoGEF-Rho GTPase pathway, Cancer Res., 73, 6206, 10.1158/0008-5472.CAN-13-1049 Feigin, 2014, G-protein-coupled receptor GPR161 is overexpressed in breast cancer and is a promoter of cell proliferation and invasion, Proc. Natl. Acad. Sci. USA, 111, 4191, 10.1073/pnas.1320239111 Dufourny, 2008, GPR50 is the mammalian ortholog of Mel1c: evidence of rapid evolution in mammals, BMC Evol. Biol., 8, 105, 10.1186/1471-2148-8-105 Jockers, 2016, Update on melatonin receptors: IUPHAR Review 20, Br. J. Pharmacol., 173, 2702, 10.1111/bph.13536 Thomson, 2005, Sex-specific association between bipolar affective disorder in women and GPR50, an X-linked orphan G protein-coupled receptor, Mol. Psychiatry, 10, 470, 10.1038/sj.mp.4001593 Bechtold, 2012, A role for the melatonin-related receptor GPR50 in leptin signaling, adaptive thermogenesis, and torpor, Curr. Biol., 22, 70, 10.1016/j.cub.2011.11.043 Anyanwu, 2014 Grünewald, 2009, GPR50 interacts with neuronal NOGO-A and affects neurite outgrowth, Mol. Cell. Neurosci., 42, 363, 10.1016/j.mcn.2009.08.007 Khan, 2016, The emerging role of GPR50 receptor in brain, Biomed. Pharmacother., 78, 121, 10.1016/j.biopha.2016.01.003 Choi, 2015, G protein-coupled receptors in stem cell maintenance and somatic reprogramming to pluripotent or cancer stem cells, BMB Rep., 48, 68, 10.5483/BMBRep.2015.48.2.250 Wojciech, 2018, The orphan GPR50 receptor promotes constitutive TGFβ receptor signaling and protects against cancer development, Nat. Commun., 9, 1216, 10.1038/s41467-018-03609-x Ahmad, 2018 Zhan, 2017, Wnt signaling in cancer, Oncogene, 36, 1461, 10.1038/onc.2016.304 Venkatesh, 2018, Targeting Notch signalling pathway of cancer stem cells, Stem Cell Investig., 5, 5, 10.21037/sci.2018.02.02 Sari, 2018, Hedgehog Signaling in Cancer: A Prospective Therapeutic Target for Eradicating Cancer Stem Cells, Cells, 7, 208, 10.3390/cells7110208 Hanna, 2016, Hedgehog signaling: modulation of cancer properies and tumor mircroenvironment, Mol. Cancer, 15, 24, 10.1186/s12943-016-0509-3 Park, 2018, The Role of Hippo Pathway in Cancer Stem Cell Biology, Mol. Cells, 41, 83 Lu, 2013, Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1, Cancer Cell, 23, 171, 10.1016/j.ccr.2012.12.021 Ladi, 2005, The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands, J. Cell Biol., 170, 983, 10.1083/jcb.200503113 Mullendore, 2009, Ligand-dependent Notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer, Clin. Cancer Res., 15, 2291, 10.1158/1078-0432.CCR-08-2004 Bozkulak, 2009, Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling, Mol. Cell. Biol., 29, 5679, 10.1128/MCB.00406-09 Li, 2019, ADAM17 promotes lymph node metastasis in gastric cancer via activation of the Notch and Wnt signaling pathways, Int. J. Mol. Med., 43, 914 Guo, 2013, Inhibition of ADAM-17 more effectively down-regulates the Notch pathway than that of γ-secretase in renal carcinoma, J. Exp. Clin. Cancer Res., 32, 26, 10.1186/1756-9966-32-26 Jing, 2016, MicroR-140-5p suppresses tumor cell migration and invasion by targeting ADAM10-mediated Notch1 signaling pathway in hypopharyngeal squamous cell carcinoma, Exp. Mol. Pathol., 100, 132, 10.1016/j.yexmp.2015.12.008 Zolkiewska, 2008, ADAM proteases: ligand processing and modulation of the Notch pathway, Cell. Mol. Life Sci., 65, 2056, 10.1007/s00018-008-7586-4 Liu, 2012, Suppression of Akt/Foxp3-mediated miR-183 expression blocks Sp1-mediated ADAM17 expression and TNFα-mediated NFκB activation in piceatannol-treated human leukemia U937 cells, Biochem. Pharmacol., 84, 670, 10.1016/j.bcp.2012.06.007 Van Schaeybroeck, 2014, ADAM17-dependent c-MET-STAT3 signaling mediates resistance to MEK inhibitors in KRAS mutant colorectal cancer, Cell Rep., 7, 1940, 10.1016/j.celrep.2014.05.032 Yamashita, 2009, Activation of PKA, p38 MAPK and ERK1/2 by gonadotropins in cumulus cells is critical for induction of EGF-like factor and TACE/ADAM17 gene expression during in vitro maturation of porcine COCs, J. Ovarian Res., 2, 20, 10.1186/1757-2215-2-20 Wang, 2013, Mutual interaction between YAP and CREB promotes tumorigenesis in liver cancer, Hepatology, 58, 1011, 10.1002/hep.26420 Mizui, 1999, cDNA cloning of mouse tumor necrosis factor-alpha converting enzyme (TACE) and partial analysis of its promoter, Gene, 233, 67, 10.1016/S0378-1119(99)00155-9 Szalad, 2009, Transcription factor Sp1 induces ADAM17 and contributes to tumor cell invasiveness under hypoxia, J. Exp. Clin. Cancer Res., 28, 129, 10.1186/1756-9966-28-129 Artavanis-Tsakonas, 2010, Notch: the past, the present, and the future, Curr. Top. Dev. Biol., 92, 1, 10.1016/S0070-2153(10)92001-2 Tang, 2016, Tetracyclines increase lipid phosphate phosphatase expression on plasma membranes and turnover of plasma lysophosphatidate, J. Lipid Res., 57, 597, 10.1194/jlr.M065086 Xing, 2011, Hypoxia-induced Jagged2 promotes breast cancer metastasis and self-renewal of cancer stem-like cells, Oncogene, 30, 4075, 10.1038/onc.2011.122 Li, 2011, GPR50 interacts with TIP60 to modulate glucocorticoid receptor signalling, PLoS ONE, 6, e23725, 10.1371/journal.pone.0023725 Levoye, 2006, The orphan GPR50 receptor specifically inhibits MT1 melatonin receptor function through heterodimerization, EMBO J., 25, 3012, 10.1038/sj.emboj.7601193 Kopan, 2009, The canonical Notch signaling pathway: unfolding the activation mechanism, Cell, 137, 216, 10.1016/j.cell.2009.03.045 Fortini, 2009, Notch signaling: the core pathway and its posttranslational regulation, Dev. Cell, 16, 633, 10.1016/j.devcel.2009.03.010 Bigas, 2016, Notch Signaling in Cell–Cell Communication Pathways, Curr. Stem Cell Rep., 2, 349, 10.1007/s40778-016-0065-1 Gan, 2018, Notch1 regulates tongue cancer cells proliferation, apoptosis and invasion, Cell Cycle, 17, 216, 10.1080/15384101.2017.1395534 Lai, 2018, Interference of Notch 1 inhibits the proliferation and invasion of breast cancer cells: Involvement of the β-catenin signaling pathway, Mol. Med. Rep., 17, 2472 Aster, 2017, The Varied Roles of Notch in Cancer, Annu. Rev. Pathol., 12, 245, 10.1146/annurev-pathol-052016-100127 Ntziachristos, 2014, From fly wings to targeted cancer therapies: a centennial for notch signaling, Cancer Cell, 25, 318, 10.1016/j.ccr.2014.02.018 Nowell, 2017, Notch as a tumour suppressor, Nat. Rev. Cancer, 17, 145, 10.1038/nrc.2016.145 Lu, 2016, Oncogenic role of the Notch pathway in primary liver cancer, Oncol. Lett., 12, 3, 10.3892/ol.2016.4609 Villanueva, 2012, Notch signaling is activated in human hepatocellular carcinoma and induces tumor formation in mice, Gastroenterology, 143, 1660, 10.1053/j.gastro.2012.09.002 Seals, 2003, The ADAMs family of metalloproteases: multidomain proteins with multiple functions, Genes Dev., 17, 7, 10.1101/gad.1039703 Edwards, 2008, The ADAM metalloproteinases, Mol. Aspects Med., 29, 258, 10.1016/j.mam.2008.08.001 Rocks, 2008, Emerging roles of ADAM and ADAMTS metalloproteinases in cancer, Biochimie, 90, 369, 10.1016/j.biochi.2007.08.008 Mazzocca, 2010, Involvement of ADAMs in tumorigenesis and progression of hepatocellular carcinoma: Is it merely fortuitous or a real pathogenic link?, Biochim. Biophys. Acta, 1806, 74 Le Gall, 2009, ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha, Mol. Biol. Cell, 20, 1785, 10.1091/mbc.e08-11-1135 Lorenzen, 2011, Multimerisation of A disintegrin and metalloprotease protein-17 (ADAM17) is mediated by its EGF-like domain, Biochem. Biophys. Res. Commun., 415, 330, 10.1016/j.bbrc.2011.10.056 González-Foruria, 2017, Dysregulation of the ADAM17/Notch signalling pathways in endometriosis: from oxidative stress to fibrosis, Mol. Hum. Reprod., 23, 488, 10.1093/molehr/gax028 van Tetering, 2009, Metalloprotease ADAM10 is required for Notch1 site 2 cleavage, J. Biol. Chem., 284, 31018, 10.1074/jbc.M109.006775 Inoue, 2012, TGFα shedding assay: an accurate and versatile method for detecting GPCR activation, Nat. Methods, 9, 1021, 10.1038/nmeth.2172 Sokolina, 2017, Systematic protein-protein interaction mapping for clinically relevant human GPCRs, Mol. Syst. Biol., 13, 918, 10.15252/msb.20167430 Höcker, 1998, Sp1 and CREB mediate gastrin-dependent regulation of chromogranin A promoter activity in gastric carcinoma cells, J. Biol. Chem., 273, 34000, 10.1074/jbc.273.51.34000 Li, 2004, Gene regulation by Sp1 and Sp3, Biochem. Cell Biol., 82, 460, 10.1139/o04-045 Wang, 2008, Targeted inhibition of Sp1-mediated transcription for antiangiogenic therapy of metastatic human gastric cancer in orthotopic nude mouse models, Int. J. Oncol., 33, 161 Wang, 2007, [Expression of transcription factor Sp1 in human gastric cancer tissue and its correlation with prognosis], Zhonghua Zhong Liu Za Zhi, 29, 107 Pore, 2004, Sp1 is involved in Akt-mediated induction of VEGF expression through an HIF-1-independent mechanism, Mol. Biol. Cell, 15, 4841, 10.1091/mbc.e04-05-0374 Chuang, 2013, Cyclooxygenase-2 up-regulates CCR7 expression via AKT-mediated phosphorylation and activation of Sp1 in breast cancer cells, J. Cell. Physiol., 228, 341, 10.1002/jcp.24136 Chang, 2013, Fibroblast growth factor-2 up-regulates the expression of nestin through the Ras-Raf-ERK-Sp1 signaling axis in C6 glioma cells, Biochem. Biophys. Res. Commun., 434, 854, 10.1016/j.bbrc.2013.04.031 Hu, 2017, Elevated COX-2 Expression Promotes Angiogenesis Through EGFR/p38-MAPK/Sp1-Dependent Signalling in Pancreatic Cancer, Sci. Rep., 7, 470, 10.1038/s41598-017-00288-4 Liu, 2017, The cellular senescence of leukemia-initiating cells from acute lymphoblastic leukemia is postponed by β-Arrestin1 binding with P300-Sp1 to regulate hTERT transcription, Cell Death Dis., 8, e2756, 10.1038/cddis.2017.164 Rhodes, 2004, ONCOMINE: a cancer microarray database and integrated data-mining platform, Neoplasia, 6, 1, 10.1016/S1476-5586(04)80047-2 Rhodes, 2007, Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles, Neoplasia, 9, 166, 10.1593/neo.07112 Clough, 2016, The Gene Expression Omnibus Database, Methods Mol. Biol., 1418, 93, 10.1007/978-1-4939-3578-9_5 Aguirre-Gamboa, 2013, SurvExpress: an online biomarker validation tool and database for cancer gene expression data using survival analysis, PLoS ONE, 8, e74250, 10.1371/journal.pone.0074250 Cerami, 2012, The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data, Cancer Discov., 2, 401, 10.1158/2159-8290.CD-12-0095 Gao, 2013, Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal, Sci. Signal., 6, pl1, 10.1126/scisignal.2004088 Liu, 2009, TACE-mediated ectodomain shedding of the type I TGF-β receptor downregulates TGF-β signaling, Mol. Cell, 35, 26, 10.1016/j.molcel.2009.06.018 Li, 2012 Saha, 2017, KRT19 directly interacts with β-catenin/RAC1 complex to regulate NUMB-dependent NOTCH signaling pathway and breast cancer properties, Oncogene, 36, 332, 10.1038/onc.2016.221 Salmon, 2007, Production and Titration of Lentiviral Vectors, Curr. Protoc. Human Genet., Chapter 12 Nasri, 2014, Production, purification and titration of a lentivirus-based vector for gene delivery purposes, Cytotechnology, 66, 1031, 10.1007/s10616-013-9652-5 Saha, 2018, Cytokeratin 19 (KRT19) has a Role in the Reprogramming of Cancer Stem Cell-Like Cells to Less Aggressive and More Drug-Sensitive Cells, Int. J. Mol. Sci., 19, 1423, 10.3390/ijms19051423 Saha, 2019, Opposing Regulation of Cancer Properties via KRT19-Mediated Differential Modulation of Wnt/β-Catenin/Notch Signaling in Breast and Colon Cancers, Cancers (Basel), 11, 99, 10.3390/cancers11010099 Saha, 2017, Valproic Acid Induces Endocytosis-Mediated Doxorubicin Internalization and Shows Synergistic Cytotoxic Effects in Hepatocellular Carcinoma Cells, Int. J. Mol. Sci., 18, 1048, 10.3390/ijms18051048 Lee, 2010, RORalpha attenuates Wnt/β-catenin signaling by PKCalpha-dependent phosphorylation in colon cancer, Mol. Cell, 37, 183, 10.1016/j.molcel.2009.12.022 Wang, 2015, Combining detection of Notch1 and tumor necrosis factor-α converting enzyme is a reliable biomarker for the diagnosis of abdominal aortic aneurysms, Life Sci., 127, 39, 10.1016/j.lfs.2015.02.009