Docking protein-1 promotes inflammatory macrophage signaling in gastric cancer

References

• Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. GLOBOCAN 2012 v1.0, cancer incidence and mortality worldwide: IARC CANCERBASE No. 11 [Internet]. Lyon (France): International Agency for Research on Cancer; 2013. http://globocan.iarc.fr.
   Google Scholar
• Lordick F, Janjigian YY. Clinical impact of tumour biology in the management of gastroesophageal cancer. Nat Rev Clin Oncol. 2016;13:1–18. doi:10.1038/nrclinonc.2016.15.
   PubMed Web of Science ®Google Scholar
• Shaib WL, Nammour JP, Gill H, Mody M, Saba NF. The future prospects of immune therapy in gastric and esophageal Adenocarcinoma. J Clin Med. 2016;5. doi:10.3390/jcm5110100.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research, N. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–209. doi:10.1038/nature13480.
   PubMed Web of Science ®Google Scholar
• Cassetta L, Pollard JW. Targeting macrophages: therapeutic approaches in cancer. Nat Rev Drug Discov. 2018;17:887–904. doi:10.1038/nrd.2018.169.
   PubMed Web of Science ®Google Scholar
• Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41:14–20. doi:10.1016/j.immuni.2014.06.008.
   PubMed Web of Science ®Google Scholar
• Yuan G, Regel I, Lian F, Friedrich T, Hitkova I, Hofheinz RD, Ströbel P, Langer R, Keller G, Röcken C, et al. WNT6 is a novel target gene of caveolin-1 promoting chemoresistance to epirubicin in human gastric cancer cells. Oncogene. 2013;32:375–387. doi:10.1038/onc.2012.40.
   PubMed Web of Science ®Google Scholar
• Burgermeister E, Friedrich T, Hitkova I, Regel I, Einwächter H, Zimmermann W, Röcken C, Perren A, Wright MB, Schmid RM, et al. The Ras inhibitors caveolin-1 and docking protein 1 activate peroxisome proliferator-activated receptor gamma through spatial relocalization at helix 7 of its ligand-binding domain. Mol Cell Biol. 2011;31:3497–3510. doi:10.1128/MCB.01421-10.
   PubMed Web of Science ®Google Scholar
• Mashima R, Hishida Y, Tezuka T, Yamanashi Y. The roles of Dok family adapters in immunoreceptor signaling. Immunol Rev. 2009;232:273–285. doi:10.1111/j.1600-065X.2009.00844.x.
   PubMed Web of Science ®Google Scholar
• Friedrich T, Söhn M, Gutting T, Janssen K-P, Behrens H-M, Röcken C, Ebert MPA, Burgermeister E. Subcellular compartmentalization of docking protein-1 contributes to progression in colorectal cancer. EBioMedicine. 2016;8:159–172. doi:10.1016/j.ebiom.2016.05.003.
   PubMed Web of Science ®Google Scholar
• Sylla BS, Murphy K, Cahir-McFarland E, Lane WS, Mosialos G, Kieff E. The X-linked lymphoproliferative syndrome gene product SH2D1A associates with p62dok (Dok1) and activates NF-kappa B. Proc Natl Acad Sci U S A. 2000;97:7470–7475. doi:10.1073/pnas.130193097.
   PubMed Web of Science ®Google Scholar
• Hosooka T, Noguchi T, Kotani K, Nakamura T, Sakaue H, Inoue H, Ogawa W, Tobimatsu K, Takazawa K, Sakai M, et al. Dok1 mediates high-fat diet-induced adipocyte hypertrophy and obesity through modulation of PPAR-gamma phosphorylation. Nat Med. 2008;14:188–193. doi:10.1038/nm1706.
   PubMed Web of Science ®Google Scholar
• Balassiano K, Lima S, Jenab M, Overvad K, Tjonneland A, Boutron-Ruault MC, Clavel-Chapelon F, Canzian F, Kaaks R, Boeing H, et al. Aberrant DNA methylation of cancer-associated genes in gastric cancer in the European prospective investigation into cancer and nutrition (EPIC-EURGAST). Cancer Lett. 2011;311:85–95. doi:10.1016/j.canlet.2011.06.038.
   PubMed Web of Science ®Google Scholar
• Mashima R, Honda K, Yang Y, Morita Y, Inoue A, Arimura S, Nishina H, Ema H, Nakauchi H, Seed B, et al. Mice lacking Dok-1, Dok-2, and Dok-3 succumb to aggressive histiocytic sarcoma. Lab Invest. 2010;90:1357–1364. doi:10.1038/labinvest.2010.121.
   PubMed Web of Science ®Google Scholar
• Lamkin TJ, Chin V, Yen A. All-trans retinoic acid induces p62DOK1 and p56DOK2 expression which enhances induced differentiation and G0 arrest of HL-60 leukemia cells. Am J Hematol. 2006;81:603–615. doi:10.1002/ajh.20667.
   PubMed Web of Science ®Google Scholar
• Hiragun T, Peng Z, Beaven MA. Dexamethasone up-regulates the inhibitory adaptor protein Dok-1 and suppresses downstream activation of the mitogen-activated protein kinase pathway in antigen-stimulated RBL-2H3 mast cells. Mol Pharmacol. 2005;67:598–603. doi:10.1124/mol.104.008607.
   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;2:401–404. doi:10.1158/2159-8290.CD-12-0095.
   PubMed Web of Science ®Google Scholar
• Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, Dixon MF, Fenoglio-Preiser CM, Fléjou JF, Geboes K, et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000;47:251–255. doi:10.1136/gut.47.2.251.
   PubMed Web of Science ®Google Scholar
• Siouda M, Frecha C, Accardi R, Yue J, Cuenin C, Gruffat H, Manet E, Herceg Z, Sylla BS, Tommasino M, et al. Epstein-Barr virus down-regulates tumor suppressor DOK1 expression. PLoS Pathog. 2014;10:e1004125. doi:10.1371/journal.ppat.1004125.
   PubMed Web of Science ®Google Scholar
• Forbes SA, Beare D, Bindal N, Bamford S, Ward S, Cole CG, Jia M, Kok C, Boutselakis H, De T, et al. COSMIC: high-resolution cancer genetics using the catalogue of somatic mutations in cancer. Curr Protoc Hum Genet. 2016;91:10 11 11–10 11 37. doi:10.1002/cphg.21.
   PubMedGoogle Scholar
• Fels Elliott DR, Perner J, Li X, Symmons MF, Verstak B, Eldridge M, Bower L, O’Donovan M, Gay NJ, Fitzgerald RC, et al. Impact of mutations in Toll-like receptor pathway genes on esophageal carcinogenesis. PLoS Genet. 2017;13:e1006808. doi:10.1371/journal.pgen.1006808.
   PubMed Web of Science ®Google Scholar
• Chistiakov DA, Killingsworth MC, Myasoedova VA, Orekhov AN, Bobryshev YV. CD68/macrosialin: not just a histochemical marker. Lab Invest. 2017;97:4–13. doi:10.1038/labinvest.2016.116.
   PubMed Web of Science ®Google Scholar
• Vannini F, Kashfi K, Nath N. The dual role of iNOS in cancer. Redox Biol. 2015;6:334–343. doi:10.1016/j.redox.2015.08.009.
   PubMed Web of Science ®Google Scholar
• Spiller KL, Wrona EA, Romero-Torres S, Pallotta I, Graney PL, Witherel CE, Panicker LM, Feldman RA, Urbanska AM, Santambrogio L, et al. Differential gene expression in human, murine, and cell line-derived macrophages upon polarization. Exp Cell Res. 2016;347:1–13. doi:10.1016/j.yexcr.2015.10.017.
   PubMed Web of Science ®Google Scholar
• Gutting T, Weber CA, Weidner P, et al. PPARgamma-activation increases intestinal M1 macrophages and mitigates formation of serrated adenomas in mutant KRAS mice. Oncoimmunology. 2018;7:e1423168. doi:10.1080/2162402X.2018.1490854.
   PubMed Web of Science ®Google Scholar
• Castano-Rodriguez N, Kaakoush NO, Mitchell HM. Pattern-recognition receptors and gastric cancer. Front Immunol. 2014;5:336. doi: 10.3389/fimmu.2014.00336.
   PubMed Web of Science ®Google Scholar
• Garcia-Diaz A, Shin DS, Moreno BH, Saco J, Escuin-Ordinas H, Rodriguez GA, Zaretsky JM, Sun L, Hugo W, Wang X, et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 2017;19:1189–1201. doi:10.1016/j.celrep.2017.04.031.
   PubMed Web of Science ®Google Scholar
• An LL, Gorman JV, Stephens G, Swerdlow B, Warrener P, Bonnell J, Mustelin T, Fung M, Kolbeck R. Complement C5a induces PD-L1 expression and acts in synergy with LPS through Erk1/2 and JNK signaling pathways. Sci Rep. 2016;6:33346. doi:10.1038/srep33346.
   PubMed Web of Science ®Google Scholar
• Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, Gupta R, Tsai JM, Sinha R, Corey D, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 2017;545:495–499. doi:10.1038/nature22396.
   PubMed Web of Science ®Google Scholar
• Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehár J, Kryukov GV, Sonkin D, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483:603–607. doi:10.1038/nature11003.
   PubMed Web of Science ®Google Scholar
• Prost S, Relouzat F, Spentchian M, Ouzegdouh Y, Saliba J, Massonnet G, Beressi J-P, Verhoeyen E, Raggueneau V, Maneglier B, et al. Erosion of the chronic myeloid leukaemia stem cell pool by PPARgamma agonists. Nature. 2015;525:380–383. doi:10.1038/nature15248.
   PubMed Web of Science ®Google Scholar
• Guo B, Huang X, Lee MR, Lee SA, Broxmeyer HE. Antagonism of PPAR-gamma signaling expands human hematopoietic stem and progenitor cells by enhancing glycolysis. Nat Med. 2018;24:360–367. doi:10.1038/nm.4477.
   PubMed Web of Science ®Google Scholar
• Leong SH, Lwin KM, Lee SS, Ng WH, Ng KM, Tan SY, Ng BL, Carter NP, Tang C, Lian Kon O. Chromosomal breaks at FRA18C: association with reduced DOK6 expression, altered oncogenic signaling and increased gastric cancer survival. NPJ Precis Oncol. 2017;1:9. doi:10.1038/s41698-017-0012-3.
   PubMed Web of Science ®Google Scholar
• Miyagaki H, Yamasaki M, Takahashi T, Kurokawa Y, Miyata H, Nakajima K, Takiguchi S, Fujiwara Y, Mori M, Doki Y. DOK2 as a marker of poor prognosis of patients with gastric adenocarcinoma after curative resection. Ann Surg Oncol. 2012;19:1560–1567. doi:10.1245/s10434-011-2157-6.
   PubMed Web of Science ®Google Scholar
• Berger AH, Niki M, Morotti A, Taylor BS, Socci ND, Viale A, Brennan C, Szoke J, Motoi N, Rothman PB, et al. Identification of DOK genes as lung tumor suppressors. Nat Genet. 2010;42:216–223. doi:10.1038/ng.527.
   PubMed Web of Science ®Google Scholar
• Friedrich T, Richter B, Gaiser T, Weiss C, Janssen K-P, Einwächter H, Schmid RM, Ebert MPA, Burgermeister E. Deficiency of caveolin-1 in Apc(min/+) mice promotes colorectal tumorigenesis. Carcinogenesis. 2013;34:2109–2118. doi:10.1093/carcin/bgt142.
   PubMed Web of Science ®Google Scholar
• Lahmidi S, Strunk U, Smiley JR, Pearson A, Duplay P. Herpes simplex virus 1 infection of T cells causes VP11/12-dependent phosphorylation and degradation of the cellular protein Dok-2. Virology. 2017;511:66–73. doi:10.1016/j.virol.2017.08.018.
   PubMed Web of Science ®Google Scholar
• Janas JA, Van Aelst L. Oncogenic tyrosine kinases target Dok-1 for ubiquitin-mediated proteasomal degradation to promote cell transformation. Mol Cell Biol. 2011;31:2552–2565. doi:10.1128/MCB.05045-11.
   PubMed Web of Science ®Google Scholar
• Zhang QW, Liu L, Gong C-Y, Shi H-S, Zeng Y-H, Wang X-Z, Zhao Y-W, Wei Y-Q, Hoque MO. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One. 2012;7:e50946. doi:10.1371/journal.pone.0050946.
   PubMed Web of Science ®Google Scholar
• Pantano F, Berti P, Guida FM, Perrone G, Vincenzi B, Amato MMC, Righi D, Dell’aquila E, Graziano F, Catalano V, et al. The role of macrophages polarization in predicting prognosis of radically resected gastric cancer patients. J Cell Mol Med. 2013;17:1415–1421. doi:10.1111/jcmm.12109.
   PubMed Web of Science ®Google Scholar
• Zhang H, Wang X, Shen Z, Xu J, Qin J, Sun Y. Infiltration of diametrically polarized macrophages predicts overall survival of patients with gastric cancer after surgical resection. Gastric Cancer. 2015;18:740–750. doi:10.1007/s10120-014-0422-7.
   PubMed Web of Science ®Google Scholar
• Yamaguchi T, Fushida S, Yamamoto Y, Tsukada T, Kinoshita J, Oyama K, Miyashita T, Tajima H, Ninomiya I, Munesue S, et al. Tumor-associated macrophages of the M2 phenotype contribute to progression in gastric cancer with peritoneal dissemination. Gastric Cancer. 2016;19:1052–1065. doi:10.1007/s10120-015-0579-8.
   PubMed Web of Science ®Google Scholar
• Panda A, Mehnert JM, Hirshfield KM, Riedlinger G, Damare S, Saunders T, Kane M, Sokol L, Stein MN, Poplin E, et al. Immune activation and benefit from Avelumab in EBV-positive gastric cancer. J Natl Cancer Inst. 2018;110:316–320. doi:10.1093/jnci/djx213.
   PubMedGoogle Scholar
• Chang YH, Heo YJ, Cho J, Song SY, Lee J, Kim K-M. Computational measurement of tumor immune microenvironment in gastric adenocarcinomas. Sci Rep. 2018;8:13887. doi:10.1038/s41598-018-32299-0.
   PubMed Web of Science ®Google Scholar
• Kim ST, Cristescu R, Bass AJ, Kim K-M, Odegaard JI, Kim K, Liu XQ, Sher X, Jung H, Lee M, et al. Comprehensive molecular characterization of clinical responses to PD-1 inhibition in metastatic gastric cancer. Nat Med. 2018;24:1449–1458. doi:10.1038/s41591-018-0101-z.
   PubMed Web of Science ®Google Scholar
• Ayers M,Nebozhyn M, Cristescu R, McClanahan TK, Perini R, Rubin E, Cheng JD, Kaufman DR, Loboda AMolecular Profiling of Cohorts of Tumor Samples to Guide Clinical Development of Pembrolizum. ab as Monotherapy. Clin Cancer Res. 2019;25:1564–1573. doi: 10.1158/1078-0432.CCR-18-1316.
   PubMed Web of Science ®Google Scholar
• Waseda M, Arimura S, Shimura E, Nakae S, Yamanashi Y. Loss of Dok-1 and Dok-2 in mice causes severe experimental colitis accompanied by reduced expression of IL-17A and IL-22. Biochem Biophys Res Commun. 2016;478:135–142. doi:10.1016/j.bbrc.2016.07.079.
   PubMed Web of Science ®Google Scholar
• Yasuda T, Shirakata M, Iwama A, Ishii A, Ebihara Y, Osawa M, Honda K, Shinohara H, Sudo K, Tsuji K, Nakauchi H. Role of Dok-1 and Dok-2 in myeloid homeostasis and suppression of leukemia. J Exp Med. 2004;200:1681–1687. doi:10.1084/jem.20041247.
   PubMed Web of Science ®Google Scholar
• Coppin E, De Grandis M, Pandolfi PP, Arcangeli M-L, Aurrand-Lions M, Nunès JA. Dok1 and Dok2 Proteins regulate cell cycle in hematopoietic stem and progenitor cells. J Immunol. 2016;196:4110–4121. doi:10.4049/jimmunol.1501037.
   PubMed Web of Science ®Google Scholar
• Celis-Gutierrez J, Boyron M, Walzer T, Pandolfi PP, Jonjić S, Olive D, Dalod M, Vivier E, Nunès JA. Dok1 and Dok2 proteins regulate natural killer cell development and function. Embo J. 2014;33:1928–1940. doi:10.15252/embj.201387404.
   PubMed Web of Science ®Google Scholar
• Besin G, Yousefi M, Saba I, Klinck R, Pandolfi PP, Duplay P. Dok-1 overexpression promotes development of gammadelta natural killer T cells. Eur J Immunol. 2012;42:2491–2504. doi:10.1002/eji.201242421.
   PubMed Web of Science ®Google Scholar
• Laroche-Lefebvre C, Yousefi M, Daudelin J-F, Charpentier T, Tarrab E, Klinck R, Lamarre A, Labrecque N, Stäger S, Duplay P. Dok-1 and Dok-2 Regulate the Formation of Memory CD8+ T Cells. J Immunol. 2016;197:3618–3627. doi:10.4049/jimmunol.1600385.
   PubMed Web of Science ®Google Scholar
• Lahmidi S, Yousefi M, Dridi S, Duplay P, Pearson A. Dok-1 and Dok-2 are required to maintain herpes simplex virus 1-Specific CD8(+) T cells in a murine model of ocular infection. J Virol. 2017;91. doi:10.1128/JVI.00955-17.
   PubMed Web of Science ®Google Scholar
• De Simone M, Spagnuolo L, Lorè NI, Cigana C, De Fino I, Broman KW, Iraqi FA, Bragonzi A. Mapping genetic determinants of host susceptibility to Pseudomonas aeruginosa lung infection in mice. BMC Genomics. 2016;17:351. doi:10.1186/s12864-016-3328-4.
   PubMed Web of Science ®Google Scholar
• Cottet S, Corthesy-Theulaz I, Spertini F, Corthesy B. Microaerophilic conditions permit to mimic in vitro events occurring during in vivo Helicobacter pylori infection and to identify Rho/Ras-associated proteins in cellular signaling. J Biol Chem. 2002;277:33978–33986. doi:10.1074/jbc.M201726200.
   PubMed Web of Science ®Google Scholar
• Shinohara H, Inoue A, Toyama-Sorimachi N, Nagai Y, Yasuda T, Suzuki H, Horai R, Iwakura Y, Yamamoto T, Karasuyama H, et al. Dok-1 and Dok-2 are negative regulators of lipopolysaccharide-induced signaling. J Exp Med. 2005;201:333–339. doi:10.1084/jem.20041817.
   PubMed Web of Science ®Google Scholar
• Kim SS, Lee K-G, Chin C-S, Ng S-K, Pereira NA, Xu S, Lam K-P. DOK3 is required for IFN-beta production by enabling TRAF3/TBK1 complex formation and IRF3 activation. J Immunol. 2014;193:840–848. doi:10.4049/jimmunol.1301601.
   PubMed Web of Science ®Google Scholar
• Itoh S, Lemay S, Osawa M, Che W, Duan Y, Tompkins A, Brookes PS, Sheu -S-S, Abe J-I. Mitochondrial Dok-4 recruits Src kinase and regulates NF-kappaB activation in endothelial cells. J Biol Chem. 2005;280:26383–26396. doi:10.1074/jbc.M410262200.
   PubMed Web of Science ®Google Scholar
• Hooker E, Baldwin C, Roodman V, Batra A, Isa NN, Takano T, Lemay S. Binding and inhibition of the ternary complex factor Elk-4/Sap1 by the adapter protein Dok-4. Biochem J. 2017;474:1509–1528. doi:10.1042/BCJ20160832.
   PubMed Web of Science ®Google Scholar
• Ou X, Xu S, Li YF, Lam KP. Adaptor protein DOK3 promotes plasma cell differentiation by regulating the expression of programmed cell death 1 ligands. Proc Natl Acad Sci U S A. 2014;111:11431–11436. doi:10.1073/pnas.1400539111.
   PubMed Web of Science ®Google Scholar
• Niu Y, Roy F, Saltel F, Andrieu-Soler C, Dong W, Chantegrel A-L, Accardi R, Thépot A, Foiselle N, Tommasino M, et al. A nuclear export signal and phosphorylation regulate Dok1 subcellular localization and functions. Mol Cell Biol. 2006;26:4288–4301. doi:10.1128/MCB.01817-05.
   PubMed Web of Science ®Google Scholar
• Lloberas J, Celada A. p21(waf1/CIP1), a CDK inhibitor and a negative feedback system that controls macrophage activation. Eur J Immunol. 2009;39:691–694. doi:10.1002/eji.200939262.
   PubMed Web of Science ®Google Scholar
• Jiang X, Huang L, Xing D. Photoactivation of Dok1/ERK/PPARgamma signaling axis inhibits excessive lipolysis in insulin-resistant adipocytes. Cell Signal. 2015;27:1265–1275. doi:10.1016/j.cellsig.2015.03.010.
   PubMed Web of Science ®Google Scholar
• Demers A, Caron V, Rodrigue-Way A, Wahli W, Ong H, Tremblay A, Cao Y. A concerted kinase interplay identifies PPARgamma as a molecular target of ghrelin signaling in macrophages. PLoS One. 2009;4:e7728. doi:10.1371/journal.pone.0007728.
   PubMed Web of Science ®Google Scholar
• Boger C, Behrens HM, Kruger S, Rocken C. The novel negative checkpoint regulator VISTA is expressed in gastric carcinoma and associated with PD-L1/PD-1: A future perspective for a combined gastric cancer therapy? Oncoimmunology. 2017;6:e1293215. doi:10.1080/2162402X.2017.1293215.
   PubMed Web of Science ®Google Scholar
• Boger C, Krüger S, Behrens HM, Bock S, Haag J, Kalthoff H, Röcken C. Epstein-Barr virus-associated gastric cancer reveals intratumoral heterogeneity of PIK3CA mutations. Ann Oncol. 2017;28:1005–1014. doi:10.1093/annonc/mdx047.
   PubMed Web of Science ®Google Scholar
• Ebert MP, Tänzer M, Balluff B, Burgermeister E, Kretzschmar AK, Hughes DJ, Tetzner R, Lofton-Day C, Rosenberg R, Reinacher-Schick AC, et al. TFAP2E-DKK4 and chemoresistance in colorectal cancer. N Engl J Med. 2012;366:44–53. doi:10.1056/NEJMoa1009473.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. doi:10.1093/nar/29.9.e45.
   PubMed Web of Science ®Google Scholar
• Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia. 2004;6:1–6. doi:10.1016/s1476-5586(04)80047-2.
   PubMed Web of Science ®Google Scholar