Molecular mechanism of peritoneal dissemination in gastric cancer

Qing-Jiang Hu , Shuhei Ito , Kazuyoshi Yanagihara , Koshi Mimori

Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4 : 39

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Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4:39 DOI: 10.20517/2394-4722.2018.08
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Molecular mechanism of peritoneal dissemination in gastric cancer

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Abstract

Peritoneal dissemination (PD) is the most common cause of metastasis in gastric cancer (GC). Because there are no standard treatments for PD, it is associated with a poor prognosis. Although clinicians have performed intraperitoneal chemotherapy for GC with PD, the outcome remains unsatisfactory. Therefore, the development of novel treatments and diagnostic tools for PD is expected to improve the prognosis of GC patients with PD. Notably, it is essential to elucidate the molecular mechanisms involved in the development of PD in GC. In this review, the molecular mechanisms of PD (three steps: detachment from the primary tumor, adaptation to the microenvironment of the peritoneal cavity, and attachment to peritoneal mesothelial cells) and new topics in GC are highlighted.

Keywords

Gastric cancer / peritoneal dissemination / molecular mechanism

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Qing-Jiang Hu, Shuhei Ito, Kazuyoshi Yanagihara, Koshi Mimori. Molecular mechanism of peritoneal dissemination in gastric cancer. Journal of Cancer Metastasis and Treatment, 2018, 4: 39 DOI:10.20517/2394-4722.2018.08

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References

[1]

Torre LA,Siegel RL,Lortet-Tieulent J.Global cancer statistics, 2012.CA Cancer J Clin2015;65:87-108

[2]

Thomassen I,van Ramshorst B,Bosscha K,Lemmens VE.Peritoneal carcinomatosis of gastric origin: a population-based study on incidence, survival and risk factors.Int J Cancer2014;134:622-8

[3]

Wilke H,Van Cutsem E,Bodoky G,Hironaka S,Lipatov O,Cunningham D,Komatsu Y,Emig M,Ferry D,Schwartz JD.Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial.Lancet Oncol2014;15:1224-35

[4]

Bang YJ,Feyereislova A,Shen L,Lordick F,Omuro Y,Aprile G,Hill J,Ruschoff J.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.Lancet2010;376:687-97

[5]

Yonemura Y,Obata T.Recent advances in the treatment of peritoneal dissemination of gastrointestinal cancers by nucleoside antimetabolites.Cancer Sci2007;98:11-8

[6]

Kanda M.Molecular mechanisms of peritoneal dissemination in gastric cancer.World J Gastroenterol2016;22:6829-40 PMCID:PMC4974582

[7]

Lim B,Kim JH,Lee WS,Park JY,Park KH,Park JL,Rha SY.Genetic alterations and their clinical implications in gastric cancer peritoneal carcinomatosis revealed by whole-exome sequencing of malignant ascites.Oncotarget2016;7:8055-66 PMCID:PMC4884975

[8]

Kurashige J,Sawada G,Eguchi H,Mori M,Yashiro M,Baba H.Epigenetic modulation and repression of miR-200b by cancer-associated fibroblasts contribute to cancer invasion and peritoneal dissemination in gastric cancer.Carcinogenesis2015;36:133-41

[9]

Hanahan D.Hallmarks of cancer: the next generation.Cell2011;144:646-74

[10]

Liu X.E-cadherin and gastric cancer: cause, consequence, and applications.Biomed Res Int2014;2014:637308 PMCID:PMC4145387

[11]

Guilford P,Harraway J,McLeod N,Taite H,Miller A.E-cadherin germline mutations in familial gastric cancer.Nature1998;392:402-5

[12]

Kuphal F.E-cadherin modulates Wnt-dependent transcription in colorectal cancer cells but does not alter Wnt-independent gene expression in fibroblasts.Exp Cell Res2006;312:457-67

[13]

Kourtidis A,Pence LJ.A central role for cadherin signaling in cancer.Exp Cell Res2017;358:78-85

[14]

Asnaghi L,Quadri R,Qian X,Papageorge AG.E-cadherin negatively regulates neoplastic growth in non-small cell lung cancer: role of Rho GTPases.Oncogene2010;29:2760-71 PMCID:PMC3365679

[15]

Mao Z,Rong Y,Wang X,Zhang J.Connective tissue growth factor enhances the migration of gastric cancer through downregulation of E-cadherin via the NF-kappaB pathway.Cancer Sci2011;102:104-10

[16]

Piao HL,Wang M,Liang H.alpha-catenin acts as a tumour suppressor in E-cadherin-negative basal-like breast cancer by inhibiting NF-kappaB signalling.Nat Cell Biol2014;16:245-54 PMCID:PMC3943677

[17]

Janda E,Lehmann K,Beug H.Raf plus TGFbeta-dependent EMT is initiated by endocytosis and lysosomal degradation of E-cadherin.Oncogene2006;25:7117-30

[18]

Fukata M.Rho-family GTPases in cadherin-mediated cell-cell adhesion.Nature Rev Mol Cell Biol2001;2:887-97

[19]

O'Connor K.Dynamic functions of RhoA in tumor cell migration and invasion.Small GTPases2013;4:141-7 PMCID:PMC3976970

[20]

Leve F.Rho GTPase signaling in the development of colorectal cancer.J Cell Biochem2012;113:2549-59

[21]

Matsumoto S,Sato A,Kagawa Y,Kikuchi A.A combination of Wnt and growth factor signaling induces Arl4c expression to form epithelial tubular structures.EMBO J2014;33:702-18 PMCID:PMC4000088

[22]

Hu Q,Sato K,Nambara S,Hayashi N,Ito S,Saeki H,Maehara Y.Identification of ARL4C as a peritoneal dissemination-associated gene and its clinical significance in gastric cancer.Ann Surg Oncol2018;25:745-53

[23]

Vihinen P.Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets.Int J Cancer2002;99:157-66

[24]

Yamada T,Yoshihara K,Kanazawa A,Yamamoto N,Fujii S,Kunisaki C,Morinaga S,Rino Y,Masuda M.Overexpression of MMP-13 gene in colorectal cancer with liver metastasis.Anticancer Res2010;30:2693-9

[25]

Yonemura Y,Fujita H,Bandou E,Miwa K,Sasaki T.Role of MMP-7 in the formation of peritoneal dissemination in gastric cancer.Gastric Cancer2000;3:63-70

[26]

Peng L,Li W,Meng L,Jiang B,Shou C.PRL-3 promotes the motility, invasion, and metastasis of LoVo colon cancer cells through PRL-3-integrin beta1-ERK1/2 and-MMP2 signaling.Mol Cancer2009;8:110 PMCID:PMC2792223

[27]

Lee GH,Chung MJ,Kim HR.Lysyl oxidase-like-1 enhances lung metastasis when lactate accumulation and monocarboxylate transporter expression are involved.Oncol Lett2011;2:831-8 PMCID:PMC3408044

[28]

Itoh Y.MT1-MMP: a potent modifier of pericellular microenvironment.J Cell Physiol2006;206:1-8

[29]

Huang J,Li G,Chen P,Hou F,Zhong M,Xia X.EphA2 promotes epithelial-mesenchymal transition through the Wnt/beta-catenin pathway in gastric cancer cells.Oncogene2014;33:2737-47

[30]

Peng Z,Fang EH,Tong Q.Role of epithelial-mesenchymal transition in gastric cancer initiation and progression.World J Gastroenterol2014;20:5403-10 PMCID:PMC4017055

[31]

Prieto-Garcia E,Garcia-Ruiz I.Epithelial-to-mesenchymal transition in tumor progression.Med Oncol2017;34:122

[32]

Sciacovelli M.Metabolic reprogramming and epithelial-to-mesenchymal transition in cancer.FEBS J2017;284:3132-44 PMCID:PMC6049610

[33]

Xiao Q.Lysyl oxidase, extracellular matrix remodeling and cancer metastasis.Cancer Microenviron2012;5:261-73 PMCID:PMC3460045

[34]

Kurashige J,Niida A,Deng N,Uchi R,Takahashi Y,Inomata M,Fukagawa T,Sasaki H,Mori M,Baba H,Tan P.Integrated molecular profiling of human gastric cancer identifies DDR2 as a potential regulator of peritoneal dissemination.Sci Rep2016;6:22371 PMCID:PMC4776110

[35]

Gilkes DM,Wirtz D.Hypoxia and the extracellular matrix: drivers of tumour metastasis.Nat Rev Cancer2014;14:430-9 PMCID:PMC4283800

[36]

Simpson CD,Schimmer AD.Anoikis resistance and tumor metastasis.Cancer Lett2008;272:177-85

[37]

Miao ZF,Zhao TT,Gao J,Xu HM.Peritoneal milky spots serve as a hypoxic niche and favor gastric cancer stem/progenitor cell peritoneal dissemination through hypoxia-inducible factor 1alpha.Stem Cells2014;32:3062-74 PMCID:PMC4282537

[38]

Huang D,Li X,Sun L,Zhong X,Song L,Gao P.HIF-1-mediated suppression of acyl-CoA dehydrogenases and fatty acid oxidation is critical for cancer progression.Cell Rep2014;8:1930-42

[39]

Semenza GL.HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations.J Clin Invest2013;123:3664-71 PMCID:PMC3754249

[40]

Denko NC.Hypoxia, HIF1 and glucose metabolism in the solid tumour.Nat Rev Cancer2008;8:705-13

[41]

Barker HE,Erler JT.The rationale for targeting the LOX family in cancer.Nat Rev Cancer2012;12:540-52

[42]

Merino D,Asselin-Labat ML,Pal B,Anderson RL,Bouillet P,Visvader JE.Pro-apoptotic Bim suppresses breast tumor cell metastasis and is a target gene of SNAI2.Oncogene2015;34:3926-34

[43]

Smit MA,Song JY,Peeper DS.A Twist-Snail axis critical for TrkB-induced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis.Mol Cell Biol2009;29:3722-37 PMCID:PMC2698746

[44]

Baba K,Miyake S,Wakiyama K,Okuyama K,Tanaka T,Yanagihara K.Hypoxia-induced ANGPTL4 sustains tumour growth and anoikis resistance through different mechanisms in scirrhous gastric cancer cell lines.Sci Rep2017;7:11127 PMCID:PMC5594024

[45]

Douma S,Zevenhoven J,Van Garderen E.Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB.Nature2004;430:1034-9

[46]

Paoli P,Chiarugi P.Anoikis molecular pathways and its role in cancer progression.Biochim Biophys Acta2013;1833:3481-98

[47]

Buchheit CL,Schafer ZT.Cancer cell survival during detachment from the ECM: multiple barriers to tumour progression.Nat Rev Cancer2014;14:632-41

[48]

Altomare DA.Perturbations of the AKT signaling pathway in human cancer.Oncogene2005;24:7455-64

[49]

Davies MA,Dhesi H,McDonnell TJ,Yung WK.Regulation of Akt/PKB activity, cellular growth, and apoptosis in prostate carcinoma cells by MMAC/PTEN.Cancer Res1999;59:2551-6

[50]

Vitolo MI,Szmacinski M,Waldman T,Martin SS,Bachman KE.Deletion of PTEN promotes tumorigenic signaling, resistance to anoikis, and altered response to chemotherapeutic agents in human mammary epithelial cells.Cancer Res2009;69:8275-83 PMCID:PMC2783190

[51]

Avizienyte E.Src and FAK signalling controls adhesion fate and the epithelial-to-mesenchymal transition.Curr Opin Cell Biol2005;17:542-7

[52]

Bouchard V,Thibodeau S,Fujita N,Beaulieu JF,Vezina A,Vachon PH.Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways.J Cell Physiol2007;212:717-28

[53]

Cives M,Rizzo FM,D'Oronzo S,Silvestris F.Osteotropism of neuroendocrine tumors: role of the CXCL12/ CXCR4 pathway in promoting EMT in vitro.Oncotarget2017;8:22534-49 PMCID:PMC5410243

[54]

Yao C,Song H,Qu Y,Shi R.CXCL12/CXCR4 axis upregulates twist to induce EMT in human glioblastoma.Mol Neurobiol2016;53:3948-53

[55]

Koizumi K,Akashi T,Saiki I.Chemokine receptors in cancer metastasis and cancer cell-derived chemokines in host immune response.Cancer Sci2007;98:1652-8

[56]

Wendt MK,Vongsa RA.Constitutive CXCL12 expression induces anoikis in colorectal carcinoma cells.Gastroenterology2008;135:508-17 PMCID:PMC2583344

[57]

van der Wal JBC.Biology of the peritoneum in normal homeostasis and after surgical trauma.Colorectal Dis2007;9:9-13

[58]

Psaila B.The metastatic niche: adapting the foreign soil.Nat Rev Cancer2009;9:285-93 PMCID:PMC3682494

[59]

Chiang AC.Molecular basis of metastasis.N Engl J Med2008;359:2814-23 PMCID:PMC4189180

[60]

Nishimori H,Denno R,Hata F,Ura H,Isomura H,Hirata K.A novel experimental mouse model of peritoneal dissemination of human gastric cancer cells: different mechanisms in peritoneal dissemination and hematogenous metastasis.Jpn J Cancer Res2000;91:715-22 PMCID:PMC5926407

[61]

Takatsuki H,Sano R,Tsuji T.Adhesion of gastric carcinoma cells to peritoneum mediated by alpha3beta1 integrin (VLA-3).Cancer Res2004;64:6065-70

[62]

Tanaka M,Itoh G,Goto A,Yanagihara K,Aiba N.Mesothelial cells create a novel tissue niche that facilitates gastric cancer invasion.Cancer Res2017;77:684-95

[63]

Aoyagi K,Yano S,Imaizumi T,Shirouzu K.VEGF significance in peritoneal recurrence from gastric cancer.Gastric Cancer2005;8:155-63

[64]

Yoshikawa T,Miyagi Y,Kimura M,Kobayashi O.Up-regulation of hypoxia-inducible factor-1 alpha and VEGF mRNAs in peritoneal dissemination of patients with gastric cancer.Anticancer Res2006;26:3849-53

[65]

Kamiyama M,Ishikawa T,Hasegawa S,Nagashima Y,Mitsuhashi M,Hoffman RM,Shimada H.VEGF receptor antisense therapy inhibits angiogenesis and peritoneal dissemination of human gastric cancer in nude mice.Cancer Gene Ther2002;9:197-201

[66]

Muro K,Shankaran V,Catenacci D,Eder JP,Le DT,McRee AJ,Pathiraja K,Emancipator K,Koshiji M.Pembrolizumab for patients with PD-L1-positive advanced gastric cancer (KEYNOTE-012): a multicentre, open-label, phase 1b trial.Lancet Oncol2016;17:717-26

[67]

Kang YK,Satoh T,Chao Y,Chung HC,Muro K,Yeh KH,Oh SC,Tamura T,Hamamoto Y,Chin K,Minashi K,Tsuda M.Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial.Lancet2017;390:2461-71

[68]

Cancer Genome Atlas Research Network.Comprehensive molecular characterization of gastric adenocarcinoma.Nature2014;513:202-9 PMCID:PMC4170219

[69]

Kamath RV,Wang C,Slusarczyk A,Wang J,Jovanovic B,Nayar R,Shi F.Perinucleolar compartment prevalence has an independent prognostic value for breast cancer.Cancer Res2005;65:246-53

[70]

Norton JT,Wang C,Kim JJ.Perinucleolar compartment prevalence is a phenotypic pancancer marker of malignancy.Cancer2008;113:861-9 PMCID:PMC4780316

[71]

Frankowski KJ,Patnaik S,Southall N,Teper Y,Kandela I,Dextras C,Bian Y,Titus S,Wen Y,Griner LM,Meng Z,Vilimas T,Kozlov S,Quadri HS,Long C,Chen W,Huang H,Goldberg E,Xi R,Sahagian G,Mazar A,Zheng W,Aube J,Marugan JJ.Metarrestin, a perinucleolar compartment inhibitor, effectively suppresses metastasis.Sci Transl Med2018;10:eaap8307

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