Microenvironment in the pathogenesis of gastric cancer metastasis

Hiroshi Sawayama , Takatsugu Ishimoto , Hideo Baba

Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4 : 10

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Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4:10 DOI: 10.20517/2394-4722.2017.79
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Microenvironment in the pathogenesis of gastric cancer metastasis

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Abstract

Tumor tissues contain cancer cells, other cellular and non-cellular components. Tumor microenvironments consist of cancer cells and various types of stromal cells, cancer associated fibroblasts, bone marrow-derived cells, endothelial cells, and hematopoietic cells, mainly tumor-associated macrophages and tumor-infiltrating lymphocytes. Increasing recent evidence has demonstrated that alteration of tumor microenvironments is deeply implicated in tumor progression and metastasis in gastric cancer (GC) patients. Recent investigations have provided insights into the molecular mechanisms of the interaction between tumor cells and tumor microenvironments. Interactions between cancer cells and their microenvironment with cytokines and microRNA in extracellular vesicles, such as the exosome, can have a substantial impact on tumor characteristics. Alterations in the tumor microenvironment may play a crucial role in facilitating the progression of tumor cells and metastasis, as well as the activation of cell signaling pathways, which are associated with GC cell proliferation and invasion by genetic or epigenetic alterations. In this review, significant molecular insights into the tumor microenvironment, which consist of cancer associated fibroblasts, bone marrow-derived cells, tumor-associated macrophages and tumor-infiltrating lymphocytes; the interactions between cancer cells and their microenvironment; and the clinical impacts of alterations of GC microenvironments will be discussed.

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Tumor microenvironments / cancer associated fibroblasts / bone marrow-derived cells / tumor-associated macrophages / tumor-infiltrating lymphocytes

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Hiroshi Sawayama, Takatsugu Ishimoto, Hideo Baba. Microenvironment in the pathogenesis of gastric cancer metastasis. Journal of Cancer Metastasis and Treatment, 2018, 4: 10 DOI:10.20517/2394-4722.2017.79

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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]

Sasako M,Yamamoto S,Nashimoto A,Hiratsuka M,Kinoshita T,Yamamura Y.D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer..N Engl J Med2008;359:453-62

[3]

Waddell T,Allum W,Cervantes A.Gastric cancer: ESMO-ESSO-ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up..Ann Oncol2013;24 Suppl 6:vi57-63

[4]

Ajani JA,Besh S,Das P,Fakih MG,Gerdes H,Hayman JA,Ilson DH,Kleinberg LR,Lockhart AC,Mulcahy MF,Posey JA,Scott WJ,Varghese TKJr,Washington MK,Wright CD,Sundar H.Gastric cancer, version 2.2013: featured updates to the NCCN Guidelines..J Natl Compr Canc Netw2013;11:531-46

[5]

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

[6]

Fuchs CS,Yong CJ,Passalacqua R,Safran H,Aprile G,Melichar B,Topuzov E,Chau I,Sivanandan C,Koshiji M,Liepa AM,Schwartz JD.Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial..Lancet2014;383:31-9

[7]

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

[8]

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

[9]

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

[10]

Houghton J,Nomura S,Carlson J,Cai X,Goldenring JR.Gastric cancer originating from bone marrow-derived cells..Science2004;306:1568-71

[11]

Quante M,Tomita H,Wang SS,Baik GH,Diprete B,Friedman R,Tycko B.Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth..Cancer Cell2011;19:257-72 PMCID:PMC3060401

[12]

Varon C,Mazurier F,Chambonnier L,Giese A,Carlotti M.Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice..Gastroenterology2012;142:281-91

[13]

Ferrand J,Schmid-Alliana A,Varon C.Helicobacter pylori infection of gastrointestinal epithelial cells in vitro induces mesenchymal stem cell migration through an NF-kappaB-dependent pathway..PLoS One2011;6:e29007 PMCID:PMC3247220

[14]

Zhu L,Shi J,Chen G,Liu AB,Ye J,Wang H,Fang J,Wang TC,Tu SP.Crosstalk between bone marrow-derived myofibroblasts and gastric cancer cells regulates cancer stemness and promotes tumorigenesis..Oncogene2016;35:5388-99 PMCID:PMC5063653

[15]

Zhu M,Yang F,Cai J,Fu H,Zhu W,Xu W.miR-155-5p inhibition promotes the transition of bone marrow mesenchymal stem cells to gastric cancer tissue derived MSC-like cells via NF-kappaB p65 activation..Oncotarget2016;7:16567-80

[16]

Kasashima H,Nakamae H,Masuda G,Fukuoka T,Nakane T,Hirakawa K.CXCL1-chemokine (C-X-C Motif) receptor 2 signaling stimulates the recruitment of bone marrow-derived mesenchymal cells into diffuse-type gastric cancer stroma..Am J Pathol2016;186:3028-39

[17]

Buhring HJ,Cerabona F,Kanz L.Phenotypic characterization of distinct human bone marrow-derived MSC subsets..Ann N Y Acad Sci2009;1176:124-34

[18]

Boxall SA.Markers for characterization of bone marrow multipotential stromal cells..Stem Cells Int2012;2012:975871

[19]

Jones EA,English A,Mundy J,Chapman T,Hatton P.Synovial fluid mesenchymal stem cells in health and early osteoarthritis: detection and functional evaluation at the single-cell level..Arthritis Rheum2008;58:1731-40

[20]

Kasashima H,Nakamae H,Kinoshita H,Fukuoka T,Sakurai K,Kubo N,Muguruma K,Nakane T,Hirakawa K.Bone marrow-derived stromal cells are associated with gastric cancer progression..Br J Cancer2015;113:443-52 PMCID:PMC4522640

[21]

Khazaie K,Khan MW,Gounaris E,Bonertz A,Strouch MJ,Phillips JD,Bentrem DJ.The significant role of mast cells in cancer..Cancer Metastasis Rev2011;30:45-60

[22]

Mukherjee S,Dutta C,Karmakar R.Evaluation of endoscopic biopsy in gastric lesions with a special reference to the significance of mast cell density..Indian J Pathol Microbiol2009;52:20-4

[23]

Zhao Y,Cai K,Tao K,Wang J.Increased numbers of gastric-infiltrating mast cells and regulatory T cells are associated with tumor stage in gastric adenocarcinoma patients..Oncol Lett2012;4:755-8 PMCID:PMC3506702

[24]

Ribatti D,Marzullo A,Annese T,Crivellato E.Mast cells and angiogenesis in gastric carcinoma..Int J Exp Pathol2010;91:350-6 PMCID:PMC2962893

[25]

Lin C,Zhang H,Li R,Li H,Xu J.Tryptase expression as a prognostic marker in patients with resected gastric cancer..Br J Surg2017;104:1037-44

[26]

Shikotra A,Green RH,Bradding P.Mast cell phenotype, TNFalpha expression and degranulation status in non-small cell lung cancer..Sci Rep2016;6:38352 PMCID:PMC5138591

[27]

Balkwill F.Inflammation and cancer: back to Virchow?.Lancet2001;357:539-45

[28]

Zheng X,Shao Y,Chen L,Hu W,Wu C,Zhu Y.Prognostic role of tumor-infiltrating lymphocytes in gastric cancer: a meta-analysis..Oncotarget2017;8:57386-98

[29]

Kang BW,Yoon S,Jeon SW,Chung HY,Kang H.Prognostic value of tumor-infiltrating lymphocytes in Epstein-Barr virus-associated gastric cancer..Ann Oncol2016;27:494-501

[30]

Kim KJ,Cho HJ,Yang HK,Kang GH.Prognostic implications of tumor-infiltrating FoxP3+ regulatory T cells and CD8+ cytotoxic T cells in microsatellite-unstable gastric cancers..Hum Pathol2014;45:285-93

[31]

Ma J,Hao Y,Li Z,Liang Q,Zeng M.Differentiated tumor immune microenvironment of Epstein-Barr virus-associated and negative gastric cancer: implication in prognosis and immunotherapy..Oncotarget2017;8:67094-103

[32]

Kawazoe A,Kuboki Y,Nagatsuma AK,Yoshino T,Ohtsu A.Clinicopathological features of programmed death ligand 1 expression with tumor-infiltrating lymphocyte, mismatch repair, and Epstein-Barr virus status in a large cohort of gastric cancer patients..Gastric Cancer2017;20:407-15

[33]

Fang W,Sheng J,Zhang Y,Liu L,Peng P.Association between PD-L1 expression on tumour-infiltrating lymphocytes and overall survival in patients with gastric cancer..J Cancer2017;8:1579-85 PMCID:PMC5535713

[34]

Kim KJ,Kim WH.Combined prognostic effect of PD-L1 expression and immunoscore in microsatellite-unstable advanced gastric cancers..Oncotarget2017;8:58887-902

[35]

Kim JW,Ahn SH,Kim HH,Chang H,Kim YJ,Kim JH,Lee JS.Prognostic implications of immunosuppressive protein expression in tumors as well as immune cell infiltration within the tumor microenvironment in gastric cancer..Gastric Cancer2016;19:42-52

[36]

Koh J,Kim JW,Kwak Y,Ahn SH,Kim HH,Lee HS.Clinicopathologic implications of immune classification by PD-L1 expression and CD8-positive tumor-infiltrating lymphocytes in stage II and III gastric cancer patients..Oncotarget2017;8:26356-67 PMCID:PMC5432263

[37]

Zheng X,Mora J,Seeger W,Savai R.Redirecting tumor-associated macrophages to become tumoricidal effectors as a novel strategy for cancer therapy..Oncotarget2017;8:48436-52

[38]

Franklin RA,Sarkar A,Bivona MR,Pamer EG.The cellular and molecular origin of tumor-associated macrophages..Science2014;344:921-5 PMCID:PMC4204732

[39]

O'Sullivan T,Vermi W,Arthur C,Uppaluri R,Ngiow SF,Smyth MJ,Bui JD.Cancer immunoediting by the innate immune system in the absence of adaptive immunity..J Exp Med2012;209:1869-82 PMCID:PMC3457735

[40]

Luo Y,Krueger J,Lee SH,Markowitz D,Liu C,Xiang R.Targeting tumor-associated macrophages as a novel strategy against breast cancer..J Clin Invest2006;116:2132-41 PMCID:PMC1513049

[41]

Wang XL,Wu CP.Prognostic significance of tumor-associated macrophage infiltration in gastric cancer: a meta-analysis..Genet Mol Res2016;15:gmr15049040

[42]

Tauchi Y,Kumamoto K,Sakimura C,Kimura K,Amano R,Muguruma K,Maeda K,Hirakawa K.Tumor-associated macrophages induce capillary morphogenesis of lymphatic endothelial cells derived from human gastric cancer..Cancer Sci2016;107:1101-9 PMCID:PMC4982583

[43]

Kim KJ,Yang HK,Kang GH.Prognostic implication of M2 macrophages are determined by the proportional balance of tumor associated macrophages and tumor infiltrating lymphocytes in microsatellite-unstable gastric carcinoma..PLoS One2015;10:e0144192 PMCID:PMC4699826

[44]

Ishimoto T,Watanabe M,Iwatsuki M,Okabe H,Yokoyama N,Yoshikawa M,Komohara Y,Saya H.Macrophage-derived reactive oxygen species suppress miR-328 targeting CD44 in cancer cells and promote redox adaptation..Carcinogenesis2014;35:1003-11

[45]

Aruffo A,Melnick M,Seed B.CD44 is the principal cell surface receptor for hyaluronate..Cell1990;61:1303-13

[46]

Screaton GR,Mayeda A,Plebanski M,Bell JI.Identification and characterization of three members of the human SR family of pre-mRNA splicing factors..EMBO J1995;14:4336-49 PMCID:PMC394518

[47]

Screaton GR,Jackson DG,Gerth U.Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons..Proc Natl Acad Sci U S A1992;89:12160-4 PMCID:PMC50718

[48]

Takaishi S,Tu S,Shibata W,Gordon SA,Wang TC.Identification of gastric cancer stem cells using the cell surface marker CD44..Stem Cells2009;27:1006-20 PMCID:PMC2746367

[49]

Ishimoto T,Yae T,Motohara T,Oshima M,Asaba R,Masuko T,Ishikawa T,Takahashi E,Baba Y,Suematsu M,Saya H.CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth..Cancer Cell2011;19:387-400

[50]

Wyckoff JB,Lin EY,Goswami S,Segall JE,Condeelis J.Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors..Cancer Res2007;67:2649-56

[51]

Bonde AK,Kumar S,Schwendener RA.Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors..BMC Cancer2012;12:35 PMCID:PMC3314544

[52]

Wu MH,Hua KT,Lin MT.Macrophage infiltration induces gastric cancer invasiveness by activating the beta-catenin pathway..PLoS One2015;10:e0134122 PMCID:PMC4520459

[53]

Guo J,Guo Q,Zhang J.Tumor-associated macrophages induce the expression of FOXQ1 to promote epithelial-mesenchymal transition and metastasis in gastric cancer cells..Oncol Rep2017;38:2003-10 PMCID:PMC5652949

[54]

Sugihara H,Watanabe M,Iwatsuki M,Komohara Y,Baba H.Identification of miR-30e* regulation of Bmi1 expression mediated by tumor-associated macrophages in gastrointestinal cancer..PLoS One2013;8:e81839 PMCID:PMC3842972

[55]

Abiko K,Hamanishi J,Murakami R,Yoshioka Y,Konishi I.IFN-gamma from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer..Br J Cancer2015;112:1501-9 PMCID:PMC4453666

[56]

Soliman H,Antonia S.PD-L1 expression is increased in a subset of basal type breast cancer cells..PLoS One2014;9:e88557 PMCID:PMC3925108

[57]

Harada K,Estrella JS,Xu Y,Sudo K,Suzuki K,Johnson RL,Song S.Tumor-associated macrophage infiltration is highly associated with PD-L1 expression in gastric adenocarcinoma..Gastric Cancer2018;21:31-40

[58]

Kalluri R.Fibroblasts in cancer..Nat Rev Cancer2006;6:392-401

[59]

Yamaguchi H.Direct interaction between carcinoma cells and cancer associated fibroblasts for the regulation of cancer invasion..Cancers (Basel)2015;7:2054-62 PMCID:PMC4695876

[60]

De Wever O,Mareel M.Stromal myofibroblasts are drivers of invasive cancer growth..Int J Cancer2008;123:2229-38

[61]

Bissell MJ.Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression..Nat Med2011;17:320-9 PMCID:PMC3569482

[62]

Wen X,Jiao F,Sun Y,Li Q.Fibroblast activation protein-alpha-positive fibroblasts promote gastric cancer progression and resistance to immune checkpoint blockade..Oncol Res2017;25:629-40

[63]

Ishimoto T,Nandi T,Onishi N,Lin SJ,Tay ST,Cho BC,Arima K,Iwatsuki M,Oki E,Saya H,Baba H.Activation of transforming growth factor beta 1 signaling in gastric cancer-associated fibroblasts increases their motility, via expression of rhomboid 5 homolog 2, and ability to induce invasiveness of gastric cancer cells..Gastroenterology2017;153:191-204.e16

[64]

Wu X,Zhou Q,Yu Z,Li C,Zhu Z,Su L.IL-6 secreted by cancer-associated fibroblasts promotes epithelial-mesenchymal transition and metastasis of gastric cancer via JAK2/STAT3 signaling pathway..Oncotarget2017;8:20741-50

[65]

Bie Q,Sun C,Barnie PA,Peng J,Zheng D,Wang S.IL-17B activated mesenchymal stem cells enhance proliferation and migration of gastric cancer cells..Oncotarget2017;8:18914-23 PMCID:PMC5386657

[66]

Yan Y,Wang RF.Role of cancer-associated fibroblasts in invasion and metastasis of gastric cancer..World J Gastroenterol2015;21:9717-26 PMCID:PMC4562955

[67]

Yang TS,Chen X,Hua J,Zhou B.MicroRNA-106b in cancer-associated fibroblasts from gastric cancer promotes cell migration and invasion by targeting PTEN..FEBS Lett2014;588:2162-9

[68]

Naito Y,Oue N,Sentani K,Hirakawa K.MicroRNA-143 regulates collagen type III expression in stromal fibroblasts of scirrhous type gastric cancer..Cancer Sci2014;105:228-35 PMCID:PMC4317817

[69]

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

[70]

Lee KW,Sung CO.Twist1 is a key regulator of cancer-associated fibroblasts..Cancer Res2015;75:73-85

[71]

Sung CO,Han S.Twist1 is up-regulated in gastric cancer-associated fibroblasts with poor clinical outcomes..Am J Pathol2011;179:1827-38 PMCID:PMC3181370

[72]

Lippitz BE.Cytokine patterns in patients with cancer: a systematic review..Lancet Oncol2013;14:e218-28

[73]

Samarendra H,Petrinic T,Reddy S,Gordon-Weeks A.A meta-analysis of CXCL12 expression for cancer prognosis..Br J Cancer2017;117:124-35

[74]

Han M,Zhang Y,Huang B,Bian R.The prognosis and clinicopathology of CXCR4 in gastric cancer patients: a meta-analysis..Tumour Biol2014;35:4589-97

[75]

Balkwill F.The significance of cancer cell expression of the chemokine receptor CXCR4..Semin Cancer Biol2004;14:171-9

[76]

Teicher BA.CXCL12 (SDF-1)/CXCR4 pathway in cancer..Clin Cancer Res2010;16:2927-31

[77]

He H,Shen Z,Wang X,Liu F,Sun Y.Upregulated expression of C-X-C chemokine receptor 4 is an independent prognostic predictor for patients with gastric cancer..PLoS One2013;8:e71864 PMCID:PMC3735563

[78]

Lee HJ,Kim HY,Yun HJ,Kim S.Chemokine receptor CXCR4 expression, function, and clinical implications in gastric cancer..Int J Oncol2009;34:473-80

[79]

Chen G,Wang X,Ding J.Inhibition of chemokine (CXC motif) ligand 12/chemokine (CXC motif) receptor 4 axis (CXCL12/CXCR4)-mediated cell migration by targeting mammalian target of rapamycin (mTOR) pathway in human gastric carcinoma cells..J Biol Chem2012;287:12132-41 PMCID:PMC3320958

[80]

Izumi D,Miyake K,Eto K,Yasuda T,Kaida T,Imamura Y,Iwatsuki M,Baba Y,Miyamoto Y,Watanabe M,Araki N,Baba H.CXCL12/CXCR4 activation by cancer-associated fibroblasts promotes integrin beta1 clustering and invasiveness in gastric cancer..Int J Cancer2016;138:1207-19

[81]

Hashimoto I,Tatematsu M,Cho S,Nakashima A,Saito S,Saiki I.Blocking on the CXCR4/mTOR signalling pathway induces the anti-metastatic properties and autophagic cell death in peritoneal disseminated gastric cancer cells..Eur J Cancer2008;44:1022-9

[82]

Guo ZJ,Qian F,Yu X,Cui W,Zhang X,Wang JM,Bian XW.Transcription factor RUNX2 up-regulates chemokine receptor CXCR4 to promote invasive and metastatic potentials of human gastric cancer..Oncotarget2016;7:20999-1012

[83]

Tiveron MC,Daou P,Cremer H.Expression and function of CXCR7 in the mouse forebrain..J Neuroimmunol2010;224:72-9

[84]

Cheng Y,Che X,Song N,Gong J,Liu Y.CXCL12/SDF-1alpha induces migration via SRC-mediated CXCR4-EGFR cross-talk in gastric cancer cells..Oncol Lett2017;14:2103-10 PMCID:PMC5530148

[85]

Xin Q,Yu HB,Cui YF,Ma Z,Liu W.CXCR7/CXCL12 axis is involved in lymph node and liver metastasis of gastric carcinoma..World J Gastroenterol2017;23:3053-65 PMCID:PMC5423042

[86]

Nambara S,Oki E,Maehara Y.Overexpression of CXCR7 is a novel prognostic indicator in gastric cancer..Dig Surg2017;34:312-8

[87]

Park SH,Casagrande F,Nothnagel HJ,Kiefer H,De Angelis AA,Opella SJ.Structure of the chemokine receptor CXCR1 in phospholipid bilayers..Nature2012;491:779-83

[88]

Sallusto F.Chemokines and leukocyte traffic..Nat Immunol2008;9:949-52

[89]

Cao Y,Zhang H,Li R,Li H,Zhang W.CXC chemokine receptor 1 predicts postoperative prognosis and chemotherapeutic benefits for TNM II and III resectable gastric cancer patients..Oncotarget2017;8:20328-39

[90]

Wang J,Wang K,Luo B,Wang W,Li J.Repertaxin, an inhibitor of the chemokine receptors CXCR1 and CXCR2, inhibits malignant behavior of human gastric cancer MKN45 cells in vitro and in vivo and enhances efficacy of 5-fluorouracil..Int J Oncol2016;48:1341-52 PMCID:PMC4777600

[91]

Xiang Z,Xia GK,Wei ZW,Yu J,He Y,Brekken RA,Zhang CH.A positive crosstalk between CXCR4 and CXCR2 promotes gastric cancer metastasis..Oncogene2017;36:5122-33

[92]

Yang SB,Wu JH,Zhan W.Association between CXCR2 and IL-22BP expression indicate a poor outcome for gastric adenocarcinoma progression..Oncol Lett2016;12:1477-84 PMCID:PMC4950243

[93]

Peinado H,Lyden D.The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts..Semin Cancer Biol2011;21:139-46

[94]

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

[95]

Brinckerhoff CE.Matrix metalloproteinases: a tail of a frog that became a prince..Nat Rev Mol Cell Biol2002;3:207-14

[96]

Parsons SL,Brown PD,Steele RJ.Matrix metalloproteinases..Br J Surg1997;84:160-6

[97]

Imai K,Nakanishi I,Fujii Y,Okada Y.Matrix metalloproteinase 7 (matrilysin) from human rectal carcinoma cells. Activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties..J Biol Chem1995;270:6691-7

[98]

Ii M,Adachi Y,Shinomura Y.Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis..Exp Biol Med (Maywood)2006;231:20-7

[99]

Nagase H.Matrix metalloproteinases..J Biol Chem1999;274:21491-4

[100]

Shen W,Wei B.The prognostic role of matrix metalloproteinase 2 in gastric cancer: a systematic review with meta-analysis..J Cancer Res Clin Oncol2014;140:1003-9

[101]

Wang HL,Zhang Y.Relationships between abnormal MMP2 expression and prognosis in gastric cancer: a meta-analysis of cohort studies..Cancer Biother Radiopharm2014;29:166-72

[102]

Soleyman-Jahi S,Abdirad A,Heidari R.Prognostic significance of matrix metalloproteinase-7 in gastric cancer survival: a meta-analysis..PLoS One2014;10:e0122316 PMCID:PMC4412628

[103]

Chen J,Zhou HC,Lu Y,Wu W.Prognostic value of matrix metalloproteinase-9 in gastric cancer: a meta-analysis..Hepatogastroenterology2014;61:518-24

[104]

Loffek S,Angel P,Krieg T.High invasive melanoma cells induce matrix metalloproteinase-1 synthesis in fibroblasts by interleukin-1alpha and basic fibroblast growth factor-mediated mechanisms..J Invest Dermatol2005;124:638-43

[105]

Cardoso AP,Pinto AT,Monteiro C,Santos SG,Seruca R,Mareel M,Oliveira MJ.Matrix metalloproteases as maestros for the dual role of LPS- and IL-10-stimulated macrophages in cancer cell behaviour..BMC Cancer2015;15:456 PMCID:PMC4456051

[106]

Wang Y,Wu X,Gao Q.Interleukin 17A promotes gastric cancer invasiveness via NF-kappaB mediated matrix metalloproteinases 2 and 9 expression..PLoS One2014;9:e96678 PMCID:PMC4048176

[107]

Cowden Dahl KD,Hudson LG.PEA3 is necessary for optimal epidermal growth factor receptor-stimulated matrix metalloproteinase expression and invasion of ovarian tumor cells..Mol Cancer Res2007;5:413-21 PMCID:PMC3621069

[108]

Toschi E,Sgadari C,Cereseto A,Palladino C,Leone P,Butto S,Monini P.Activation of matrix-metalloproteinase-2 and membrane-type-1-matrix-metalloproteinase in endothelial cells and induction of vascular permeability in vivo by human immunodeficiency virus-1 Tat protein and basic fibroblast growth factor..Mol Biol Cell2001;12:2934-46 PMCID:PMC60146

[109]

Udayakumar TS,Nagle RB.Fibroblast growth factor-1 induced promatrilysin expression through the activation of extracellular-regulated kinases and STAT3..Neoplasia2002;4:60-7 PMCID:PMC1503316

[110]

Bond M,Baker AH.Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B..FEBS Lett1998;435:29-34

[111]

Shan YQ,Zhou CH,Ye J,Ju TF.MMP-9 is increased in the pathogenesis of gastric cancer by the mediation of HER2..Cancer Gene Ther2015;22:101-7

[112]

Liu J,Wang W,Chen F,Ding J,Xie WF.Cancer-associated fibroblasts promote hepatocellular carcinoma metastasis through chemokine-activated hedgehog and TGF-beta pathways..Cancer Lett2016;379:49-59

[113]

Shifrin DAJr,Coffey RJ.Extracellular vesicles: communication, coercion, and conditioning..Mol Biol Cell2013;24:1253-9 PMCID:PMC3639038

[114]

Raposo G.Extracellular vesicles: exosomes, microvesicles, and friends..J Cell Biol2013;200:373-83 PMCID:PMC3575529

[115]

Deng G,Zhang Y,Cheng Y,Zhang S,Liu Y.Gastric cancer-derived exosomes promote peritoneal metastasis by destroying the mesothelial barrier..FEBS Lett2017;591:2167-79

[116]

Ren J,Li H,Pang L,Gu Q,Liu B.Characterization of exosomal RNAs derived from human gastric cancer cells by deep sequencing..Tumour Biol2017;39:1010428317695012

[117]

Tokuhisa M,Kosaka N,Yashiro M,Kosaka T,Akiyama H,Endo I.Exosomal miRNAs from peritoneum lavage fluid as potential prognostic biomarkers of peritoneal metastasis in gastric cancer..PLoS One2015;10:e0130472 PMCID:PMC4514651

[118]

Zhang H,Liu R,Zhou L,Li S,Li J,Huang D,Zhang L,Ba Y.Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis..Nat Commun2017;8:15016 PMCID:PMC5394240

[119]

Wu L,Zhang B,Yuan X,Pan Z,Xu W.Exosomes derived from gastric cancer cells activate NF-kappaB pathway in macrophages to promote cancer progression..Tumour Biol2016;37:12169-80

[120]

Ma M,Liu Z,Deng H,Wang X,Zuo C.miRNA-221 of exosomes originating from bone marrow mesenchymal stem cells promotes oncogenic activity in gastric cancer..Onco Targets Ther2017;10:4161-71 PMCID:PMC5574589

[121]

Liu D,Trojanowicz B,Shi D,Wang Z.CD97 promotion of gastric carcinoma lymphatic metastasis is exosome dependent..Gastric Cancer2016;19:754-66 PMCID:PMC4906076

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