Vascular endothelial cells facilitated HCC invasion and metastasis through the Akt and NF-κB pathways induced by paracrine cytokines

Journal of Experimental and Clinical Cancer Research

Volumn 32, Issue 1, 2013, Pages

  Wang, Yao Hui ^a,b   Dong, Yin Ying ^a   Wang, Wei Min ^a   Xie, Xiao Ying ^a   Wang, Zhi Ming ^a   Chen, Rong Xin ^a   Chen, Jie ^a   Gao, Dong Mei ^a   Cui, Jie Feng ^a   Ren, Zheng Gang ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

Author keywords

Cytokine; Endothelial cell; Hepatocellular carcinoma; Invasiveness; Metastasis

Indexed keywords

ENDOSTATIN; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B;

ARTICLE; CARCINOGENICITY; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER CELL CARCINOMA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR INVASION; UPREGULATION; VASCULAR ENDOTHELIAL CELL; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM METASTASIS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84881294106     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-32-51     Document Type: Article

References (49)

1. Global cancer statistics, 2002. Parkin DM, Bray F, Ferlay J, Pisani P, Ca-a Cancer Journal for Clinicians 2005 55 74 108 10.3322/canjclin.55.2.74 15761078
2. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Yang JD, Nakamura I, Roberts LR, Semin Cancer Biol 2011 21 35 43 10.1016/j.semcancer.2010.10.007 20946957
3. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Amann T, Bataille F, Spruss T, Muhlbauer M, Gabele E, Scholmerich J, Kiefer P, Bosserhoff AK, Hellerbrand C, Cancer Sci 2009 100 646 653 10.1111/j.1349-7006.2009.01087.x 19175606
4. Hepatic stellate cells stimulate HCC cell migration via laminin-5 production. Santamato A, Fransvea E, Dituri F, Caligiuri A, Quaranta M, Niimi T, Pinzani M, Antonaci S, Giannelli G, Clin Sci 2011 121 159 168 10.1042/CS20110002 21413933
5. Activated hepatic stellate cells promote hepatocellular carcinoma development in immunocompetent mice. Zhao W, Zhang L, Yin Z, Su W, Ren G, Zhou C, You J, Fan J, Wang X, Int J Cancer 2011 129 2651 2661 10.1002/ijc.25920 21213212
6. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Mantovani A, Sica A, Allavena P, Garlanda C, Locati M, Hum Immunol 2009 70 325 330 10.1016/j.humimm.2009.02.008 19236898
7. Distinct role of macrophages in different tumor microenvironments. Lewis CE, Pollard JW, Cancer Res 2006 66 605 612 10.1158/0008-5472.CAN-05-4005 16423985
8. Endothelial cells stimulate growth of normal and cancerous breast epithelial cells in 3D culture. Ingthorsson S, Sigurdsson V, Fridriksdottir A Jr, Jonasson JG, Kjartansson J, Magnusson MK, Gudjonsson T, BMC research notes 2010 3 184 10.1186/1756-0500-3-184 20609224
9. Cross talk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells through STAT3/Akt/ERK signaling. Neiva KG, Zhang Z, Miyazawa M, Warner KA, Karl E, Nor JE, Neoplasia 2009 11 583 593 19484147
10. Endothelium-coated tumor clusters are associated with poor prognosis and micrometastasis of hepatocellular carcinoma after resection. Ding T, Xu J, Zhang Y, Guo RP, Wu WC, Zhang SD, Qian CN, Zheng L, Cancer 2011 117 4878 4889 10.1002/cncr.26137 21480209
11. Stepwise metastatic human hepatocellular carcinoma cell model system with multiple metastatic potentials established through consecutive in vivo selection and studies on metastatic characteristics. Li Y, Tian B, Yang J, Zhao L, Wu X, Ye SL, Liu YK, Tang ZY, J Cancer Res Clin Oncol 2004 130 460 468 15146329
12. Identification of metastasis candidate proteins among HCC cell lines by comparative proteome and biological function analysis of S100A4 in metastasis in vitro. Cui JF, Liu YK, Zhang LJ, Shen HL, Song HY, Dai Z, Yu YL, Zhang Y, Sun RX, Chen J, et al. Proteomics 2006 6 5953 5961 10.1002/pmic.200500460 17051636
13. Regulatory mechanisms of interleukin-8 production induced by tumour necrosis factor-alpha in human hepatocellular carcinoma cells. Wang Y, Wang W, Wang L, Wang X, Xia J, J Cell Mol Med 2012 16 496 506 10.1111/j.1582-4934.2011. 01337.x 21545687
14. A three-dimensional cell biology model of human hepatocellular carcinoma in vitro. Tang J, Cui J, Chen R, Guo K, Kang X, Li Y, Gao D, Sun L, Xu C, Chen J, et al. Tumour Biol 2011 32 469 479 10.1007/s13277-010-0140-7 21140254
15. After insufficient radiofrequency ablation, tumor-associated endothelial cells exhibit enhanced angiogenesis and promote invasiveness of residual hepatocellular carcinoma. Kong J, Kong L, Kong J, Ke S, Gao J, Ding X, Zheng L, Sun H, Sun W, J Transl Med 2012 10 230 10.1186/1479-5876-10-230 23171368
16. Vascular changes in hepatocellular carcinoma. Yang ZF, Poon RT, Anatomical record (Hoboken, NJ: 2007) 2008 291 721 734 10.1002/ar.20668
17. Human hepatocellular carcinoma tumor-derived endothelial cells manifest increased angiogenesis capability and drug resistance compared with normal endothelial cells. Xiong YQ, Sun HC, Zhang W, Zhu XD, Zhuang PY, Zhang JB, Wang L, Wu WZ, Qin LX, Tang ZY, Clin Cancer Res 2009 15 4838 4846 10.1158/1078-0432.CCR-08-2780 19638466
18. Overexpression of platelet-derived growth factor receptor alpha in endothelial cells of hepatocellular carcinoma associated with high metastatic potential. Zhang T, Sun HC, Xu Y, Zhang KZ, Wang L, Qin LX, Wu WZ, Liu YK, Ye SL, Tang ZY, Clin Cancer Res 2005 11 8557 8563 10.1158/1078-0432.CCR-05-0944 16361537
19. Endothelial cells and normal breast epithelial cells enhance invasion of breast carcinoma cells by CXCR-4-dependent up-regulation of urokinase-type plasminogen activator receptor (uPAR, CD87) expression. Serrati S, Margheri F, Fibbi G, Di Cara G, Minafra L, Pucci-Minafra I, Liotta F, Annunziato F, Pucci M, Del Rosso M, J Pathol 2008 214 545 554 10.1002/path.2309 18189329
20. Bcl-2 orchestrates a cross-talk between endothelial and tumor cells that promotes tumor growth. Kaneko T, Zhang Z, Mantellini MG, Karl E, Zeitlin B, Verhaegen M, Soengas MS, Lingen M, Strieter RM, Nunez G, Nor JE, Cancer Res 2007 67 9685 9693 10.1158/0008-5472.CAN-07-1497 17942898
21. Stromal endothelial cells directly influence cancer progression. Franses JW, Baker AB, Chitalia VC, Edelman ER, Sci Transl Med 2011 3 66ra65
22. Monocyte chemoattractant protein-1 modulates invasion and apoptosis of PC-3M prostate cancer cells via regulating expression of VEGF, MMP9 and caspase-3. Shi CL, Yu CH, Zhang Y, Zhao D, Chang XH, Wang WH, APJCP 2011 12 555 559 21545229
23. Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. Zhang J, Lu Y, Pienta KJ, J Natl Cancer Inst 2010 102 522 528 10.1093/jnci/djq044 20233997
24. Monocyte chemoattractant protein-1/CCL2 produced by stromal cells promotes lung metastasis of 4T1 murine breast cancer cells. Yoshimura T, Howard OM, Ito T, Kuwabara M, Matsukawa A, Chen K, Liu Y, Liu M, Oppenheim JJ, Wang JM, PLoS One 2013 8 58791 10.1371/journal.pone.0058791 23527025
25. Monocyte chemoattractant protein-1 (MCP-1)/CCL2 secreted by hepatic myofibroblasts promotes migration and invasion of human hepatoma cells. Dagouassat M, Suffee N, Hlawaty H, Haddad O, Charni F, Laguillier C, Vassy R, Martin L, Schischmanoff PO, Gattegno L, et al. Int J Cancer 2010 126 1095 1108 19642141
26. CXCL16 functions as a novel chemotactic factor for prostate cancer cells in vitro. Lu Y, Wang J, Xu Y, Koch AE, Cai Z, Chen X, Galson DL, Taichman RS, Zhang J, Mol Cancer Res 2008 6 546 554 10.1158/1541-7786.MCR-07-0277 18344492
27. High-level expression of chemokine CXCL16 by tumor cells correlates with a good prognosis and increased tumor-infiltrating lymphocytes in colorectal cancer. Hojo S, Koizumi K, Tsuneyama K, Arita Y, Cui Z, Shinohara K, Minami T, Hashimoto I, Nakayama T, Sakurai H, et al. Cancer Res 2007 67 4725 4731 10.1158/0008-5472.CAN-06-3424 17510400
28. Expression and potential function of the CXC chemokine CXCL16 in pancreatic ductal adenocarcinoma. Wente MN, Gaida MM, Mayer C, Michalski CW, Haag N, Giese T, Felix K, Bergmann F, Giese NA, Friess H, Int J Oncol 2008 33 297 308 18636150
29. Chemokine receptor expression profiles in nasopharyngeal carcinoma and their association with metastasis and radiotherapy. Ou DL, Chen CL, Lin SB, Hsu CH, Lin LI, J Pathol 2006 210 363 373 10.1002/path.2053 16955398
30. Overexpression of CXCL16 and its receptor CXCR6/Bonzo promotes growth of human schwannomas. Held-Feindt J, Rehmke B, Mentlein R, Hattermann K, Knerlich F, Hugo HH, Ludwig A, Mehdorn HM, Glia 2008 56 764 774 10.1002/glia.20651 18293410
31. CXCR6 upregulation contributes to a proinflammatory tumor microenvironment that drives metastasis and poor patient outcomes in hepatocellular carcinoma. Gao Q, Zhao YJ, Wang XY, Qiu SJ, Shi YH, Sun J, Yi Y, Shi JY, Shi GM, Ding ZB, et al. Cancer Res 2012 72 3546 3556 10.1158/0008-5472.CAN-11-4032 22710437
32. The interleukin-8 pathway in cancer. Waugh DJ, Wilson C, Clin Cancer Res 2008 14 6735 6741 10.1158/1078-0432.CCR-07-4843 18980965
33. Interleukin-8 is constitutively and commonly produced by various human carcinoma cell-lines. Sakamoto K, Masuda T, Mita S, Ishiko T, Nakashima Y, Arakawa H, Egami H, Harada S, Matsushima K, Ogawa M, Int J Clin Lab Res 1992 22 216 219 10.1007/BF02591427 1334734
34. Interleukin 8 expression regulates tumorigenicity and metastasis in human bladder cancer. Inoue K, Slaton JW, Kim SJ, Perrotte P, Eve BY, Bar-Eli M, Radinsky R, Dinney CP, Cancer Res 2000 60 2290 2299 10786697
35. Interleukin-8 in non-small cell lung carcinoma: relation with angiogenic pattern and p53 alterations. Boldrini L, Gisfredi S, Ursino S, Lucchi M, Mussi A, Basolo F, Pingitore R, Fontanini G, Lung Cancer 2005 50 309 317 10.1016/j.lungcan.2005.07.002 16125276
36. Increased serum interleukin-8 in patients with early and metastatic breast cancer correlates with early dissemination and survival. Benoy IH, Salgado R, Van Dam P, Geboers K, Van Marck E, Scharpe S, Vermeulen PB, Dirix LY, Clin Cancer Res 2004 10 7157 7162 10.1158/1078-0432.CCR-04-0812 15534087
37. Interleukin-8 serum levels in patients with hepatocellular carcinoma: correlations with clinicopathological features and prognosis. Ren Y, Poon RT, Tsui HT, Chen WH, Li Z, Lau C, Yu WC, Fan ST, Clin Cancer Res 2003 9 5996 6001 14676125
38. Enhanced expression and clinical significance of chemokine receptor CXCR2 in hepatocellular carcinoma. Liu Z, Yang L, Xu J, Zhang X, Wang B, J Surg Res 2011 166 241 246 10.1016/j.jss.2009.07.014 20018298
39. Interleukin 8 in human hepatocellular carcinoma correlates with cancer cell invasion of vessels but not with tumor angiogenesis. Kubo F, Ueno S, Hiwatashi K, Sakoda M, Kawaida K, Nuruki K, Aikou T, Ann Surg Oncol 2005 12 800 807 10.1245/ASO.2005.07.015 16132378
40. Survival and apoptosis: a dysregulated balance in liver cancer. Fabregat I, Roncero C, Fernandez M, Liver Int 2007 27 155 162 10.1111/j.1478-3231.2006. 01409.x 17311609
41. MEK/ERK signaling is a critical mediator for integrin-induced cell scattering in highly metastatic hepatocellular carcinoma cells. Honma N, Genda T, Matsuda Y, Yamagiwa S, Takamura M, Ichida T, Aoyagi Y, Lab Invest 2006 86 687 696 10.1038/labinvest.3700427 16636681
42. Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells. Saxena NK, Sharma D, Ding X, Lin S, Marra F, Merlin D, Anania FA, Cancer Res 2007 67 2497 2507 10.1158/0008-5472.CAN-06-3075 17363567
43. Activation of the ERK and AKT signalling pathway predicts poor prognosis in hepatocellular carcinoma and ERK activation in cancer tissue is associated with hepatitis C virus infection. Schmitz KJ, Wohlschlaeger J, Lang H, Sotiropoulos GC, Malago M, Steveling K, Reis H, Cicinnati VR, Schmid KW, Baba HA, J Hepatol 2008 48 83 90 10.1016/j.jhep.2007.08.018 17998146
44. Ardipusilloside inhibits survival, invasion and metastasis of human hepatocellular carcinoma cells. Lou L, Ye W, Chen Y, Wu S, Jin L, He J, Tao X, Zhu J, Chen X, Deng A, Wang J, Phytomedicine 2012 19 603 608 10.1016/j.phymed.2012.01.003 22349030
45. Involvement of PI3K/PTEN/AKT/mTOR pathway in invasion and metastasis in hepatocellular carcinoma: association with MMP-9. Chen JS, Wang Q, Fu XH, Huang XH, Chen XL, Cao LQ, Chen LZ, Tan HX, Li W, Bi J, Zhang LJ, Hepatol Res 2009 39 177 186 10.1111/j.1872-034X.2008.00449.x 19208038
46. CCL2 increases MMP-9 expression and cell motility in human chondrosarcoma cells via the Ras/Raf/MEK/ERK/NF-kappaB signaling pathway. Tang CH, Tsai CC, Biochem Pharmacol 2012 83 335 344 10.1016/j.bcp.2011.11.013 22138288
47. CXCR6 induces prostate cancer progression by the AKT/mammalian target of rapamycin signaling pathway. Wang J, Lu Y, Wang J, Koch AE, Zhang J, Taichman RS, Cancer Res 2008 68 10367 10376 10.1158/0008-5472.CAN-08-2780 19074906
48. Acetaldehyde induces matrix metalloproteinase-9 gene expression via nuclear factor-kappaB and activator protein 1 signaling pathways in human hepatocellular carcinoma cells: association with the invasive potential. Hsiang CY, Wu SL, Chen JC, Lo HY, Li CC, Chiang SY, Wu HC, Ho TY, Toxicol Lett 2007 171 78 86 10.1016/j.toxlet.2007.04.009 17543481
49. Interleukin 17A promotes hepatocellular carcinoma metastasis via NF-kB induced matrix metalloproteinases 2 and 9 expression. Li J, Lau GK, Chen L, Dong SS, Lan HY, Huang XR, Li Y, Luk JM, Yuan YF, Guan XY, PloS one 2011 6 21816 10.1371/journal.pone.0021816 21760911