MicroRNA-27b, microRNA-101 and microRNA-128 inhibit angiogenesis by down-regulating vascular endothelial growth factor C expression in gastric cancers

Oncotarget

Volumn 6, Issue 35, 2015, Pages 37458-37470

  Liu, Hai Ting ^a   Xing, Ai Yan ^a   Chen, Xu ^a   Ma, Ran Ran ^a   Wang, Ya Wen ^a   Shi, Duan Bo ^a   Zhang, Hui ^a   Li, Peng ^a   Chen, Hong Fang ^a,b   Li, Yu Hong ^a,c   Gao, Peng ^a  

^a SHANDONG UNIVERSITY   (China)

^b Department of Pathology   (China)

^c LIAOCHENG PEOPLE'S HOSPITAL   (China)

Author keywords

Angiogenesis; Gastric cancer; MicroRNA 101; MicroRNA 128; MicroRNA 27b

Indexed keywords

MICRORNA; MICRORNA 101; MICRORNA 128; MICRORNA 27B; UNCLASSIFIED DRUG; VASCULOTROPIN C; MIRN101 MICRORNA, HUMAN; MIRN128 MICRORNA, HUMAN; MIRN27 MICRORNA, HUMAN; VEGFC PROTEIN, HUMAN;

ADULT; ANTIANGIOGENIC ACTIVITY; ARTICLE; BLOOD VESSEL DENSITY; BLOOD VESSEL PARAMETERS; CANCER CLASSIFICATION; CANCER PROGNOSIS; CANCER SIZE; CANCER STAGING; CANCER SURVIVAL; CANCER TISSUE; CAPILLARY DENSITY; CELL INVASION ASSAY; CELL MIGRATION ASSAY; CELL PROLIFERATION ASSAY; CELLULAR PARAMETERS; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GASTRIC CANCER CELL LINE; GENE FUNCTION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUCIFERASE ASSAY; LYMPH VESSEL DENSITY; LYMPHATIC DENSITY; MAJOR CLINICAL STUDY; MALE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; STOMACH CANCER; TUBE FORMATION; TUMOR SUPPRESSOR GENE; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; CELL MOTION; CELL PROLIFERATION; GASTRECTOMY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; KAPLAN MEIER METHOD; LYMPH VESSEL; METABOLISM; MICROVASCULATURE; MIDDLE AGED; MORTALITY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTOR; TREATMENT OUTCOME; TUMOR CELL LINE; TUMOR INVASION; TUMOR VOLUME; VASCULARIZATION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; GASTRECTOMY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; KAPLAN-MEIER ESTIMATE; LYMPHATIC VESSELS; MALE; MICRORNAS; MICROVESSELS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTORS; TRANSFECTION; TREATMENT OUTCOME; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 84947708354     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6059     Document Type: Article

References (34)

1. Wang J, Wang Q, Liu H, Hu B, Zhou W, Cheng Y. MicroRNA expression and its implication for the diagnosis and therapeutic strategies of gastric cancer. Cancer Lett. 2010;297:137-143.
2. Huang J, Yang Y, Yang J, Li X. Regenerating gene family member 4 promotes growth and migration of gastric cancer through protein kinase B pathway. Int J Clin Exp Med. 2014;7:3037-3044.
3. Le XF, Merchant O, Bast RC, Calin GA. The Roles of MicroRNAs in the Cancer Invasion-Metastasis Cascade. Cancer Microenviron. 2010;3:137-147.
4. Bockhorn M, Jain RK, Munn LL. Active versus passive mechanisms in metastasis: do cancer cells crawl into vessels, or are they pushed? Lancet Oncol. 2007;8:444-448.
5. Maehara Y, Kabashima A, Koga T, Tokunaga E, Takeuchi H, Kakeji Y, Sugimachi K. Vascular invasion and potential for tumor angiogenesis and metastasis in gastric carcinoma. Surgery. 2000;128:408-416.
6. Joukov V, Sorsa T, Kumar V, Jeltsch M, Claesson-Welsh L, Cao Y, Saksela O, Kalkkinen N, Alitalo K. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 1997;16:3898-3911.
7. Kaushal V, Mukunyadzi P, Dennis RA, Siegel ER, Johnson DE, Kohli M. Stage-specific characterization of the vascular endothelial growth factor axis in prostate cancer: expression of lymphangiogenic markers is associated with advancedstage disease. Clin Cancer Res. 2005;11:584-593.
8. Witte D, Thomas A, Ali N, Carlson N, Younes M. Expression of the vascular endothelial growth factor receptor-3 (VEGFR-3) and its ligand VEGF-C in human colorectal adenocarcinoma. Anticancer Res. 2002;22:1463-1466.
9. Wang HJ, Ruan HJ, He XJ, Ma YY, Jiang XT, Xia YJ, Ye ZY, Tao HQ. MicroRNA-101 is down-regulated in gastric cancer and involved in cell migration and invasion. Eur J Cancer. 2010;46:2295-2303.
10. Gao Y, Zeng F, Wu JY, Li HY, Fan JJ, Mai L, Zhang J, Ma DM, Li Y, Song FZ. MiR-335 inhibits migration of breast cancer cells through targeting oncoprotein c-Met. Tumour Biol. 2015;36:2875-83.
11. Bin Z, Dedong H, Xiangjie F, Hongwei X, Qinghui Y. The MicroRNA-367 Inhibits the Invasion and Metastasis of Gastric Cancer by Directly Repressing Rab23. Genet Test Mol Biomarkers. 2015;19:69-74.
12. Wang SH, Zhou JD, He QY, Yin ZQ, Cao K, Luo CQ. MiR-199a inhibits the ability of proliferation and migration by regulating CD44-Ezrin signaling in cutaneous squamous cell carcinoma cells. Int J Clin Exp Pathol. 2014;7:7131-7141.
13. Su JL, Yen CJ, Chen PS, Chuang SE, Hong CC, Kuo IH, Chen HY, Hung MC, Kuo ML. The role of the VEGF-C/VEGFR-3 axis in cancer progression. Br J Cancer. 2007;96:541-545.
14. Rutkowski JM, Boardman KC, Swartz MA. Characterization of lymphangiogenesis in a model of adult skin regeneration. Am J Physiol Heart Circ Physiol. 2006;291:H1402-1410.
15. Khromova N, Kopnin P, Rybko V, Kopnin BP. Downregulation of VEGF-C expression in lung and colon cancer cells decelerates tumor growth and inhibits metastasis via multiple mechanisms. Oncogene. 2012;31:1389-1397.
16. Da MX, Zhang YB, Yao JB, Duan YX. DNA methylation regulates expression of VEGF-C, and S-adenosylmethionine is effective for VEGF-C methylation and for inhibiting cancer growth. Braz J Med Biol Res. 2014;47:1021-1028.
17. Cheng HT, Hung WC. Inhibition of lymphangiogenic factor VEGF-C expression and production by the histone deacetylase inhibitor suberoylanilide hydroxamic acid in breast cancer cells. Oncol Rep. 2013;29:1238-1244.
18. Engelmann D, Mayoli-Nussle D, Mayrhofer C, Furst K, Alla V, Stoll A, Spitschak A, Abshagen K, Vollmar B, Ran S, Putzer BM. E2F1 promotes angiogenesis through the VEGF-C/VEGFR-3 axis in a feedback loop for cooperative induction of PDGF-B. J Mol Cell Biol. 2013;5:391-403.
19. Sun L, Duan J, Jiang Y, Wang L, Huang N, Lin L, Liao Y, Liao W. Metastasis-associated in colon cancer-1 upregulates vascular endothelial growth factor-C/D to promote lymphangiogenesis in human gastric cancer. Cancer Lett. 2015;357:242-253.
20. Shah MY, Calin GA. MicroRNAs as therapeutic targets in human cancers. Wiley Interdiscip Rev RNA. 2014;5:537-548.
21. Ye J, Wu X, Wu D, Wu P, Ni C, Zhang Z, Chen Z, Qiu F, Xu J, Huang J. miRNA-27b targets vascular endothelial growth factor C to inhibit tumor progression and angiogenesis in colorectal cancer. PLoS One. 2013;8:e60687.
22. Lei Y, Li B, Tong S, Qi L, Hu X, Cui Y, Li Z, He W, Zu X, Wang Z, Chen M. miR-101 suppresses vascular endothelial growth factor C that inhibits migration and invasion and enhances cisplatin chemosensitivity of bladder cancer cells. PLoS One. 2015;10:e0117809.
23. Hu J, Cheng Y, Li Y, Jin Z, Pan Y, Liu G, Fu S, Zhang Y, Feng K, Feng Y. microRNA-128 plays a critical role in human non-small cell lung cancer tumourigenesis, angiogenesis and lymphangiogenesis by directly targeting vascular endothelial growth factor-C. Eur J Cancer. 2014;50:2336-2350.
24. Yan X, Chen X, Liang H, Deng T, Chen W, Zhang S, Liu M, Gao X, Liu Y, Zhao C, Wang X, Wang N, Li J, et al. miR-143 and miR-145 synergistically regulate ERBB3 to suppress cell proliferation and invasion in breast cancer. Mol Cancer. 2014;13:220.
25. Chen B, Duan L, Yin G, Tan J, Jiang X. Simultaneously expressed miR-424 and miR-381 synergistically suppress the proliferation and survival of renal cancer cells-Cdc2 activity is up-regulated by targeting WEE1. Clinics (Sao Paulo). 2013;68:825-833.
26. Derfoul A, Juan AH, Difilippantonio MJ, Palanisamy N, Ried T, Sartorelli V. Decreased microRNA-214 levels in breast cancer cells coincides with increased cell proliferation, invasion and accumulation of the Polycomb Ezh2 methyltransferase. Carcinogenesis. 2011;32:1607-1614.
27. Li MH, Fu SB, Xiao HS. Genome-wide analysis of microRNA and mRNA expression signatures in cancer. Acta Pharmacol Sin. 2015;36:1200-11.
28. Gao P, Zhou GY, Zhang QH, Su ZX, Zhang TG, Xiang L, Wang Y, Zhang SL, Mu K. Lymphangiogenesis in gastric carcinoma correlates with prognosis. J Pathol. 2009;218:192-200.
29. Dumoff KL, Chu C, Xu X, Pasha T, Zhang PJ, Acs G. Low D2-40 immunoreactivity correlates with lymphatic invasion and nodal metastasis in early-stage squamous cell carcinoma of the uterine cervix. Mod Pathol. 2005;18:97-104.
30. Wang X, Chen X, Fang J, Yang C. Overexpression of both VEGF-A and VEGF-C in gastric cancer correlates with prognosis, and silencing of both is effective to inhibit cancer growth. Int J Clin Exp Pathol. 2013;6:586-597.
31. Gao P, Wong CC, Tung EK, Lee JM, Wong CM, Ng IO. Deregulation of microRNA expression occurs early and accumulates in early stages of HBV-associated multistep hepatocarcinogenesis. J Hepatol. 2011;54:1177-1184.
32. Fanelli R, Schembri L, Piarulli U, Pinoli M, Rasini E, Paolillo M, Galiazzo MC, Cosentino M, Marino F. Effects of a novel cyclic RGD peptidomimetic on cell proliferation, migration and angiogenic activity in human endothelial cells. Vasc Cell. 2014;6:11.
33. Pourgholami MH, Khachigian LM, Fahmy RG, Badar S, Wang L, Chu SW, Morris DL. Albendazole inhibits endothelial cell migration, tube formation, vasopermeability, VEGF receptor-2 expression and suppresses retinal neovascularization in ROP model of angiogenesis. Biochem Biophys Res Commun. 2010;397:729-734.
34. Sun D, Liu Y, Yu Q, Zhou Y, Zhang R, Chen X, Hong A, Liu J. The effects of luminescent ruthenium(II) polypyridyl functionalized selenium nanoparticles on bFGF-induced angiogenesis and AKT/ERK signaling. Biomaterials.2013;34:171-180.