Plasma miR-185 is decreased in patients with esophageal squamous cell carcinoma and might suppress tumor migration and invasion by targeting RAGE

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 309, Issue 9, 2015, Pages G719-G729

  Jing, Rongrong ^a   Chen, Wen ^a   Wang, Huimin ^a   Ju, Shaoqing ^a   Cong, Hui ^a   Sun, Baolan ^a   Jin, Qin ^a   Chu, Shaopeng ^a   Xu, Lili ^a   Cui, Ming ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Esophageal squamous cell carcinoma; Metastasis; MicroRNA 185; Plasma; Receptor for advanced glycation end products

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; BIOLOGICAL MARKER; HEAT SHOCK PROTEIN 27; KI 67 ANTIGEN; MICRORNA; MICRORNA 185; UNCLASSIFIED DRUG; AGER PROTEIN, HUMAN; HSPB1 PROTEIN, HUMAN; MIRN185 MICRORNA, HUMAN; TUMOR MARKER;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BLOOD LEVEL; CANCER CELL LINE; CANCER PATIENT; CELL INVASION ASSAY; CELL MIGRATION ASSAY; CELL VIABILITY; CONTROLLED STUDY; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUCIFERASE ASSAY; LUNG METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; TUMOR INVASION; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BIOLOGY; BLOOD; CARCINOMA, SQUAMOUS CELL; CELL MOTION; CELL PROLIFERATION; DOWN REGULATION; DRUG SCREENING; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION; GENE THERAPY; GENETIC DATABASE; GENETIC TRANSFECTION; GENETICS; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PROCEDURES; SECONDARY; SIGNAL TRANSDUCTION; TIME; TUMOR CELL LINE; TUMOR VOLUME; VERY ELDERLY;

ADULT; ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; AGED; AGED, 80 AND OVER; ANIMALS; BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DOWN-REGULATION; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC THERAPY; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84946214504     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00078.2015     Document Type: Article

References (44)

1. Boone BA, Orlichenko L, Schapiro NE, Loughran P, Gianfrate GC, Ellis JT, Singhi AD, Kang R, Tang D, Lotze MT, Zeh HJ. The receptor for advanced glycation end products (RAGE) enhances autophagy and neutrophil extracellular traps in pancreatic cancer. Cancer Gene Ther 22: 326–334, 2015
2. Chen TS, Lai RC, Lee MM, Choo AB, Lee CN, Lim SK. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res 38: 215–224, 2010
3. Chen X, Zhang L, Zhang IY, Liang J, Wang H, Ouyang M, Wu S, da Fonseca AC, Weng L, Yamamoto Y, Yamamoto H, Natarajan R, Badie B. RAGE expression in tumor-associated macrophages promotes angiogenesis in glioma. Cancer Res 74: 7285–7297, 2014
4. Cheng M, Liu H, Zhang D, Liu Y, Wang C, Liu F, Chen J. HMGB1 enhances the AGE-induced expression of CTGF and TGF-β via RAGEdependent signaling in renal tubular epithelial cells. Am J Nephrol 41: 257–266, 2015
5. Dahlmann M, Okhrimenko A, Marcinkowski P, Osterland M, Herrmann P, Smith J, Heizmann CW, Schlag PM, Stein U. RAGE mediates S100A4-induced cell motility via MAPK/ERK and hypoxia signaling and is a prognostic biomarker for human colorectal cancer metastasis. Oncotarget 5: 3220–3233, 2014
6. Ding DP, Chen ZL, Zhao XH, Wang JW, Sun J, Wang Z, Tan FW, Tan XG, Li BZ, Zhou F, Shao K, Li N, Qiu B, He J. miR-29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression. Carcinogenesis 32: 1025–1032, 2011
7. During RL, Gibson BG, Li W, Bishai EA, Sidhu GS, Landry J, Southwick FS. Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. EMBO J 26: 2240–2250, 2007
8. Elangovan I, Thirugnanam S, Chen A, Zheng G, Bosland MC, Kajdacsy- Balla A, Gnanasekar M. Targeting receptor for advanced glycation end products (RAGE) expression induces apoptosis and inhibits prostate tumor growth. Biochem Biophys Res Commun 417: 1133–1138, 2012
9. Hamano R, Miyata H, Yamasaki M, Kurokawa Y, Hara J, Moon JH, Nakajima K, Takiguchi S, Fujiwara Y, Mori M, Doki Y. Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res 17: 3029–3038, 2011
10. Huang Z, Huang S, Wang Q, Liang L, Ni S, Wang L, Sheng W, He X, Du X. MicroRNA-95 promotes cell proliferation and targets sorting Nexin 1 in human colorectal carcinoma. Cancer Res 71: 2582–2589, 2011
11. Iwasaki YW, Kiga K, Kayo H, Fukuda-Yuzawa Y, Weise J, Inada T, Tomita M, Ishihama Y, Fukao T. Global microRNA elevation by inducible Exportin 5 regulates cell cycle entry. RNA 19: 490–497, 2013
12. James EN, Delany AM, Nair LS. Post-transcriptional regulation in osteoblasts using localized delivery of miR-29a inhibitor from nanofibers to enhance extracellular matrix deposition. Acta Biomater 10: 3571–3580, 2014
13. Jing RR, Cui M, Sun BL, Yu J, Wang HM. Tissue-specific expression profiling of receptor for advanced glycation end products and its soluble forms in esophageal and lung cancer. Genet Test Mol Biomarkers 14: 55–361, 2010
14. Jing RR, Wang HM, Jiang SY, Zhang QZ. Up regulation of RAGE in esophageal cancer and down regulation in lung cancer and their relationship to clinicopathological features. Lab Med 39: 661–667, 2008
15. Ko SY, Ko HA, Shieh TM, Chang WC, Chen HI, Chang SS, Lin IH. Cell migration is regulated by AGE-RAGE interaction in human oral cancer cells in vitro. PLoS One 9: e110542, 2014
16. Kong KL, Kwong DL, Chan TH, Law SY, Chen L, Li Y, Qin YR, Guan XY. MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 61: 33–42, 2012
17. Lakshman M, Xu L, Ananthanarayanan V, Cooper J, Takimoto CH, Helenowski I, Pelling JC, Bergan RC. Dietary genistein inhibits metastasis of human prostate cancer in mice. Cancer Res 68: 2024–2032, 2008
18. Li HP, Zeng XC, Zhang B, Long JT, Zhou B, Tan GS, Zeng WX, Chen W, Yang JY. miR-451 inhibits cell proliferation in human hepatocellular carcinoma through direct suppression of IKK-_. Carcinogenesis 34: 2443–2451, 2013
19. Li Q, Wang JX, He YQ, Feng C, Zhang XJ, Sheng JQ, Li PF. MicroRNA-185 regulates chemotherapeutic sensitivity in gastric cancer by targeting apoptosis repressor with caspase recruitment domain. Cell Death Dis 5: e1197, 2014
20. Liao X, Xue H, Wang YC, Nazor KL, Guo S, Trivedi N, Peterson SE, Liu Y, Loring JF, Laurent LC. Matched miRNA and mRNA signatures from a hESC-based in vitro model of pancreatic differentiation reveal novel regulatory interactions. J Cell Sci 126: 3848–3861, 2013
21. Liu M, Lang N, Chen X, Tang Q, Liu S, Huang J, Zheng Y, Bi F. miR-185 targets RhoA and Cdc42 expression and inhibits the proliferation potential of human colorectal cells. Cancer Lett 301: 151–160, 2011
22. Malik P, Chaudhry N, Mittal R, Mukherjee TK. Role of receptor for advanced glycation end products in the complication and progression of various types of cancers. Biochim Biophys Acta 1850: 1898–1904, 2015
23. Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, Lim B, Rigoutsos I. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126: 1203–1217, 2006
24. Nasser MW, Wani NA, Ahirwar DK, Powell CA, Ravi J, Elbaz M, Zhao H, Padilla L, Zhang X, Shilo K, Ostrowski M, Shapiro C, Carson WE 3rd, Ganju RK. RAGE mediates S100A7-induced breast cancer growth and metastasis by modulating the tumor microenvironment. Cancer Res 75: 974–985, 2015
25. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stern D, Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 267: 14998–15004, 1992
26. Osbourne A, Calway T, Broman M, McSharry S, Earley J, Kim GH. Downregulation of Connexin43 by microRNA-130a in cardiomyocytes results in cardiac arrhythmias. J Mol Cell Cardiol 74: 53–63, 2014
27. Pigati L, Yaddanapudi SC, Iyengar R, Kim DJ, Hearn SA, Danforth D, Hastings ML, Duelli DM. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One 5: e13515, 2010
28. Pu XX, Huang GL, Guo HQ, Guo CC, Li H, Ye S, Ling S, Jiang L, Tian Y, Lin TY. Circulating miR-221 directly amplified from plasma is a potential diagnostic and prognostic marker of colorectal cancer and is correlated with p53 expression. J Gastroenterol Hepatol 25: 1674–1680, 2010
29. Qu F, Cui X, Hong Y, Wang J, Li Y, Chen L, Liu Y, Gao Y, Xu D, Wang Q. MicroRNA-185 suppresses proliferation, invasion, migration, and tumorigenicity of human prostate cancer cells through targeting androgen receptor. Mol Cell Biochem 377: 121–130, 2013
30. Sugaya K, Fukagawa T, Matsumoto K, Mita K, Takahashi E, Ando A, Inoko H, Ikemura T. Three genes in the human MHC class III region near the junction with the class II: gene for receptor of advanced glycosylation end products, PBX2 homeobox gene and a notch homolog, human counterpart of mouse mammary tumor gene int-3. Genomics 23: 408–419, 1994
31. Tang H, Liu P, Yang L, Xie X, Ye F, Wu M, Liu X, Chen B, Zhang L, Xie X. miR-185 suppresses tumor proliferation by directly targeting E2F6 and DNMT1 and indirectly upregulating BRCA1 in triple-negative breast cancer. Mol Cancer Ther 13: 3185–3197, 2014
32. Tang H, Wang Z, Liu X, Liu Q, Xu G, Li G, Wu M. LRRC4 inhibits glioma cell growth and invasion through a miR-185-dependent pathway. Curr Cancer Drug Targets 12: 1032–1042, 2012
33. Toiyama Y, Takahashi M, Hur K, Nagasaka T, Tanaka K, Inoue Y, Kusunoki M, Boland CR, Goel A. Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J Natl Cancer Inst 105: 849–859, 2013
34. Tsujiura M, Komatsu S, Ichikawa D, Shiozaki A, Konishi H, Takeshita H, Moriumura R, Nagata H, Kawaguchi T, Hirajima S, Arita T, Fujiwara H, Okamoto K, Otsuji E. Circulating miR-18a in plasma contributes to cancer detection and monitoring in patients with gastric cancer. Gastric Cancer 18: 271–279, 2015
35. Villegas-Ruiz V, Juárez-Méndez S, Pérez-González OA, Arreola H, Paniagua-García L, Parra-Melquiadez M, Peralta-Rodríguez R, López-Romero R, Monroy-García A, Mantilla-Morales A, Gómez- Gutiérrez G, Román-Bassaure E, Salcedo M. Heterogeneity of microRNAs expression in cervical cancer cells: over -expression of miR-196a. Int J Clin Exp Pathol 7: 1389–1401, 2014
36. Wang B, Li J, Sun M, Sun L, Zhang X. miRNA expression in breast cancer varies with lymph node metastasis and other clinicopathologic features. IUBMB Life 66: 371–377, 2014
37. Wu R, Duan L, Cui F, Cao J, Xiang Y, Tang Y, Zhou L. S100A9 promotes human hepatocellular carcinoma cell growth and invasion through RAGE-mediated ERK1/2 and p38 MAPK pathways. Exp Cell Res 334: 228–238, 2015
38. Xiong X, Wang Y, Liu C, Lu Q, Liu T, Chen G, Rao H, Luo S. Heat shock protein 90β stabilizes focal adhesion kinase and enhances cell migration and invasion in breast cancer cells. Exp Cell Res 326: 78–89, 2014
39. Xu F, Zhang H, Su Y, Kong J, Yu H, Qian B. Up-regulation of microRNA-183-3p is a potent prognostic marker for lung adenocarcinoma of female non-smokers. Clin Transl Oncol 16: 980–985, 2014
40. Xu XC, Abuduhadeer X, Zhang WB, Li T, Gao H, Wang YH. Knockdown of RAGE inhibits growth and invasion of gastric cancer cells. Eur J Histochem 57: e36, 2013
41. Yang J, Zhang Z, Chen C, Liu Y, Si Q, Chuang TH, Li N, Gomez- Cabrero A, Reisfeld RA, Xiang R, Luo Y. MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene. Oncogene 33: 3014–3023, 2014
42. Yang S, Li Y, Gao J, Zhang T, Li S, Luo A, Chen H, Ding F, Wang X, Liu Z. MicroRNA -34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Oncogene 32: 4294–4303, 2013
43. Zhang J, Luo X, Li H, Yue X, Deng L, Cui Y, Lu Y. MicroRNA-223 functions as an oncogene in human colorectal cancer cells. Oncol Rep 32: 115–120, 2014
44. Zhou X, Zhang CZ, Lu SX, Chen GG, Li LZ, Liu LL, Yi C, Fu J, Hu W, Wen JM, Yun JP. miR-625 suppresses tumour migration and invasion by targeting IGF2BP1 in hepatocellular carcinoma. Oncogene 34: 965–977, 2015.