MiR1 suppresses the growth of esophageal squamous cell carcinoma in vivo and in vitro through the downregulation of MET, cyclin D1 and CDK4 expression

International Journal of Molecular Medicine

Volumn 38, Issue 1, 2016, Pages 113-122

  Jiang, Sen ^a,b   Zhao, Chao ^a,b   Yang, Xiaodi ^c   Li, Xiangyang ^a,b   Pan, Qing ^d   Huang, Haijin ^a,b   Wen, Xuyang ^a,b   Shan, Husheng ^a,b   Li, Qianwen ^a,b   Du, Yunxiang ^a,b   Zhao, Yaping ^a,b  

^a The 82nd Hospital of the People's Liberation Army   (China)

^b BENGBU MEDICAL COLLEGE   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d Huaiyin Hospital of Huaian City   (China)

Author keywords

Cyclin D1; Cyclin dependent kinase 4; Esophageal squamous cell carcinoma; MET; MicroRNA; MicroRNA1

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 4; MICRORNA 1; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; 3' UNTRANSLATED REGION; CCND1 PROTEIN, HUMAN; CDK4 PROTEIN, HUMAN; LUCIFERASE; MICRORNA; MIRN1 MICRORNA, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOINFORMATICS; CANCER INHIBITION; CARCINOGENESIS; CARCINOMA CELL; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE MODEL; MTT ASSAY; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA CELL LINE; TRYPAN BLUE ASSAY; TUMOR XENOGRAFT; 3' UNTRANSLATED REGION; ANIMAL; BAGG ALBINO MOUSE; DRUG SCREENING; ESOPHAGUS TUMOR; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MIDDLE AGED; NUCLEOTIDE SEQUENCE; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ANIMALS; APOPTOSIS; BASE SEQUENCE; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; DOWN-REGULATION; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; LUCIFERASES; MALE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; PROTO-ONCOGENE PROTEINS C-MET; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84978820234     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2016.2619     Document Type: Article

References (55)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127: 2893-2917, 2010.
2. Vizcaino AP, Moreno V, Lambert R and Parkin DM: Time trends incidence of both major histologic types of esophageal carcinomas in selected countries, 1973-1995. Int J Cancer 99: 860-868, 2002.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin 61: 69-90, 2011.
4. Layke JC and Lopez PP: Esophageal cancer: a review and update. Am Fam Physician 73: 2187-2194, 2006.
5. Stoner GD and Wang LS: Chemoprevention of esophageal squamous cell carcinoma with berries. Top Curr Chem 329: 1-20, 2013.
6. Kamangar F, Chow WH, Abnet CC and Dawsey SM: Environmental causes of esophageal cancer. Gastroenterol Clin North Am 38: 27-57, 2009.
7. Hyland PL, Freedman ND, Hu N, Tang ZZ, Wang L, Wang C, Ding T, Fan JH, Qiao YL, Golozar A, et al: Genetic variants in sex hormone metabolic pathway genes and risk of esophageal squamous cell carcinoma. Carcinogenesis 34: 1062-1068, 2013.
8. Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866, 2006.
9. Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004.
10. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004, 2004.
11. Wu BL, Xu LY, Du ZP, Liao LD, Zhang HF, Huang Q, Fang GQ and Li EM: MiRNA profile in esophageal squamous cell carcinoma: downregulation of miR143 and miR145. World J Gastroenterol 17: 79-88, 2011.
12. Tsuchiya S, Fujiwara T, Sato F, Shimada Y, Tanaka E, Sakai Y, Shimizu K and Tsujimoto G: MicroRNA-210 regulates cancer cell proliferation through targeting fibroblast growth factor receptor-like 1 (FGFRL1). J Biol Chem 286: 420-428, 2011.
13. Kong KL, Kwong DL, Chan TH, Law SY, Chen L, Li Y, Qin YR and 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.
14. Kang M, Li Y, Liu W, Wang R, Tang A, Hao H, Liu Z and Ou H: miR129-2 suppresses proliferation and migration of esophageal carcinoma cells through downregulation of SOX4 expression. Int J Mol Med 32: 51-58, 2013.
15. Wang N, Zhang CQ, He JH, Duan XF, Wang YY, Ji X, Zang WQ, Li M, Ma YY, Wang T and Zhao GQ: MiR21 down-regulation suppresses cell growth, invasion and induces cell apoptosis by targeting FASL, TIMP3, and RECK genes in esophageal carcinoma. Dig Dis Sci 58: 1863-1870, 2013.
16. Ni Y, Meng L, Wang L, Dong W, Shen H, Wang G, Liu Q and Du J: MicroRNA-143 functions as a tumor suppressor in human esophageal squamous cell carcinoma. Gene 517: 197-204, 2013.
17. Zhang M, Zhou S, Zhang L, Zhang J, Cai H, Zhu J, Huang C and Wang J: miR518b is down-regulated, and involved in cell proliferation and invasion by targeting Rap1b in esophageal squamous cell carcinoma. FEBS Lett 586: 3508-3521, 2012.
18. Tao J, Wu D, Xu B, Qian W, Li P, Lu Q, Yin C and Zhang W: microRNA-133 inhibits cell proliferation, migration and invasion in prostate cancer cells by targeting the epidermal growth factor receptor. Oncol Rep 27: 1967-1975, 2012.
19. Ding DP, Chen ZL, Zhao XH, Wang JW, Sun J, Wang Z, Tan FW, Tan XG, Li BZ, Zhou F, et al: miR29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression. Carcinogenesis 32: 1025-1032, 2011.
20. Fu HL, Wu P, Wang XF, Wang JG, Jiao F, Song LL, Xie H, Wen XY, Shan HS, Du YX and Zhao YP: Altered miRNA expression is associated with differentiation, invasion, and metastasis of esophageal squamous cell carcinoma (ESCC) in patients from Huaian, China. Cell Biochem Biophys 67: 657-668, 2013.
21. Novello C, Pazzaglia L, Cingolani C, Conti A, Quattrini I, Manara MC, Tognon M, Picci P and Benassi MS: miRNA expression profile in human osteosarcoma: role of miR1 and miR133b in proliferation and cell cycle control. Int J Oncol 42: 667-675, 2013.
22. Nohata N, Hanazawa T, Enokida H and Seki N: microRNA1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers. Oncotarget 3: 9-21, 2012.
23. Hou G, Zhang Q, Wang L, Liu M, Wang J and Xue L: mTOR inhibitor rapamycin alone or combined with cisplatin inhibits growth of esophageal squamous cell carcinoma in nude mice. Cancer Lett 290: 248-254, 2010.
24. Wang F, Zhang P, Ma Y, Yang J, Moyer MP, Shi C, Peng J and Qin H: NIRF is frequently upregulated in colorectal cancer and its oncogenicity can be suppressed by let-7a microRNA. Cancer Lett 314: 223-231, 2012.
25. Matsushima K, Isomoto H, Yamaguchi N, Inoue N, Machida H, Nakayama T, Hayashi T, Kunizaki M, Hidaka S, Nagayasu T, et al: MiRNA-205 modulates cellular invasion and migration via regulating zinc finger E-box binding homeobox 2 expression in esophageal squamous cell carcinoma cells. J Transl Med 9: 30, 2011.
26. Guo Y, Chen Z, Zhang L, Zhou F, Shi S, Feng X, Li B, Meng X, Ma X, Luo M, et al: Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res 68: 26-33, 2008.
27. Leidner RS, Ravi L, Leahy P, Chen Y, Bednarchik B, Streppel M, Canto M, Wang JS, Maitra A, Willis J, et al: The microRNAs, MiR31 and MiR375, as candidate markers in Barrett's esophageal carcinogenesis. Genes Chromosomes Cancer 51: 473-479, 2012.
28. Lee KH, Goan YG, Hsiao M, Lee CH, Jian SH, Lin JT, Chen YL and Lu PJ: MicroRNA-373 (miR373) post-transcriptionally regulates large tumor suppressor, homolog 2 (LATS2) and stimulates proliferation in human esophageal cancer. Exp Cell Res 315: 2529-2538, 2009.
29. Yokobori T, Suzuki S, Tanaka N, Inose T, Sohda M, Sano A, Sakai M, Nakajima M, Miyazaki T, Kato H and Kuwano H: MiR150 is associated with poor prognosis in esophageal squamous cell carcinoma via targeting the EMT inducer ZEB1. Cancer Sci 104: 48-54, 2013.
30. Takeshita N, Mori M, Kano M, Hoshino I, Akutsu Y, Hanari N, Yoneyama Y, Ikeda N, Isozaki Y, Maruyama T, et al: miR203 inhibits the migration and invasion of esophageal squamous cell carcinoma by regulating LASP1. Int J Oncol 41: 1653-1661, 2012.
31. Yamamoto N, Kinoshita T, Nohata N, Itesako T, Yoshino H, Enokida H, Nakagawa M, Shozu M and Seki N: Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion by targeting focal adhesion pathways in cervical squamous cell carcinoma. Int J Oncol 42: 1523-1532, 2013.
32. Leone V, D'Angelo D, Rubio I, de Freitas PM, Federico A, Colamaio M, Pallante P, Medeiros-Neto G and Fusco A: MiR1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4, and SDF-1alpha. J Clin Endocrinol Metab 96: E1388-E1398, 2011.
33. Li D, Yang P, Li H, Cheng P, Zhang L, Wei D, Su X, Peng J, Gao H, Tan Y, et al: MicroRNA-1 inhibits proliferation of hepatocarcinoma cells by targeting endothelin-1. Life Sci 91: 440-447, 2012.
34. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, Yi M, Stephens RM, Seng V, Sheppard-Tillman H, et al: MiR1 and miR200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 32: 296-306, 2013.
35. Nohata N, Sone Y, Hanazawa T, Fuse M, Kikkawa N, Yoshino H, Chiyomaru T, Kawakami K, Enokida H, Nakagawa M, et al: miR1 as a tumor suppressive microRNA targeting TAGLN2 in head and neck squamous cell carcinoma. Oncotarget 2: 29-42, 2011.
36. Taulli R, Bersani F, Foglizzo V, Linari A, Vigna E, Ladanyi M, Tuschl T and Ponzetto C: The muscle-specific microRNA miR206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. J Clin Invest 119: 2366-2378, 2009.
37. Wu CD, Kuo YS, Wu HC and Lin CT: MicroRNA-1 induces apoptosis by targeting prothymosin alpha in nasopharyngeal carcinoma cells. J Biomed Sci 18: 80, 2011.
38. Nohata N, Hanazawa T, Kikkawa N, Sakurai D, Fujimura L, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nakagawa M, et al: Tumour suppressive microRNA-874 regulates novel cancer networks in maxillary sinus squamous cell carcinoma. Br J Cancer 105: 833-841, 2011.
39. Nohata N, Hanazawa T, Kikkawa N, Sakurai D, Sasaki K, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nakagawa M, et al: Identification of novel molecular targets regulated by tumor suppressive miR1/miR133a in maxillary sinus squamous cell carcinoma. Int J Oncol 39: 1099-1107, 2011.
40. Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nohata N, Fuse M, Ichikawa T, Naya Y, Nakagawa M and Seki N: Tumour suppressors miR1 and miR133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer 106: 405-413, 2012.
41. Brennecke J, Stark A, Russell RB and Cohen SM: Principles of microRNA-target recognition. PLoS Biol 3: e85, 2005.
42. Kato H, Arao T, Matsumoto K, Fujita Y, Kimura H, Hayashi H, Nishiki K, Iwama M, Shiraishi O, Yasuda A, et al: Gene amplification of EGFR, HER2, FGFR2 and MET in esophageal squamous cell carcinoma. Int J Oncol 42: 1151-1158, 2013.
43. Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H and Rustgi AK: Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc Natl Acad Sci USA 107: 11026-11031, 2010.
44. Leelawat K, Leelawat S, Tepaksorn P, Rattanasinganchan P, Leungchaweng A, Tohtong R and Sobhon P: Involvement of c-Met/hepatocyte growth factor pathway in cholangiocarcinoma cell invasion and its therapeutic inhibition with small interfering RNA specific for c-Met. J Surg Res 136: 78-84, 2006.
45. Ketterer K, Kong B, Frank D, Giese NA, Bauer A, Hoheisel J, Korc M, Kleeff J, Michalski CW and Friess H: Neuromedin U is overexpressed in pancreatic cancer and increases invasiveness via the hepatocyte growth factor c-Met pathway. Cancer Lett 277: 72-81, 2009.
46. Zeng ZS, Weiser MR, Kuntz E, Chen CT, Khan SA, Forslund A, Nash GM, Gimbel M, Yamaguchi Y, Culliford AT IV, et al: c-Met gene amplification is associated with advanced stage colorectal cancer and liver metastases. Cancer Lett 265: 258-269, 2008.
47. Ke AW, Shi GM, Zhou J, Wu FZ, Ding ZB, Hu MY, Xu Y, Song ZJ, Wang ZJ, Wu JC, et al: Role of overexpression of CD151 and/or c-Met in predicting prognosis of hepatocellular carcinoma. Hepatology 49: 491-503, 2009.
48. Drebber U, Baldus SE, Nolden B, Grass G, Bollschweiler E, Dienes HP, Hölscher AH and Mönig SP: The overexpression of c-met as a prognostic indicator for gastric carcinoma compared to p53 and p21 nuclear accumulation. Oncol Rep 19: 1477-1483, 2008.
49. Tuynman JBLS, Lagarde SM, Ten Kate FJ, Richel DJ and van Lanschot JJ: Met expression is an independent prognostic risk factor in patients with oesophageal adenocarcinoma. Br J Cancer 98: 1102-1108, 2008.
50. Cecchi F, Rabe DC and Bottaro DP: Targeting the HGF/Met signaling pathway in cancer therapy. Expert Opin Ther Targets 16: 553-572, 2012.
51. Peters S and Adjei AA: MET: A promising anticancer therapeutic target. Nat Rev Clin Oncol 9: 314-326, 2012.
52. Reid JF, Sokolova V, Zoni E, Lampis A, Pizzamiglio S, Bertan C, Zanutto S, Perrone F, Camerini T, Gallino G, et al: miRNA profiling in colorectal cancer highlights miR1 involvement in MET-dependent proliferation. Mol Cancer Res 10: 504-515, 2012.
53. Yan D, Dong XE, Chen X, Wang L, Lu C, Wang J, Qu J and Tu L: MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development. J Biol Chem 284: 29596-29604, 2009.
54. Shirali S, Aghaei M, Shabani M, Fathi M, Sohrabi M and Moeinifard M: Adenosine induces cell cycle arrest and apoptosis via cyclinD1/Cdk4 and Bcl-2/Bax pathways in human ovarian cancer cell line OVCAR-3. Tumour Biol 34: 1085-1095, 2013.
55. Fong LY, Nguyen VT, Farber JL, Huebner K and Magee PN: Early deregulation of the the p16ink4a-cyclin D1/cyclin-dependent kinase 4-retinoblastoma pathway in cell proliferation-driven esophageal tumorigenesis in zinc-deficient rats. Cancer Res 60: 4589-4595, 2000.