MicroRNA-26b inhibits tumor metastasis by targeting the KPNA2/c-jun pathway in human gastric cancer

Oncotarget

Volumn 7, Issue 26, 2016, Pages 39511-39526

  Tsai, Ming Ming ^a,c   Huang, Hsiang Wei ^b   Wang, Chia Siu ^c   Lee, Kam Fai ^c   Tsai, Chung Ying ^b   Lu, Pei Hsuan ^d   Chi, Hsiang Cheng ^b   Lin, Yang Hsiang ^b   Kuo, Liang Mou ^c   Lin, Kwang Huei ^b,c  

^a CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

C jun; Gastric cancer; KPNA2; MiR 26b; Prognosis

Indexed keywords

KPNA2 PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 26B; ONCOPROTEIN; PROTEIN C JUN; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; KARYOPHERIN ALPHA; KPNA2 PROTEIN, HUMAN; MIRN26A MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER STAGING; CANCER SURVIVAL; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; LUNG METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; STOMACH CANCER; SURVIVAL RATE; AGED; CELL MOTION; DISEASE EXACERBATION; GENE EXPRESSION REGULATION; HELICOBACTER PYLORI; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PROGNOSIS; PROMOTER REGION; STOMACH TUMOR; TREATMENT OUTCOME; TUMOR CELL LINE; VERY ELDERLY;

3' UNTRANSLATED REGIONS; ADULT; AGED; AGED, 80 AND OVER; ALPHA KARYOPHERINS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HELICOBACTER PYLORI; HUMANS; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM METASTASIS; PROGNOSIS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; STOMACH NEOPLASMS; TREATMENT OUTCOME;

EID: 84982975974     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8629     Document Type: Article

References (53)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin. 2008; 58:71-96.
2. Department of Health T. (Department of Health, Taiwan. Cause of death statistics. 2010 [assessed April 7th 2010]. 2010.
3. Tsujimoto H, Ono S, Ichikura T, Matsumoto Y, Yamamoto J, Hase K. Roles of inflammatory cytokines in the progression of gastric cancer: friends or foes? Gastric Cancer. 2010; 13:212-221.
4. Ventura A, Jacks T. MicroRNAs and cancer: short RNAs go a long way. Cell. 2009; 136586-591.
5. Kent OA, Mendell JT. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene. 2006; 25:6188-6196.
6. Tsai MM, Wang CS, Tsai CY, Chen CY, Chi HC, Tseng YH, Chung PJ, Lin YH, Chung IH, Lin KH. MicroRNA-196a/-196b promote cell metastasis via negative regulation of radixin in human gastric cancer. Cancer Lett. 2014; 351:222-231.
7. Zhang C, Tong J, Huang G. Nicotinamide phosphoribosyl transferase (Nampt) is a target of microRNA-26b in colorectal cancer cells. PloS one. 2013; 8:e69963.
8. Tan S, Ding K, Li R, Zhang W, Li G, Kong X, Qian P, Lobie PE, Zhu T. Identification of miR-26 as a key mediator of estrogen stimulated cell proliferation by targeting CHD1, GREB1 and KPNA2. Breast Cancer Res. 2014; 16:R40.
9. Zhang Z, Wang J, Lu X. An integrated study of natural hydroxyapatite-induced osteogenic differentiation of mesenchymal stem cells using transcriptomics, proteomics and microRNA analyses. Biomed Mater. 2014; 9:045005.
10. Wang CI, Wang CL, Wang CW, Chen CD, Wu CC, Liang Y, Tsai YH, Chang YS, Yu JS, Yu CJ. Importin subunit alpha-2 is identified as a potential biomarker for non-small cell lung cancer by integration of the cancer cell secretome and tissue transcriptome. Int J Cancer. 2011; 128:2364-2372.
11. Noetzel E, Rose M, Bornemann J, Gajewski M, Knuchel R, Dahl E. Nuclear transport receptor karyopherin-alpha2 promotes malignant breast cancer phenotypes in vitro. Oncogene. 2012; 31:2101-2114.
12. Jensen JB, Munksgaard PP, Sorensen CM, Fristrup N, Birkenkamp-Demtroder K, Ulhoi BP, Jensen KM, Orntoft TF, Dyrskjot L. High expression of karyopherin-alpha2 defines poor prognosis in non-muscle-invasive bladder cancer and in patients with invasive bladder cancer undergoing radical cystectomy. Eur Urol. 2011; 59:841-848.
13. Barreto-Zuniga R, Maruyama M, Kato Y, Aizu K, Ohta H, Takekoshi T, Bernal SF. Significance of Helicobacter pylori infection as a risk factor in gastric cancer: serological and histological studies. J Gastroenterol. 1997; 32:289-294.
14. Kim KM, Kwon MS, Hong SJ, Min KO, Seo EJ, Lee KY, Choi SW, Rhyu MG. Genetic classification of intestinal-type and diffuse-type gastric cancers based on chromosomal loss and microsatellite instability. Virchows Arch. 2003; 443:491-500.
15. Yasui W, Oue N, Kuniyasu H, Ito R, Tahara E, Yokozaki H. Molecular diagnosis of gastric cancer: present and future. Gastric Cancer. 2001; 4:113-121.
16. Liu NN, Wang Y, Wu Q. [Jianpi jiedu recipe inhibited Helicobacter pylori-induced the expression of cyclooxygenase-2 via p38MAPK/ATF-2 signal transduction pathway in human gastric cancer cells]. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2011; 31:926-931.
17. Wang CI, Chien KY, Wang CL, Liu HP, Cheng CC, Chang YS, Yu JS, Yu CJ. Quantitative proteomics reveals regulation of karyopherin subunit alpha-2 (KPNA2) and its potential novel cargo proteins in nonsmall cell lung cancer. Mol Cell Proteomics. 2012; 11:1105-1122.
18. Huang L, Wang HY, Li JD, Wang JH, Zhou Y, Luo RZ, Yun JP, Zhang Y, Jia WH, Zheng M. KPNA2 promotes cell proliferation and tumorigenicity in epithelial ovarian carcinoma through upregulation of c-Myc and downregulation of FOXO3a. Cell Death Dis. 2013; 4:e745.
19. Li FQ, Xu B, Wu YJ, Yang ZL, Qian JJ. Differential microRNA expression in signet-ring cell carcinoma compared with tubular adenocarcinoma of human gastric cancer. Genetics and molecular research. 2015; 14:739-747.
20. Sandhu R, Rivenbark AG, Mackler RM, Livasy CA, Coleman WB. Dysregulation of microRNA expression drives aberrant DNA hypermethylation in basal-like breast cancer. Int J Oncol. 2014; 44:563-572.
21. Shah MS, Davidson LA, Chapkin RS. Mechanistic insights into the role of microRNAs in cancer: influence of nutrient crosstalk. Frontiers in genetics. 2012; 3:305.
22. Solomides CC, Evans BJ, Navenot JM, Vadigepalli R, Peiper SC, Wang ZX. MicroRNA profiling in lung cancer reveals new molecular markers for diagnosis. Acta cytologica. 2012; 56:645-654.
23. Zhao L, Sun Y, Hou Y, Peng Q, Wang L, Luo H, Tang X, Zeng Z, Liu M. MiRNA expression analysis of cancer-associated fibroblasts and normal fibroblasts in breast cancer. Int J Biochem Cell Biol. 2012; 44:2051-2059.
24. Bakre A, Mitchell P, Coleman JK, Jones LP, Saavedra G, Teng M, Tompkins SM, Tripp RA. Respiratory syncytial virus modifies microRNAs regulating host genes that affect virus replication. J Gen Virol. 2012; 93:2346-2356.
25. Hsu CM, Lin PM, Wang YM, Chen ZJ, Lin SF, Yang MY. Circulating miRNA is a novel marker for head and neck squamous cell carcinoma. Tumour biology: The J Int Soc Oncodev Biol Med. 2012; 33:1933-1942.
26. Zhu A, Kang N, He L, Li X, Xu X, Zhang H. MiR-221 and miR-26b regulate chemotactic migration of MSCs toward HGF through activation of Akt and FAK. J Cell Biochem. 2015.
27. Duan G, Ren C, Zhang Y, Feng S. MicroRNA-26b inhibits metastasis of osteosarcoma via targeting CTGF and Smad1. Tumour biology: The J Int Soc Oncodev Biol Med. 2015.
28. Du JY, Wang LF, Wang Q, Yu LD. miR-26b inhibits proliferation, migration, invasion and apoptosis induction via the downregulation of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 driven glycolysis in osteosarcoma cells. Oncology reports. 2015; 33:1890-1898.
29. Cao J, Guo T, Dong Q, Zhang J, Li Y. miR-26b is downregulated in human tongue squamous cell carcinoma and regulates cell proliferation and metastasis through a COX-2-dependent mechanism. Oncology reports. 2015; 33:974-980.
30. Liu J, Du X, Zhou J, Pan Z, Liu H, Li Q. MicroRNA-26b functions as a proapoptotic factor in porcine follicular Granulosa cells by targeting Sma-and Mad-related protein 4. Biology of reproduction. 2014; 91:146.
31. Li J, Li X, Kong X, Luo Q, Zhang J, Fang L. MiRNA-26b inhibits cellular proliferation by targeting CDK8 in breast cancer. Int J Clin Exp Med. 2014; 7:558-565.
32. Zhao N, Wang R, Zhou L, Zhu Y, Gong J, Zhuang SM. MicroRNA-26b suppresses the NF-kappaB signaling and enhances the chemosensitivity of hepatocellular carcinoma cells by targeting TAK1 and TAB3. Molecular cancer. 2014; 13:35.
33. Li J, Kong X, Zhang J, Luo Q, Li X, Fang L. MiRNA-26b inhibits proliferation by targeting PTGS2 in breast cancer. Cancer cell Int. 2013; 13:7.
34. Zhu Y, Lu Y, Zhang Q, Liu JJ, Li TJ, Yang JR, Zeng C, Zhuang SM. MicroRNA-26a/b and their host genes cooperate to inhibit the G1/S transition by activating the pRb protein. Nucleic acids Res. 2012; 40:4615-4625.
35. Li H, Sun Q, Han B, Yu X, Hu B, Hu S. MiR-26b inhibits hepatocellular carcinoma cell proliferation, migration, and invasion by targeting EphA2. Int J Clin Exp Pathol. 2015; 8:4782-4790.
36. Liang N, Zhou X, Zhao M, Zhao D, Zhu Z, Li S, Yang H. Down-regulation of microRNA-26b modulates non-small cell lung cancer cells chemoresistance and migration through the association of PTEN. Acta biochimica et biophysica Sinica. 2015; 47:530-538.
37. Kato M, Goto Y, Matsushita R, Kurozumi A, Fukumoto I, Nishikawa R, Sakamoto S, Enokida H, Nakagawa M, Ichikawa T, Seki N. MicroRNA-26a/b directly regulate La-related protein 1 and inhibit cancer cell invasion in prostate cancer. Int J Oncol. 2015; 47:710-718.
38. Verghese ET, Drury R, Green CA, Holliday DL, Lu X, Nash C, Speirs V, Thorne JL, Thygesen HH, Zougman A, Hull MA, Hanby AM, Hughes TA. MiR-26b is down-regulated in carcinoma-associated fibroblasts from ER-positive breast cancers leading to enhanced cell migration and invasion. J Pathol. 2013; 231:388-399.
39. Wu N, Zhao X, Liu M, Liu H, Yao W, Zhang Y, Cao S, Lin X. Role of microRNA-26b in glioma development and its mediated regulation on EphA2. PloS one. 2011; 6:e16264.
40. Coburn NG. Lymph nodes and gastric cancer. J Surg Oncol. 2009; 99:199-206.
41. Tie J, Pan Y, Zhao L, Wu K, Liu J, Sun S, Guo X, Wang B, Gang Y, Zhang Y, Li Q, Qiao T, Zhao Q, et al. MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the Robo1 receptor. PLoS genetics. 2010; 6:e1000879.
42. Sun T, Wang C, Xing J, Wu D. miR-429 modulates the expression of c-myc in human gastric carcinoma cells. Eur J Cancer. 2011; 47:2552-2559.
43. Lo SS, Hung PS, Chen JH, Tu HF, Fang WL, Chen CY, Chen WT, Gong NR, Wu CW. Overexpression of miR-370 and downregulation of its novel target TGFbeta-RII contribute to the progression of gastric carcinoma. Oncogene. 2012; 31:226-237.
44. Kogo R, Mimori K, Tanaka F, Komune S, Mori M. Clinical significance of miR-146a in gastric cancer cases. Clin Cancer Res. 2011; 17:4277-4284.
45. Christiansen A, Dyrskjot L. The functional role of the novel biomarker karyopherin alpha 2 (KPNA2) in cancer. Cancer Lett. 2013; 331:18-23.
46. Li XL, Jia LL, Shi MM, Li X, Li ZH, Li HF, Wang EH, Jia XS. Downregulation of KPNA2 in non-small-cell lung cancer is associated with Oct4 expression. J Transl Med. 2013; 11:232.
47. Kim SY, Kang HT, Han JA, Park SC. The transcription factor Sp1 is responsible for aging-dependent altered nucleocytoplasmic trafficking. Aging cell. 2012; 11:1102-1109.
48. Wight TN, Kinsella MG, Qwarnstrom EE. The role of proteoglycans in cell adhesion, migration and proliferation. Curr Opin Cell Biol. 1992; 4:793-801.
49. Japanese Gastric Cancer A. Japanese Classification of Gastric Carcinoma - 2nd English Edition. Gastric Cancer. 1998; 1:10-24.
50. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005; 33:e179.
51. Shih CH, Chen SL, Yen CC, Huang YH, Chen CD, Lee YS, Lin KH. Thyroid hormone receptor-dependent transcriptional regulation of fibrinogen and coagulation proteins. Endocrinology. 2004; 145:2804-2814.
52. Tsai MM, Lin PY, Cheng WL, Tsai CY, Chi HC, Chen CY, Tseng YH, Cheng YF, Chen CD, Liang Y, Liao CJ, Wu SM, Lin YH, et al. Overexpression of ADP-ribosylation factor 1 in human gastric carcinoma and its clinicopathological significance. Cancer Sci. 2012; 103:1136-1144.
53. Repesh LA. A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis. 1989; 9:192-208.