Tumor suppressor ING4 overexpression contributes to proliferation and invasion inhibition in gastric carcinoma by suppressing the NF-jB signaling pathway

Molecular Biology Reports

Volumn 40, Issue 10, 2013, Pages 5723-5732

  Li, Shijie ^a   Fan, Tianli ^b   Liu, Hongtao ^b   Chen, Jiangtao ^a   Qin, Changjiang ^a   Ren, Xuequn ^a  

^a HENAN UNIVERSITY   (China)

^b ZHENGZHOU UNIVERSITY   (China)

Author keywords

Cell invasion; Cell proliferation; Gastric carcinoma; Inhibitor of growth 4; NF jB signaling pathway

Indexed keywords

GELATINASE B; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF GROWTH 4 PROTEIN; MESSENGER RNA; SYNAPTOTAGMIN I; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UROKINASE;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; TUMOR INVASION; UPREGULATION;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; NEOPLASM INVASIVENESS; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84892712186     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-013-2675-3     Document Type: Article

References (45)

1. Liang S, He L, Zhao X, Miao Y, Gu Y, Guo C, Xue Z, Dou W, Hu F, Wu K et al (2011) MicroRNA let-7f inhibits tumor invasion and metastasis by targeting MYH9 in human gastric cancer. PLoS ONE 6(4):e18409
2. Fuchs CS, Mayer RJ (1995) Gastric carcinoma. N Engl J Med 333(1):32-41
3. Washington K (2010) 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol 17(12):3077-3079
4. Roukos DH (2010) Targeting gastric cancer with trastuzumab: new clinical practice and innovative developments to overcome resistance. Ann Surg Oncol 17(1):14-17
5. Yasui W, Yokozaki H, Fujimoto J, Naka K, Kuniyasu H, Tahara E (2000) Genetic and epigenetic alterations in multistep carcinogenesis of the stomach. J Gastroenterol 35(Suppl 12):111-115
6. Wang Y, Li G (2006) ING3 promotes UV-induced apoptosis via Fas/caspase-8 pathway in melanoma cells. J Biol Chem 281(17):11887-11893
7. Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, Onogi H, Higashimoto Y, Appella E, Yokota J et al (2003) p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res 63(10):2373-2378
8. Zhang X, Xu LS, Wang ZQ, Wang KS, Li N, Cheng ZH, Huang SZ, Wei DZ, Han ZG (2004) ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett 570(1-3):7-12
9. Li X, Zhang Q, Cai L, Wang Y, Wang Q, Huang X, Fu S, Bai J, Liu J, Zhang G et al (2009) Inhibitor of growth 4 induces apoptosis in human lung adenocarcinoma cell line A549 via Bcl-2 family proteins and mitochondria apoptosis pathway. J Cancer Res Clin Oncol 135(6):829-835
10. Shen JC, Unoki M, Ythier D, Duperray A, Varticovski L, Kumamoto K, Pedeux R, Harris CC (2007) Inhibitor of growth 4 suppresses cell spreading and cell migration by interacting with a novel binding partner, liprin alpha1. Cancer Res 67(6):2552-2558
11. Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, Barnett GH, Jain RK (2004) The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428(6980):328-332
12. Li J, Li G (2010) Cell cycle regulator ING4 is a suppressor of melanoma angiogenesis that is regulated by the metastasis suppressor BRMS1. Cancer Res 70(24):10445-10453
13. Colla S, Tagliaferri S, Morandi F, Lunghi P, Donofrio G, Martorana D, Mancini C, Lazzaretti M, Mazzera L, Ravanetti L et al (2007) The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxiainducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood 110(13):4464-4475
14. Ozer A, Wu LC, Bruick RK (2005) The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proc Natl Acad Sci USA 102(21):7481-7486
15. Wei Q, He W, Lu Y, Yao J, Cao X (2012) Effect of the tumor suppressor gene ING4 on the proliferation of MCF-7 human breast cancer cells. Oncol Lett 4(3):438-442
16. Byron SA, Min E, Thal TS, Hostetter G, Watanabe AT, Azorsa DO, Little TH, Tapia C, Kim S (2012) Negative regulation of NFkappaB by the ING4 tumor suppressor in breast cancer. PLoS ONE 7(10):e46823
17. Lou C, Jiang S, Guo X, Dong XS (2012) ING4 is negatively correlated with microvessel density in colon cancer. Tumour Biol 33(6):2357-2364
18. Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, Yang J (2012) Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther 19(10): 697-706
19. Zeng ZL, Li FJ, Gao F, Sun DS, Yao L (2013) Upregulation of miR-650 is correlated with down-regulation of ING4 and progression of hepatocellular carcinoma. J Surg Oncol 107(2): 105-110
20. Liu Y, Yu L, Wang Y, Zhang Y, Zhang G (2012) Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol 138(4):647-655
21. Zhao Y, Su C, Zhai H, Tian Y, Sheng W, Miao J, Yang J (2012) Synergistic antitumor effect of adenovirus-mediated hING4 gene therapy and (125)I radiation therapy on pancreatic cancer. Cancer Lett 316(2):211-218
22. Li XH, Kikuchi K, Zheng Y, Noguchi A, Takahashi H, Nishida T, Masuda S, Yang XH, Takano Y (2011) Downregulation and translocation of nuclear ING4 is correlated with tumorigenesis and progression of head and neck squamous cell carcinoma. Oral Oncol 47(3):217-223
23. Li M, Jin Y, Sun WJ, Yu Y, Bai J, Tong DD, Qi JP, Du JR, Geng JS, Huang Q et al (2009) Reduced expression and novel splice variants of ING4 in human gastric adenocarcinoma. J Pathol 219(1):87-95
24. Zhao H, Yang J, Fan T, Li S, Ren X (2012) RhoE functions as a tumor suppressor in esophageal squamous cell carcinoma and modulates the PTEN/PI3K/Akt signaling pathway. Tumour Biol 33(5):1363-1374
25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408
26. Lu Z, Liu H, Xue L, Xu P, Gong T, Hou G (2008) An activated Notch1 signaling pathway inhibits cell proliferation and induces apoptosis in human esophageal squamous cell carcinoma cell line EC9706. Int J Oncol 32(3):643-651
27. Bava SV, Sreekanth CN, Thulasidasan AK, Anto NP, Cheriyan VT, Puliyappadamba VT, Menon SG, Ravichandran SD, Anto RJ (2011) Akt is upstream and MAPKs are downstream of NFkappaB in paclitaxel-induced survival signaling events, which are down-regulated by curcumin contributing to their synergism. Int J Biochem Cell Biol 43(3):331-341
28. Aggarwal BB, Sung B (2011) NF-kappaB in cancer: a matter of life and death. Cancer Discov 1(6):469-471
29. Wang W, Abbruzzese JL, Evans DB, Chiao PJ (1999) Overexpression of urokinase-type plasminogen activator in pancreatic adenocarcinoma is regulated by constitutively activated RelA. Oncogene 18(32):4554-4563
30. Yang J, Wei D, Liu J (2005) Repressions of MMP-9 expression and NF-kappa B localization are involved in inhibition of lung carcinoma 95-D cell invasion by (-)-epigallocatechin-3-gallate. Biomed Pharmacother 59(3):98-103
31. Fang F, Luo LB, Tao YM, Wu F, Yang LY (2009) Decreased expression of inhibitor of growth 4 correlated with poor prognosis of hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev 18(2):409-416
32. Gunduz M, Nagatsuka H, Demircan K, Gunduz E, Cengiz B, Ouchida M, Tsujigiwa H, Yamachika E, Fukushima K, Beder L et al (2005) Frequent deletion and down-regulation of ING4, a candidate tumor suppressor gene at 12p13, in head and neck squamous cell carcinomas. Gene 356:109-117
33. Li X, Cai L, Liang M, Wang Y, Yang J, Zhao Y (2008) ING4 induces cell growth inhibition in human lung adenocarcinoma A549 cells by means of Wnt-1/beta-catenin signaling pathway. Anat Rec (Hoboken) 291(5):593-600
34. Li J, Martinka M, Li G (2008) Role of ING4 in human melanoma cell migration, invasion and patient survival. Carcinogenesis 29(7):1373-1379
35. You Q, Wang XS, Fu SB, Jin XM (2011) Downregulated expression of inhibitor of growth 4 (ING4) in advanced colorectal cancers: a non-randomized experimental study. Pathol Oncol Res 17(3):473-477
36. Wang QS, Li M, Zhang LY, Jin Y, Tong DD, Yu Y, Bai J, Huang Q, Liu FL, Liu A et al (2010) Down-regulation of ING4 is associated with initiation and progression of lung cancer. Histopathology 57(2):271-281
37. Zhan LP, Li QY, Zhang Y, Zhang TJ, Yuan ZC, Lu PS (2011) Mechanism of ING4 mediated inhibition of the proliferation and migration of human glioma cell line U251. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 27(11):1188-1190
38. Li X, Cai L, Chen H, Zhang Q, Zhang S, Wang Y, Dong Y, Cheng H, Qi J (2009) Inhibitor of growth 4 induces growth suppression and apoptosis in glioma U87MG. Pathobiology 76(4):181-192
39. Cai L, Li X, Zheng S, Wang Y, Li H, Yang J, Sun J (2009) Inhibitor of growth 4 is involved in melanomagenesis and induces growth suppression and apoptosis in melanoma cell line M14. Melanoma Res 19(1):1-7
40. Helbig G, Christopherson KW 2nd, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, Broxmeyer HE, Nakshatri H (2003) NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem 278(24):21631-21638
41. McNulty SE, Tohidian NB, Meyskens FL Jr. (2001) RelA, p50 and inhibitor of kappa B alpha are elevated in human metastatic melanoma cells and respond aberrantly to ultraviolet light B. Pigment Cell Res 14(6):456-465
42. Shishodia S, Aggarwal BB (2004) Nuclear factor-kappaB activation mediates cellular transformation, proliferation, invasion angiogenesis and metastasis of cancer. Cancer Treat Res 119: 139-173
43. Park BK, Zhang H, Zeng Q, Dai J, Keller ET, Giordano T, Gu K, Shah V, Pei L, Zarbo RJ et al (2007) NF-kappaB in breast cancer cells promotes osteolytic bone metastasis by inducing osteoclastogenesis via GM-CSF. Nat Med 13(1):62-69
44. Dong Z, Nemeth JA, Cher ML, Palmer KC, Bright RC, Fridman R (2001) Differential regulation of matrix metalloproteinase-9, tissue inhibitor of metalloproteinase-1 (TIMP-1) and TIMP-2 expression in co-cultures of prostate cancer and stromal cells. Int J Cancer 93(4):507-515
45. Pacheco MM, Nishimoto IN, Mourao Neto M, Mantovani EB, Brentani MM (2001) Prognostic significance of the combined expression of matrix metalloproteinase-9, urokinase type plasminogen activator and its receptor in breast cancer as measured by Northern blot analysis. Int J Biol Markers 16(1):62-68