N-myc downstream-regulated gene 1 downregulates cell proliferation, invasiveness, and tumorigenesis in human oral squamous cell carcinoma11Equal contributions.

Cancer Letters

Volumn 355, Issue 2, 2014, Pages 242-252

  Lee, Jehn Chuan ^a   Chung, Li Chuan ^b   Chen, Yu Jen ^a   Feng, Tsui Hsia ^b   Juang, Horng Heng ^a  

^a MACKAY MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

EMT; Invasion; MMP 2; MMP 9; NDRG1; OSCC

Indexed keywords

F ACTIN; GELATINASE; GELATINASE A; GELATINASE B; MEMBRANE PROTEIN; N MYC DOWNSTREAM REGULATED GENE 1; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL 1; TRITIUM; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; CELL CYCLE PROTEIN; N-MYC DOWNSTREAM-REGULATED GENE 1 PROTEIN; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTITUMOR GENE; ARTICLE; CARCINOGENESIS; CELL INVASION ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOSIS INHIBITION; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; OECM 1 CELL LINE; ORAL CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; S PHASE CELL CYCLE CHECKPOINT; TUMOR INVASION; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; ZYMOGRAPHY; ANIMAL; BAGG ALBINO MOUSE; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK TUMOR; METABOLISM; MOUTH TUMOR; PATHOLOGY; PHYSIOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CADHERINS; CARCINOGENESIS; CARCINOMA, SQUAMOUS CELL; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEAD AND NECK NEOPLASMS; HETEROGRAFTS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE, INBRED BALB C; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; UP-REGULATION;

EID: 84908207903     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.08.035     Document Type: Article

References (41)

1. Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 2009, 45:309-316.
2. Davis S.J., Divi V., Owen J.H., Bradford C.R., Carey T.E., Papagerakis S., et al. Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma. Arch. Otolaryngol. Head Neck Surg 2010, 136:1260-1266.
3. Bae D.H., Jansson P.J., Huang M.L., Kovacevic Z., Kalinowski D., Lee C.S., et al. The role of NDRG1 in the pathology and potential treatment of human cancers. J. Clin. Pathol 2013, 66:911-917.
4. Chen Z., Zhang D., Yue F., Zheng M., Kovacevic Z., Richardson D.R. The iron chelators Dp44mT and DFO inhibit TGF-beta-induced epithelial-mesenchymal transition via up-regulation of N-Myc downstream-regulated gene 1 (NDRG1). J. Biol. Chem 2012, 287:17016-17028.
5. Chung L.C., Tsui K.H., Feng T.H., Lee S.L., Chang P.L., Juang H.H. L-Mimosine blocks cell proliferation via upregulation of B-cell translocation gene 2 and N-myc downstream regulated gene 1 in prostate carcinoma cells. Am. J. Physiol. Cell Physiol 2012, 302:C676-C685.
6. Sun J., Zhang D., Bae D.H., Sahni S., Jansson P., Zheng Y., et al. Metastasis suppressor, NDRG1, mediates its activity through signaling pathways and molecular motors. Carcinogenesis 2013, 34:1943-1954.
7. Maruyama Y., Ono M., Kawahara A., Yokoyama T., Basaki Y., Kage M., et al. Tumor growth suppression in pancreatic cancer by a putative metastasis suppressor gene Cap43/NDRG1/Drg-1 through modulation of angiogenesis. Cancer Res 2006, 66:6233-6242.
8. Sun J., Zhang D., Zheng Y., Zhao Q., Zheng M., Kovacevic Z., et al. Targeting the metastasis suppressor, NDRG1, using novel iron chelators: regulation of stress fiber-mediated tumor cell migration via modulation of the ROCK1/pMLC2 signaling pathway. Mol. Pharmacol 2013, 83:454-469.
9. Guan R.J., Ford H.L., Fu Y., Li Y., Shaw L.M., Pardee A.B. Drg-1 as a differentiation-related, putative metastatic suppressor gene in human colon cancer. Cancer Res 2000, 60:749-755.
10. Ando T., Ishiguro H., Kimura M., Mitsui A., Kurehara H., Sugito N., et al. Decreased expression of NDRG1 is correlated with tumor progression and poor prognosis in patients with esophageal squamous cell carcinoma. Dis. Esophagus 2006, 19:454-458.
11. Bandyopadhyay S., Pai S.K., Gross S.C., Hirota S., Hosobe S., Miura K., et al. The Drg-1 gene suppresses tumor metastasis in prostate cancer. Cancer Res 2003, 63:1731-1736.
12. Dos Santos M., da Cunha Mercante A.M., Nunes F.D., Leopoldino A.M., de Carvalho M.B., Gazito D., et al. Prognostic significance of NDRG1 expression in oral and oropharyngeal squamous cell carcinoma. Mol. Biol. Rep 2012, 39:10157-10165.
13. Chang J.T., Wang H.M., Chang K.W., Chen W.H., Wen M.C., Hsu Y.M., et al. Identification of differentially expressed genes in oral squamous cell carcinoma (OSCC): overexpression of NPM, CDK1 and NDRG1 and underexpression of CHES1. Int. J. Cancer 2005, 114:942-949.
14. Hollier B.G., Evans K., Mani S.A. The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J. Mammary Gland Biol. Neoplasia 2009, 14:29-43.
15. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
16. Scanlon C.S., Van Tubergen E.A., Inglehart R.C., D'Silva N.J. Biomarkers of epithelial-mesenchymal transition in squamous cell carcinoma. J. Dent. Res 2013, 92:114-121.
17. Zhao Z., Ge J., Sun Y., Tian L., Lu J., Liu M., et al. Is E-cadherin immunoexpression a prognostic factor for head and neck squamous cell carcinoma (HNSCC)? A systematic review and meta-analysis. Oral Oncol 2012, 48:761-767.
18. Fan C.C., Wang T.Y., Cheng Y.A., Jiang S.S., Cheng C.W., Lee A.Y., et al. Expression of E-cadherin, Twist, and p53 and their prognostic value in patients with oral squamous cell carcinoma. J. Cancer Res. Clin. Oncol 2013, 139:1735-1744.
19. Lee S.S., Tsai C.H., Yu C.C., Chang Y.C. Elevated snail expression mediates tumor progression in areca quid chewing-associated oral squamous cell carcinoma via reactive oxygen species. PLoS ONE 2013, 8:e67985.
20. Zhu L.F., Hu Y., Yang C.C., Xu X.H., Ning T.Y., Wang Z.L., et al. Snail overexpression induces an epithelial to mesenchymal transition and cancer stem cell-like properties in SCC9 cells. Lab. Invest 2012, 92:744-752.
21. Tsui K.H., Chang Y.L., Feng T.H., Chung L.C., Lee T.Y., Chang P.L., et al. Growth differentiation factor-15 upregulates interleukin-6 to promote tumorigenesis of prostate carcinoma PC-3 cells. J. Mol. Endocrinol 2012, 49:153-163.
22. Juang H.H., Chung L.C., Sung H.C., Feng T.H., Lee Y.H., Chang P.L., et al. Metallothionein 3: an androgen-upregulated gene enhances cell invasion and tumorigenesis of prostate carcinoma cells. Prostate 2013, 73:1495-1506.
23. Floryk D., Thompson T.C. Antiproliferative effects of AVN944, a novel inosine 5-monophosphate dehydrogenase inhibitor, in prostate cancer cells. Int. J. Cancer 2008, 123:2294-2302.
24. Hosoya N., Sakumoto M., Nakamura Y., Narisawa T., Bilim V., Motoyama T., et al. Proteomics identified nuclear N-myc downstream-regulated gene 1 as a prognostic tissue biomarker candidate in renal cell carcinoma. Biochim. Biophys. Acta 1834, 2013:2630-2639.
25. Lane D.J., Saletta F., Suryo Rahmanto Y., Kovacevic Z., Richardson D.R. N-myc downstream regulated 1 (NDRG1) is regulated by eukaryotic initiation factor 3a (eIF3a) during cellular stress caused by iron depletion. PLoS ONE 2013, 8:e57273.
26. Liu Y.L., Bai W.T., Luo W., Zhang D.X., Yan Y., Xu Z.K., et al. Downregulation of NDRG1 promotes invasion of human gastric cancer AGS cells through MMP-2. Tumour Biol 2011, 32:99-105.
27. Angst E., Dawson D.W., Stroka D., Gloor B., Park J., Candinas D., et al. N-myc downstream regulated gene-1 expression correlates with reduced pancreatic cancer growth and increased apoptosis in vitro and in vivo. Surgery 2011, 149:614-624.
28. Koontongkaew S. The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinomas. J. Cancer 2013, 4:66-83.
29. Imanishi Y., Fujii M., Tokumaru Y., Tomita T., Kanke M., Kanzaki J., et al. Clinical significance of expression of membrane type 1 matrix metalloproteinase and matrix metalloproteinase-2 in human head and neck squamous cell carcinoma. Hum. Pathol 2000, 31:895-904.
30. Kato K., Hara A., Kuno T., Kitaori N., Huilan Z., Mori H., et al. Matrix metalloproteinases 2 and 9 in oral squamous cell carcinomas: manifestation and localization of their activity. J. Cancer Res. Clin. Oncol 2005, 131:340-346.
31. Lachat P., Shaw P., Gebhard S., van Belzen N., Chaubert P., Bosman F.T. Expression of NDRG1, a differentiation-related gene, in human tissues. Histochem. Cell Biol 2002, 118:399-408.
32. Sugiki T., Taketomi Y., Kikuchi-Yanoshita R., Murakami M., Kudo I. Association of N-myc downregulated gene 1 with heat-shock cognate protein 70 in mast cells. Biol. Pharm. Bull 2004, 27:628-633.
33. Akiba J., Murakami Y., Noda M., Watari K., Ogasawara S., Yoshida T., et al. N-myc downstream regulated gene1/Cap43 overexpression suppresses tumor growth by hepatic cancer cells through cell cycle arrest at the G0/G1 phase. Cancer Lett 2011, 310:25-34.
34. O'Neill G.M. The coordination between actin filaments and adhesion in mesenchymal migration. Cell Adhes. Migr 2009, 3:355-357.
35. Yokoyama K., Kamata N., Hayashi E., Hoteiya T., Ueda N., Fujimoto R., et al. Reverse correlation of E-cadherin and snail expression in oral squamous cell carcinoma cells in vitro. Oral Oncol 2001, 37:65-71.
36. Nguyen P.T., Kudo Y., Yoshida M., Kamata N., Ogawa I., Takata T. N-cadherin expression is involved in malignant behavior of head and neck cancer in relation to epithelial-mesenchymal transition. Histol. Histopathol 2011, 26:147-156.
37. Takkunen M., Grenman R., Hukkanen M., Korhonen M., Garcia de Herreros A., Virtanen I. Snail-dependent and -independent epithelial-mesenchymal transition in oral squamous carcinoma cells. J. Histochem. Cytochem 2006, 54:1263-1275.
38. Zhao D., Tang X.F., Yang K., Liu J.Y., Ma X.R. Over-expression of integrin-linked kinase correlates with aberrant expression of Snail, E-cadherin and N-cadherin in oral squamous cell carcinoma: implications in tumor progression and metastasis. Clin. Exp. Metastasis 2012, 29:957-969.
39. Zidar N., Bostjancic E., Gale N., Kojc N., Poljak M., Glavac D., et al. Down-regulation of microRNAs of the miR-200 family and miR-205, and an altered expression of classic and desmosomal cadherins in spindle cell carcinoma of the head and neck - hallmark of epithelial-mesenchymal transition. Hum. Pathol 2011, 42:482-488.
40. Kachhap S.K., Faith D., Qian D.Z., Shabbeer S., Galloway N.L., Pili R., et al. The N-myc down regulated gene 1 (NDRG1) is a Rab4a effector involved in vesicular recycling of E-cadherin. PLoS ONE 2007, 9:e844.
41. Song Y., Oda Y., Hori M., Kuroiwa K., Ono M., Hosoi F., et al. N-myc downstream regulated gene-1/Cap43 may play an important role in malignant progression of prostate cancer, in its close association with E-cadherin. Hum. Pathol 2010, 41:214-222.