Loss of NDRG2 promotes epithelial-mesenchymal transition of gallbladder carcinoma cells through MMP-19-mediated Slug expression

Journal of Hepatology

Volumn 63, Issue 6, 2015, Pages 1429-1439

  Lee, Dong Gwang ^a,b   Lee, Sang Hyun ^a   Kim, Jang Seong ^a   Park, Jongjin ^a,b   Cho, Young Lai ^c   Kim, Koon Soon ^d   Jo, Deog Yeon ^d   Song, Ik Chan ^d   Kim, Nayoung ^d   Yun, Hwan Jung ^d   Park, Young Jun ^a   Lee, Seon Jin ^a   Lee, Hee Gu ^a   Bae, Kwang Hee ^a   Lee, Sang Chul ^a   Shim, Sungbo ^e   Kim, Young Myeong ^f   Kwon, Young Guen ^g   Kim, Jin Man ^d   Lee, Hyo Jin ^d   Min, Jeong Ki ^a,b   more..

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c Dongguk University   (South Korea)

^d Chungnam National University   (South Korea)

^e Chungbuk National University   (South Korea)

^f Kangwon National University   (South Korea)

^g Yonsei University   (South Korea)

Author keywords

Epithelialmesenchymal transition; Gallbladder carcinoma; MMP 19; NDRG2; Slug

Indexed keywords

MATRIX METALLOPROTEINASE 19; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR SLUG; AXL RECEPTOR TYROSINE KINASE; MATRIX METALLOPROTEINASE; NDRG2 PROTEIN, HUMAN; ONCOPROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ADULT; ADVANCED CANCER; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CANCER PATIENT; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CANCER TISSUE; CARCINOMA CELL LINE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE COURSE; EPITHELIAL MESENCHYMAL TRANSITION; EXPERIMENTAL LIVER METASTASIS; FEMALE; GALLBLADDER CANCER CELL LINE; GALLBLADDER CARCINOMA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOSS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOUSE; N MYC DOWNSTREAM REGULATED GENE 2; NONHUMAN; OVERALL SURVIVAL; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL PREDICTION; TUMOR GROWTH; TUMOR INVASION; TUMOR SUPPRESSOR GENE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; CANCER TRANSPLANTATION; DEFICIENCY; GALLBLADDER TUMOR; GENETICS; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; UPREGULATION; XENOGRAFT;

AGED; ANIMALS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GALLBLADDER NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; MALE; MATRIX METALLOPROTEINASES, SECRETED; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84951140046     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.08.007     Document Type: Article

References (39)

1. I.I. Wistuba, and A.F. Gazdar Gallbladder cancer: lessons from a rare tumour Nat Rev Cancer 4 2004 695 706
2. C.M. Kang, K.S. Kim, J.S. Choi, W.J. Lee, and B.R. Kim Gallbladder carcinoma associated with anomalous pancreaticobiliary duct junction Can J Gastroenterol 21 2007 383 387
3. D. Chhabra, K. Oda, P. Jagannath, H. Utsunomiya, S. Takekoshi, and Y. Nimura Chronic heavy metal exposure and gallbladder cancer risk in India, a comparative study with Japan Asian Pac J Cancer Prev 13 2012 187 190
4. M. Rakic, L. Patrlj, M. Kopljar, R. Klicek, M. Kolovrat, B. Loncar, and et al. Gallbladder cancer Hepatobiliary Surg Nutr 3 2014 221 226
5. V. Melotte, X. Qu, M. Ongenaert, W. van Criekinge, A.P. de Bruine, H.S. Baldwin, and et al. The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications FASEB J 24 2010 4153 4166
6. X. Qu, Y. Zhai, H. Wei, C. Zhang, G. Xing, Y. Yu, and et al. Characterization and expression of three novel differentiation-related genes belong to the human NDRG gene family Mol Cell Biochem 229 2002 35 44
7. L. Shen, X. Qu, Y. Ma, J. Zheng, D. Chu, B. Liu, and et al. Tumor suppressor NDRG2 tips the balance of oncogenic TGF-beta via EMT inhibition in colorectal cancer Oncogenesis 3 2014 e86
8. Y. Deng, L. Yao, L. Chau, S.S. Ng, Y. Peng, X. Liu, and et al. N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation Int J Cancer 106 2003 342 347
9. J. Ma, W. Liu, X. Yan, Q. Wang, Q. Zhao, Y. Xue, and et al. Inhibition of endothelial cell proliferation and tumor angiogenesis by up-regulating NDRG2 expression in breast cancer cells PLoS One 7 2012 e32368
10. D.C. Lee, Y.K. Kang, W.H. Kim, Y.J. Jang, D.J. Kim, I.Y. Park, and et al. Functional and clinical evidence for NDRG2 as a candidate suppressor of liver cancer metastasis Cancer Res 68 2008 4210 4220
11. K. Polyak, and R.A. Weinberg Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits Nat Rev Cancer 9 2009 265 273
12. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat Rev Cancer 2 2002 442 454
13. M. Egeblad, and Z. Werb New functions for the matrix metalloproteinases in cancer progression Nat Rev Cancer 2 2002 161 174
14. L. Sun, M.E. Diamond, A.J. Ottaviano, M.J. Joseph, V. Ananthanarayan, and H.G. Munshi Transforming growth factor-beta 1 promotes matrix metalloproteinase-9-mediated oral cancer invasion through snail expression Mol Cancer Res 6 2008 10 20
15. A. Miyoshi, Y. Kitajima, K. Sumi, K. Sato, A. Hagiwara, Y. Koga, and et al. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells Br J Cancer 90 2004 1265 1273
16. D.C. Radisky, D.D. Levy, L.E. Littlepage, H. Liu, C.M. Nelson, J.E. Fata, and et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability Nature 436 2005 123 127
17. S.A. Illman, K. Lehti, J. Keski-Oja, and J. Lohi Epilysin (MMP-28) induces TGF-beta mediated epithelial to mesenchymal transition in lung carcinoma cells J Cell Sci 119 2006 3856 3865
18. S.J. Kim, Y. Lee, N.Y. Kim, Y. Hwang, B. Hwang, J.K. Min, and et al. Pancreatic adenocarcinoma upregulated factor, a novel endothelial activator, promotes angiogenesis and vascular permeability Oncogene 32 2013 3638 3647
19. Z.L. Liang, K. Kang, S. Yoon, S.M. Huang, J.S. Lim, J.M. Kim, and et al. NDRG2 is involved in the oncogenic properties of renal cell carcinoma and its loss is a novel independent poor prognostic factor after nephrectomy Ann Surg Oncol 19 2012 2763 2772
20. M. Jorda, D. Olmeda, A. Vinyals, E. Valero, E. Cubillo, A. Llorens, and et al. Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor J Cell Sci 118 2005 3371 3385
21. M.J. Joseph, S. Dangi-Garimella, M.A. Shields, M.E. Diamond, L. Sun, J.E. Koblinski, and et al. Slug is a downstream mediator of transforming growth factor-beta1-induced matrix metalloproteinase-9 expression and invasion of oral cancer cells J Cell Biochem 108 2009 726 736
22. J.P. Thiery, and J.P. Sleeman Complex networks orchestrate epithelial-mesenchymal transitions Nat Rev Mol Cell Biol 7 2006 131 142
23. C. Gjerdrum, C. Tiron, T. Hoiby, I. Stefansson, H. Haugen, T. Sandal, and et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival Proc Natl Acad Sci U S A 107 2010 1124 1129
24. M.K. Asiedu, F.D. Beauchamp-Perez, J.N. Ingle, M.D. Behrens, D.C. Radisky, and K.L. Knutson AXL induces epithelial-to-mesenchymal transition and regulates the function of breast cancer stem cells Oncogene 33 2014 1316 1324
25. R. Sivakumar, H. Koga, K. Selvendiran, M. Maeyama, T. Ueno, and M. Sata Autocrine loop for IGF-I receptor signaling in SLUG-mediated epithelial-mesenchymal transition Int J Oncol 34 2009 329 338
26. A.F. Hezel, and A.X. Zhu Systemic therapy for biliary tract cancers Oncologist 13 2008 415 423
27. D. Malka, V. Boige, C. Dromain, T. Debaere, M. Pocard, and M. Ducreux Biliary tract neoplasms: update 2003 Curr Opin Oncol 16 2004 364 371
28. Y.J. Kim, S.Y. Yoon, J.T. Kim, E.Y. Song, H.G. Lee, H.J. Son, and et al. NDRG2 expression decreases with tumor stages and regulates TCF/beta-catenin signaling in human colon carcinoma Carcinogenesis 30 2009 598 605
29. S.C. Choi, S.R. Yoon, Y.P. Park, E.Y. Song, J.W. Kim, W.H. Kim, and et al. Expression of NDRG2 is related to tumor progression and survival of gastric cancer patients through Fas-mediated cell death Exp Mol Med 39 2007 705 714
30. S.P. Song, S.B. Zhang, R. Liu, L. Yao, Y.Q. Hao, M.M. Liao, and et al. NDRG2 down-regulation and CD24 up-regulation promote tumor aggravation and poor survival in patients with gallbladder carcinoma Med Oncol 29 2012 1879 1885
31. A. Kim, M.J. Kim, Y. Yang, J.W. Kim, Y.I. Yeom, and J.S. Lim Suppression of NF-kappaB activity by NDRG2 expression attenuates the invasive potential of highly malignant tumor cells Carcinogenesis 30 2009 927 936
32. H. Zhao, Z. Yang, X. Wang, X. Zhang, M. Wang, Y. Wang, and et al. Triptolide inhibits ovarian cancer cell invasion by repression of matrix metalloproteinase 7 and 19 and upregulation of E-cadherin Exp Mol Med 44 2012 633 641
33. M. Muller, I.M. Beck, J. Gadesmann, N. Karschuk, A. Paschen, E. Proksch, and et al. MMP19 is upregulated during melanoma progression and increases invasion of melanoma cells Mod Pathol 23 2010 511 521
34. I. Lettau, K. Hattermann, J. Held-Feindt, R. Brauer, R. Sedlacek, and R. Mentlein Matrix metalloproteinase-19 is highly expressed in astroglial tumors and promotes invasion of glioma cells J Neuropathol Exp Neurol 69 2010 215 223
35. D. Medici, E.D. Hay, and B.R. Olsen Snail and Slug promote epithelial-mesenchymal transition through beta-catenin-T-cell factor-4-dependent expression of transforming growth factor-beta3 Mol Biol Cell 19 2008 4875 4887
36. M. Jechlinger, S. Grunert, and H. Beug Mechanisms in epithelial plasticity and metastasis: insights from 3D cultures and expression profiling J Mammary Gland Biol Neoplasia 7 2002 415 432
37. S. Julien, I. Puig, E. Caretti, J. Bonaventure, L. Nelles, F. van Roy, and et al. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition Oncogene 26 2007 7445 7456
38. W. Cao, J.L. Zhang, D.Y. Feng, X.W. Liu, Y. Li, L.F. Wang, and et al. The effect of adenovirus-conjugated NDRG2 on p53-mediated apoptosis of hepatocarcinoma cells through attenuation of nucleotide excision repair capacity Biomaterials 35 2014 993 1003
39. X. Chang, Z. Li, J. Ma, P. Deng, S. Zhang, Y. Zhi, and et al. DNA methylation of NDRG2 in gastric cancer and its clinical significance Dig Dis Sci 58 2013 715 723