Lipocalin-2 negatively modulates the epithelial-to-mesenchymal transition in hepatocellular carcinoma through the epidermal growth factor (TGF-beta1)/Lcn2/Twist1 pathway

Hepatology

Volumn 58, Issue 4, 2013, Pages 1349-1361

  Wang, Yun Peng ^a   Yu, Goung Ran ^a   Lee, Mi Jin ^a   Lee, Sang Yeop ^b   Chu, In Sun ^b   Leem, Sun Hee ^c   Kim, Dae Ghon ^a  

^a Chonbuk National University Medical School   (South Korea)

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

^c Dong A University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CYTOKERATIN 18; CYTOKERATIN 8; EPIDERMAL GROWTH FACTOR; FIBRONECTIN; NERVE CELL ADHESION MOLECULE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN;

ARTICLE; CELL DIFFERENTIATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; UPREGULATION;

ACUTE-PHASE PROTEINS; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HETEROGRAFTS; HUMANS; LIPOCALINS; LIVER NEOPLASMS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NUCLEAR PROTEINS; PHENOTYPE; PROTO-ONCOGENE PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; TWIST TRANSCRIPTION FACTOR;

EID: 84884979461     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26467     Document Type: Article

References (45)

1. Flower DR. The lipocalin protein family: structure and function. Biochem J 1996;318:1-14.
2. Kjeldsen L, Bainton DF, Sengelov H, Borregaard N. Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 1994;83:799-807.
3. Bartsch S, Tschesche H. Cloning and expression of human neutrophil lipocalin cDNA derived from bone marrow and ovarian cancer cells. FEBS Lett 1995;357:255-259.
4. Lim R, Ahmed N, Borregaard N, Riley C, Wafai R, Thompson EW, et al. Neutrophil gelatinase-associated lipocalin (NGAL) an early-screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition. Int J Cancer 2007;120:2426-2434.
5. Stoesz SP, Friedl A, Haag JD, Lindstrom MJ, Clark GM, Gould MN. Heterogeneous expression of the lipocalin NGAL in primary breast cancers. Int J Cancer 1998;79:565-572.
6. Playford RJ, Belo A, Poulsom R, Fitzgerald AJ, Harris K, Pawluczyk I, et al. Effects of mouse and human lipocalin homologues 24p3/lcn2 and neutrophil gelatinase-associated lipocalin on gastrointestinal mucosal integrity and repair. Gastroenterology 2006;131:809-817.
7. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008;108:389-397.
8. Shi H, Gu Y, Yang J, Xu L, Mi W, Yu W. Lipocalin 2 promotes lung metastasis of murine breast cancer cells. J Exp Clin Cancer Res 2008;27:83.
9. Hanai J, Mammoto T, Seth P, Mori K, Karumanchi SA, Barasch J, et al. Lipocalin 2 diminishes invasiveness and metastasis of Ras-transformed cells. J Biol Chem 2005;280:13641-13647.
10. Lee HJ, Lee EK, Lee KJ, Hong SW, Yoon Y, Kim JS. Ectopic expression of neutrophil gelatinase-associated lipocalin suppresses the invasion and liver metastasis of colon cancer cells. Int J Cancer 2006;118:2490-2497.
11. Tong Z, Kunnumakkara AB, Wang H, Matsuo Y, Diagaradjane P, Harikumar KB, et al. Neutrophil gelatinase-associated lipocalin: a novel suppressor of invasion and angiogenesis in pancreatic cancer. Cancer Res 2008; 1;68:6100-6108.
12. Chuma M, Sakamoto M, Yamazaki K, Ohta T, Ohki M, Asaka M, et al. Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology 2003;37:198-207.
13. Patil MA, Chua MS, Pan KH, Lin R, Lih CJ, Cheung ST, et al. An integrated data analysis approach to characterize genes highly expressed in hepatocellular carcinoma. Oncogene 2005;24:3737-3747.
14. Lee EK, Kim HJ, Lee KJ, Lee HJ, Lee JS, Kim DG, et al. Inhibition of the proliferation and invasion of hepatocellular carcinoma cells by lipocalin 2 through blockade of JNK and PI3K/Akt signaling. Int J Oncol 2011;38:325-333.
15. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003;15:740-746.
16. Bates RC, Mercurio AM. The epithelial-mesenchymal transition (EMT) and colorectal cancer progression. Cancer Biol Ther 2005;4:365-370.
17. Gilles C, Thompson EW. The epithelial to mesenchymal transition and metastatic progression in carcinoma. Breast J 1996;2:83-96.
18. Pallier K, Cessot A, Côté JF, Just PA, Cazes A, Fabre E, et al. TWIST1 a new determinant of epithelial to mesenchymal transition in EGFR mutated lung adenocarcinoma. PLoS One 2012;7:e29954.
19. Kim DG, Park SY, Kim H, Chun YH, Moon WS, Park SH. A comprehensive karyotypic analysis on a newly established sarcomatoid hepatocellular carcinoma cell line SH-J1 by comparative genomic hybridization and chromosome painting. Cancer Genet Cytogenet 2002;132:120-124.
20. Cui XD, Lee MJ, Yu GR, Kim IH, Yu HC, Song EY, et al. EFNA1 ligand and its receptor EphA2: potential biomarkers for hepatocellular carcinoma. Int J Cancer 2010;126:940-949.
21. Lee MJ, Yu GR, Yoo HJ, Kim JH, Yoon BI, Choi YK, et al. ANXA8 down-regulation by EGF-FOXO4 signaling is involved in cell scattering and tumor metastasis of cholangiocarcinoma. Gastroenterology 2009;137:1138-1150.
22. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998;95:14863-14868.
23. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, et al. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006;366:2-16.
24. Salomon DS, Brandt R, Ciardiello F, Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 1995;19:183-232.
25. Korc M, Chandrasekar B, Yamanaka Y, Friess H, Buchier M, Beger HG. Overexpression of the epidermal growth factor receptor in human pancreatic cancer is associated with concomitant increases in the levels of epidermal growth factor and transforming growth factor alpha. J Clin Invest 1992;90:1352-1360.
26. Poon SL, Hammond GT, Leung PCK. Epidermal growth factor-induced GnRH-II synthesis contributes to ovarian cancer cell invasion. Mol Endocrinol 2009;23:1646-1656.
27. Lee M-Y, Chou C-Y, Tang M-J, Shen M-R. Epithelial-mesenchymal transition in cervical cancer: correlation with tumor progression, epidermal growth factor receptor overexpression, and snail up-regulation. Clin Cancer Res 2008;14:4743-4750.
28. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 2003;4:499-515.
29. Kimura F, Iwaya K, Kawaguchi T, Kaise H, Yamada K, Mukai K, et al. Epidermal growth factor-dependent enhancement of invasiveness of squamous cell carcinoma of the breast. Cancer Sci 2010;101:1133-1140.
30. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009;28:15-33.
31. Matsuo N, Shiraha H, Fujikawa T, Takaoka N, Ueda N, Tanaka S, et al. Twist expression promotes migration and invasion in hepatocellular carcinoma. BMC Cancer 2009;9:240.
32. Jayaraman A, Roberts KA, Yoon J, Yarmush DM, Duan X, Lee K, et al. Identification of neutrophil gelatinase-associated lipocalin (NGAL) as a discriminatory marker of the hepatocyte-secreted protein response to IL-1beta: proteomic analysis. Biotechnol Bioeng 2005;91:502-515.
33. Cowland JB, Sorensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 2003;171:6630-6639.
34. Moss SF, Blaser MJ. Mechanisms of disease: inflammation and the origins of cancer. Nat Clin Pract Oncol 2005;2:90-97.
35. Srisomsap C, Sawangareetrakul P, Subhasitanont P, Chokchaichamnankit D, Chiablaem K, Bhudhisawasdi V, et al. Proteomic studies of cholangiocarcinoma and hepatocellular carcinoma cell secretomes. J Biomed Biotechnol 2010;2010:437143.
36. Hraba-Renevey S, Turler H, Kress M, Salomon C, Weil R. SV40-induced expression of mouse gene 24p3 involves a posttranscriptional mechanism. Oncogene 1989;4:601-608.
37. Friedl A, Stoesz SP, Buckley P, Gould MN. Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues. Cell type-specific pattern of expression. Histochem J 1999;31:433-441.
38. Leng X, Lin H, Ding T, Wang Y, Wu Y, Klumpp S, et al. Lipocalin 2 is required for BCR-ABL-induced tumorigenesis. Oncogene 2008;27:6110-6119.
39. Leng X, Ding T, Lin H, Wang Y, Hu L, Hu J, et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009;69:8579-8584.
40. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL, et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci U S A 2009;106:3913-3918.
41. Berger T, Cheung CC, Elia AJ, Mak TW. Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc Natl Acad Sci U S A 2010;107:2995-3000.
42. Hu L, Hittelman W, Lu T, Ji P, Arlinghaus R, Shmulevich I, et al. NGAL decreases E-cadherin mediated cell-cell adhesion and increases cell motility and invasion through Rac1 in colon carcinoma cells. Lab Invest 2009;89:531-548.
43. Li EM, Xu LY, Cai WJ, Xiong HQ, Shen ZY, Zeng Y. Functions of neutrophil gelatinase-associated lipocalin in the esophageal carcinoma cell line SHEEC. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2003;35:247-254.
44. Zhao XL, Sun BC. Promotion of hepatocellular carcinoma metastasis through matrix metalloproteinase activation by epithelial-mesenchymal transition regulator Twist1. J Cell Mol Med 2011;15:691-700.
45. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008;68:3645-3654.