Inhibition of the proliferation and invasion of hepatocellular carcinoma cells by lipocalin 2 through blockade of JNK and PI3K/Akt signaling

International Journal of Oncology

Volumn 38, Issue 2, 2011, Pages 325-333

  Lee, Eun Kyoung ^a,b   Kim, Hyun Jun ^a   Lee, Kong Ju ^a   Lee, Ho Jeong ^a   Lee, Ju Seog ^c   Kim, Dae Ghon ^d   Hong, Soon Won ^e   Yoon, Yeup ^a   Kim, Jang Seong ^a  

^a Mogam Biotechnology Research Institute   (South Korea)

^b Seoul National University   (South Korea)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d Chonbuk National University Medical School   (South Korea)

^e Yonsei University College of Medicine   (South Korea)

Author keywords

1 phosphatidylinositol 3 kinase; Hepatocellular carcinoma; Lipocalin 2; MAP kinase signaling; Matrix metalloproteinase 2

Indexed keywords

NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CANCER INHIBITION; CANCER INVASION; CELL PROLIFERATION; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACUTE-PHASE PROTEINS; ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOCALINS; LIVER NEOPLASMS; MALE; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS;

EID: 78651232349     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2010.854     Document Type: Article

References (49)

1. Bratt T: Lipocalins and cancer. Biochim Biophys Acta 1482: 318-326, 2000.
2. Kjeldsen L, Johnsen AH, Sengelov H and Borregaard N: Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 268: 10425-10432, 1993.
3. Chu ST, Lin HJ, Huang HL and Chen YH: The hydrophobic pocket of 24p3 protein from mouse uterine luminal fluid: fatty acid and retinol binding activity and predicted structural similarity to lipocalins. J Pept Res 52: 390-397, 1998.
4. Yang J, Goetz D, Li JY, et al: An iron delivery pathway mediated by a lipocalin. Mol Cell 10: 1045-1056, 2002.
5. Devireddy LR, Teodoro JG, Richard FA and Green MR: Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293: 829-834, 2001.
6. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN and Strong RK: The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10: 1033-1043, 2002.
7. Flo TH, Smith KD, Sato S, et al: Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921, 2004.
8. Hraba-Renevey S, Turler H, Kress M, Salomon C and Weil R: SV40-induced expression of mouse gene 24p3 involves a posttranscriptional mechanism. Oncogene 4: 601-608, 1989.
9. Liu Q and Nilsen-Hamilton M: Identification of a new acute phase protein. J Biol Chem 270: 22565-22570, 1995.
10. Friedl A, Stoesz SP, Buckley P and Gould MN: Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues. Cell type-specific pattern of expression. Histochem J 31: 433-441, 1999.
11. Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M and Kjeldsen L: Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut 38: 414-420, 1996. (Pubitemid 126423216)
12. Chuma M, Sakamoto M, Yamazaki K, et al: Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology 37: 198-207, 2003. (Pubitemid 36042161)
13. Patil MA, Chua MS, Pan KH, et al: An integrated data analysis approach to characterize genes highly expressed in hepatocellular carcinoma. Oncogene 24: 3737-3747, 2005.
14. Lee HJ, Lee EK, Lee KJ, Hong SW, Yoon Y and Kim JS: Ectopic expression of neutrophil gelatinase-associated lipocalin suppresses the invasion and liver metastasis of colon cancer cells. Int J Cancer 118: 2490-2497, 2006.
15. Lee JS, Chu IS, Mikaelyan A, et al: Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat Genet 36: 1306-1311, 2004. (Pubitemid 39577940)
16. Lee JS, Heo J, Libbrecht L, et al: A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12: 410-416, 2006.
17. Zhang D, Bar-Eli M, Meloche S and Brodt P: Dual regulation of MMP-2 expression by the type 1 insulin-like growth factor receptor: the phosphatidylinositol 3-kinase/Akt and Raf/ERK pathways transmit opposing signals. J Biol Chem 279: 19683-19690, 2004. (Pubitemid 38623405)
18. Lee JS, Chu IS, Heo J, et al: Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40: 667-676, 2004. (Pubitemid 39265589)
19. Hanai J, Mammoto T, Seth P, et al: Lipocalin 2 diminishes invasiveness and metastasis of Ras-transformed cells. J Biol Chem 280: 13641-13647, 2005.
20. Schutte K, Bornschein J and Malfertheiner P: Hepatocellular carcinoma-epidemiological trends and risk factors. Dig Dis 27: 80-92, 2009.
21. Thomas MB and Abbruzzese JL: Opportunities for targeted therapies in hepatocellular carcinoma. J Clin Oncol 23: 8093-8108, 2005.
22. Jayaraman A, Roberts KA, Yoon J, et al: Identification of neutrophil gelatinase-associated lipocalin (NGAL) as a discriminatory marker of the hepatocyte-secreted protein response to IL-1beta: a proteomic analysis. Biotechnol Bioeng 91: 502-515, 2005.
23. Cowland JB, Sorensen OE, Sehested M and Borregaard N: Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 171: 6630-6639, 2003.
24. Moss SF and Blaser MJ: Mechanisms of disease: Inflammation and the origins of cancer. Nat Clin Pract Oncol 2: 90-97, 2005.
25. Cowland JB and Borregaard N: Molecular characterization and pattern of tissue expression of the gene for neutrophil gelatinase-associated lipocalin from humans. Genomics 45: 17-23, 1997.
26. Meheus LA, Fransen LM, Raymackers JG, et al: Identification by microsequencing of lipopolysaccharide-induced proteins secreted by mouse macrophages. J Immunol 151: 1535-1547, 1993.
27. Bratt T, Ohlson S and Borregaard N: Interactions between neutrophil gelatinase-associated lipocalin and natural lipophilic ligands. Biochim Biophys Acta 1472: 262-269, 1999.
28. Missiaglia E, Blaveri E, Terris B, et al: Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int J Cancer 112: 100-112, 2004.
29. Santin AD, Zhan F, Bellone S, et al: Gene expression profiles in primary ovarian serous papillary tumors and normal ovarian epithelium: identification of candidate molecular markers for ovarian cancer diagnosis and therapy. Int J Cancer 112: 14-25, 2004.
30. Leng X, Ding T, Lin H, et al: Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 69: 8579-8584, 2009.
31. Yang J, Bielenberg DR, Rodig SJ, et al: Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 106: 3913-3918, 2009.
32. Berger T, Cheung CC, Elia AJ and Mak TW: Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc Natl Acad Sci USA 107: 2995-3000, 2010.
33. Leng X, Lin H, Ding T, et al: Lipocalin 2 is required for BCRABL-induced tumorigenesis. Oncogene 27: 6110-6119, 2008.
34. Iannetti A, Pacifico F, Acquaviva R, et al: The neutrophil gelatinase-associated lipocalin (NGAL), a NF-kappaB-regulated gene, is a survival factor for thyroid neoplastic cells. Proc Natl Acad Sci USA 105: 14058-14063, 2008.
35. Hu L, Hittelman W, Lu T, et al: NGAL decreases E-cadherin-mediated cell-cell adhesion and increases cell motility and invasion through Rac1 in colon carcinoma cells. Lab Invest 89: 531-548, 2009.
36. Tong Z, Kunnumakkara AB, Wang H, et al: Neutrophil gelatinase-associated lipocalin: a novel suppressor of invasion and angiogenesis in pancreatic cancer. Cancer Res 68: 6100-6108, 2008.
37. Yamada SD, Hickson JA, Hrobowski Y, et al: Mitogen-activated protein kinase kinase 4 (MKK4) acts as a metastasis suppressor gene in human ovarian carcinoma. Cancer Res 62: 6717-6723, 2002.
38. Xiao L and Lang W: A dominant role for the c-Jun NH2- terminal kinase in oncogenic ras-induced morphologic transformation of human lung carcinoma cells. Cancer Res 60: 400-408, 2000.
39. Chang CC, Shih JY, Jeng YM, et al: Connective tissue growth factor and its role in lung adenocarcinoma invasion and metastasis. J Natl Cancer Inst 96: 364-375, 2004.
40. Xie D, Nakachi K, Wang H, Elashoff R and Koeffler HP: Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Cancer Res 61: 8917-8923, 2001.
41. Wenger C, Ellenrieder V, Alber B, et al: Expression and differential regulation of connective tissue growth factor in pancreatic cancer cells. Oncogene 18: 1073-1080, 1999.
42. Wang GL, Iakova P, Wilde M, Awad S and Timchenko NA: Liver tumors escape negative control of proliferation via PI3K/ Akt-mediated block of C/EBP alpha growth inhibitory activity. Genes Dev 18: 912-925, 2004.
43. Qi HL, Zhang Y, Ma J, Guo P, Zhang XY and Chen HL: Insulin/ protein kinase B signalling pathway upregulates metastasis-related phenotypes and molecules in H7721 human hepatocarcinoma cell line. Eur J Biochem 270: 3795-3805, 2003. (Pubitemid 37123251)
44. Sugioka Y, Watanabe T, Inagaki Y, et al: c-Jun NH2-terminal kinase pathway is involved in constitutive matrix metalloproteinase- 1 expression in a hepatocellular carcinoma-derived cell line. Int J Cancer 109: 867-874, 2004.
45. Liu SL, Lin X, Shi DY, Cheng J, Wu CQ and Zhang YD: Reactive oxygen species stimulated human hepatoma cell proliferation via cross-talk between PI3-K/PKB and JNK signaling pathways. Arch Biochem Biophys 406: 173-182, 2002.
46. Herbst RS, Yano S, Kuniyasu H, et al: Differential expression of E-cadherin and type IV collagenase genes predicts outcome in patients with stage I non-small cell lung carcinoma. Clin Cancer Res 6: 790-797, 2000.
47. Slaton JW, Inoue K, Perrotte P, et al: Expression levels of genes that regulate metastasis and angiogenesis correlate with advanced pathological stage of renal cell carcinoma. Am J Pathol 158: 735-743, 2001.
48. Herrera CA, Xu L, Bucana CD, et al: Expression of metastasis-related genes in human epithelial ovarian tumors. Int J Oncol 20: 5-13, 2002.
49. Kuniyasu H, Ukai R, Johnston D, Troncoso P, Fidler IJ and Pettaway CA: The relative mRNA expression levels of matrix metalloproteinase to E-cadherin in prostate biopsy specimens distinguishes organ-confined from advanced prostate cancer at radical prostatectomy. Clin Cancer Res 9: 2185-2194, 2003.