Lipocalin-2 Induces Apoptosis in Human Hepatocellular Carcinoma Cells Through Activation of Mitochondria Pathways

Cell Biochemistry and Biophysics

Volumn 64, Issue 3, 2012, Pages 177-186

  Chien, Ming Hsien ^a,b   Ying, Tsung Ho ^c,d   Yang, Shun Fa ^c,d   Yu, Ji Kuen ^e   Hsu, Chih Wei ^e   Hsieh, Shu Ching ^c   Hsieh, Yi Hsien ^c,d  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e TUNGS' TAICHUNG METROHARBOR HOSPITAL   (Taiwan)

Author keywords

Apoptosis; Hepatocellular carcinoma; Lipocalin 2; Mitochondrial membrane potential

Indexed keywords

EID: 84869089517     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-012-9370-1     Document Type: Article

References (41)

1. Bosch, F. X., Ribes, J., & Borras, J. (1999). Epidemiology of primary liver cancer. Seminars in Liver Disease, 19, 271-285.
2. Teo, E. K., & Fock, K. M. (2001). Hepatocellular carcinoma: An Asian perspective. Digestive Diseases, 19, 263-268.
3. Farazi, P. A., & DePinho, R. A. (2006). Hepatocellular carcinoma pathogenesis: From genes to environment. Nature Reviews Cancer, 6, 674-687.
4. Flower, D. R., North, A. C., & Sansom, C. E. (2000). The lipocalin protein family: Structural and sequence overview. Biochimica et Biophysica Acta, 1482, 9-24.
5. Kehrer, J. P. (2010). Lipocalin-2: Pro- or Anti-apoptotic? Cell Biology and Toxicology, 26, 83-89.
6. Stoesz, S. P., Friedl, A., Haag, J. D., Lindstrom, M. J., et al. (1998). Heterogeneous expression of the lipocalin NGAL in primary breast cancers. International Journal of Cancer, 79, 565-572.
7. Zhang, H., Xu, L., Xiao, D., et al. (2007). Upregulation of neutrophil gelatinase-associated lipocalin in oesophageal squamous cell carcinoma: Significant correlation with cell differentiation and tumour invasion. Journal of Clinical Pathology, 60, 555-561.
8. Friedl, A., Stoesz, S. P., Buckley, P., & Gould, M. N. (1999). Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues. Cell type-specific pattern of expression. Histochemical Journal, 31, 433-441.
9. Nielsen, B. S., Borregaard, N., Bundgaard, J. R., et al. (1996). Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut, 38, 414-420.
10. Patil, M. A., Chua, M. S., Pan, K. H., et al. (2005). An integrated data analysis approach to characterize genes highly expressed in hepatocellular carcinoma. Oncogene, 24, 3737-3747.
11. Cho, H., & Kim, J. H. (2009). Lipocalin2 expressions correlate significantly with tumor differentiation in epithelial ovarian cancer. Journal of Histochemistry and Cytochemistry, 57, 513-521.
12. Alpizar-Alpizar, W., Laerum, O. D., Illemann, M., et al. (2009). Neutrophil gelatinase-associated lipocalin (NGAL/LCN2) is upregulated in gastric mucosa infected with helicobacter pylori. Virchows Archiv, 455, 225-233.
13. Tong, Z., Kunnumakkara, A. B., Wang, H., et al. (2008). Neutrophil gelatinase-associated lipocalin: A novel suppressor of invasion and angiogenesis in pancreatic cancer. Cancer Research, 68, 6100-6108.
14. Miharada, K., Hiroyama, T., Sudo, K., et al. (2005). Lipocalin 2 functions as a negative regulator of red blood cell production in an autocrine fashion. FASEB J, 19, 1881-1883.
15. Tong, Z., Wu, X., Ovcharenko, D., et al. (2005). Neutrophil gelatinase-associated lipocalin as a survival factor. Biochemical Journal, 391, 441-448.
16. Nelson, A. M., Zhao, W., Gilliland, K. L., et al. (2008). Neutrophil gelatinase-associated lipocalin mediates 13-cis retinoic acid-induced apoptosis of human sebaceous gland cells. J Clin Investig, 118, 1468-1478.
17. Wu, T. T., Hsieh, Y. H., Hsieh, Y. S., & Liu, J. Y. (2008). Reduction of PKC alpha decreases cell proliferation, migration, and invasion of human malignant hepatocellular carcinoma. Journal of Cellular Biochemistry, 103, 9-20.
18. Tsai, H. T., Su, P. H., Lee, T. H., et al. (2001). Significant elevation and correlation of plasma neutrophil gelatinase associated lipocalin and its complex with matrix metalloproteinase-9 in patients with pelvic inflammatory disease. Clinica Chimica Acta, 412, 1252-1256.
19. Jung, J. I., Lim, S. S., Choi, H. J., et al. (2006). Isoliquiritigenin induces apoptosis by depolarizing mitochondrial membranes in prostate cancer cells. Journal of Nutritional Biochemistry, 17, 689-696.
20. Hsieh, Y. H., Wu, T. T., Huang, C. Y., et al. (2007). p38 mitogen-activated protein kinase pathway is involved in protein kinase Calpha-regulated invasion in human hepatocellular carcinoma cells. Cancer Research, 67, 4320-4327.
21. Lee, E. K., Kim, H. J., Lee, K. J., et al. (2011). 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, 38, 325-333.
22. Devireddy, L. R., Teodoro, J. G., Richard, F. A., & Green, M. R. (2001). Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science, 293, 829-834.
23. Lin, H. H., Li, W. W., Lee, Y. C., & Chu, S. T. (2007). Apoptosis induced by uterine 24p3 protein in endometrial carcinoma cell line. Toxicology, 234, 203-215.
24. Lee, S., Lee, J., Kim, S., et al. (2007). A dual role of lipocalin 2 in the apoptosis and deramification of activated microglia. Journal of Immunology, 179, 3231-3241.
25. Berger, T., Togawa, A., Duncan, G. S., et al. (2006). Lipocalin 2-deficient mice exhibit increased sensitivity to escherichia coli infection but not to ischemia-reperfusion injury. Proceedings of the National Academy of Sciences USA, 103, 1834-1839.
26. Mannelqvist, M., Stefansson, I. M., Wik, E., et al. (2012). Lipocalin 2 expression is associated with aggressive features of endometrial cancer. BMC Cancer, 12, 169.
27. Iannetti, A., Pacifico, F., Acquaviva, R., et al. (2008). The neutrophil gelatinase associated lipocalin (NGAL), a NF-kappaB-regulated gene, is a survival factor for thyroid neoplastic cells. Proceedings of the National Academy of Sciences USA, 105, 14058-14063.
28. Bauer, M., Eickhoff, J. C., Gould, M. N., Mundhenke, C., et al. (2008). Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Research and Treatment, 108, 389-397.
29. Yang, J., & Moses, M. A. (2009). Lipocalin 2: A multifaceted modulator of human cancer. Cell Cycle, 8, 2347-2352.
30. Leng, X., Wu, Y., & Arlinghaus, R. B. (2011). Relationships of lipocalin 2 with breast tumorigenesis and metastasis. Journal of Cellular Physiology, 226, 309-314.
31. Yang, J., Bielenberg, D. R., Rodig, S. J., et al. (2009). Lipocalin 2 promotes breast cancer progression. Proceedings of the National Academy of Sciences USA, 106, 3913-3918.
32. Leng, X., Ding, T., Lin, H., et al. (2009). Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Research, 69, 8579-8584.
33. Lee, H. J., Lee, E. K., Lee, K. J., et al. (2006). Ectopic expression of neutrophil gelatinase associated lipocalin suppresses the invasion and liver metastasis of colon cancer cells. International Journal of Cancer, 118, 2490-2497.
34. Crompton, M., Barksby, E., Johnson, N., & Capano, M. (2002). Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie, 84, 143-152.
35. Green, D. R. (2005). Apoptotic pathways: Ten minutes to dead. Cell, 121, 671-674.
36. Armstrong, J. S. (2006). The role of the mitochondrial permeability transition in cell death. Mitochondrion, 6, 225-234.
37. Radogna, F., Cristofanon, S., Paternoster, L., et al. (2008). Melatonin antagonizes the intrinsic pathway of apoptosis via mitochondrial targeting of bcl-2. Journal of Pineal Research, 44, 316-325.
38. Cory, S., Huang, D. C., & Adams, J. M. (2003). The bcl-2 family: Roles in cell survival and oncogenesis. Oncogene, 22, 8590-8607.
39. Salvesen, G. S., & Riedl, S. J. (2008). Caspase mechanisms. Advances in Experimental Medicine and Biology, 615, 13-23.
40. Peter, M. E., & Krammer, P. H. (2003). The cd95(apo-1/fas) disc and beyond. Cell Death and Differentiation, 10, 26-35.
41. Li, F., Srinivasan, A., Wang, Y., et al. (1997). Cell-specific induction of apoptosis by microinjection of cytochrome c. Bcl-xl has activity independent of cytochrome c release. Journal of Biological Chemistry, 272, 30299-30305.