Pigment epithelial-derived factor (PEDF)-triggered lung cancer cell apoptosis relies on p53 protein-driven Fas ligand (fas-L) up-regulation and Fas protein cell surface translocation

Journal of Biological Chemistry

Volumn 289, Issue 44, 2014, Pages 30785-30799

  Li, Lei ^a,c   Yao, Ya Chao ^d   Fang, Shu Huan ^e   Ma, Cai Qi ^a   Cen, Yi ^a   Xu, Zu Min ^f   Dai, Zhi Yu ^a   Li, Cen ^a   Li, Shuai ^a   Zhang, Ting ^a   Hong, Hong Hai ^a   Qi, Wei Wei ^a   Zhou, Ti ^a   Li, Chao Yang ^b   Yang, Xia ^a,b   Gao, Guo Quan ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

^d Department of Orthopedics   (China)

^e GUANGZHOU UNIVERSITY OF CHINESE MEDICINE   (China)

^f GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CELL DEATH; CELL MEMBRANES; DISEASES; PROTEINS; TUMORS;

APOPTOSIS PATHWAYS; HUMAN LUNG CANCER CELLS; INDUCED APOPTOSIS; LUNG CANCER CELLS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PRO-APOPTOTIC EFFECTS; SIGNALING PATHWAYS; THERAPEUTIC STRATEGY;

CELL SIGNALING;

ANTINEOPLASTIC AGENT; CASP8 PROTEIN, HUMAN; CASPASE 8; EYE PROTEIN; FAS ANTIGEN; FAS LIGAND; FAS PROTEIN, HUMAN; NERVE GROWTH FACTOR; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 13; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIGMENT EPITHELIUM-DERIVED FACTOR; PROTEIN P53; PTPN13 PROTEIN, HUMAN; SERINE PROTEINASE INHIBITOR; TP53 PROTEIN, HUMAN;

ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; HUMAN; LUNG TUMOR; MALE; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; NUDE MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; TUMOR CELL LINE; UPREGULATION;

ANIMALS; ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 8; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; EYE PROTEINS; FAS LIGAND PROTEIN; HUMANS; LUNG NEOPLASMS; MALE; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NERVE GROWTH FACTORS; PPAR GAMMA; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 13; SERPINS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84908666153     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.590000     Document Type: Article

References (53)

1. Steele, F. R., Chader, G. J., Johnson, L. V., and Tombran-Tink, J. (1993) Pigment epithelium-derived factor: neurotrophic activity and identification as a member of the serine protease inhibitor gene family. Proc. Natl. Acad. Sci. U. S. A. 90, 1526-1530
2. Zhang, S. X., Wang, J. J., Gao, G., Shao, C., Mott, R., and Ma, J. X. (2006) Pigment epithelium-derived factor (PEDF) is an endogenous antiinflammatory factor. FASEB J. 20, 323-325
3. Stellmach, V., Crawford, S. E., Zhou, W., and Bouck, N. (2001) Prevention of ischemia-induced retinopathy by the natural ocular antiangiogenic agent pigment epithelium-derived factor. Proc. Natl. Acad. Sci. U. S. A. 98, 2593-2597
4. Crowe, S., Wu, L. E., Economou, C., Turpin, S. M., Matzaris, M., Hoehn, K. L., Hevener, A. L., James, D. E., Duh, E. J., and Watt, M. J. (2009) Pigment epithelium-derived factor contributes to insulin resistance in obesity. Cell Metab. 10, 40-47
5. Ek, E. T., Dass, C. R., and Choong, P. F. (2006) Pigment epithelium-derived factor: a multimodal tumor inhibitor. Mol. Cancer Ther. 5, 1641-1646
6. Broadhead, M. L., Dass, C. R., and Choong, P. F. (2009) In vitro and in vivo biological activity of PEDF against a range of tumors. Expert Opin. Ther. Targets 13, 1429-1438
7. Guan, M., Jiang, H., Xu, C., Xu, R., Chen, Z., and Lu, Y. (2007) Adenovirusmediated PEDF expression inhibits prostate cancer cell growth and results in augmented expression of PAI-2. Cancer Biol. Ther. 6, 419-425
8. Guan, M., Pang, C. P., Yam, H. F., Cheung, K. F., Liu, W. W., and Lu, Y. (2004) Inhibition of glioma invasion by overexpression of pigment epitheliumderived factor. Cancer Gene Ther. 11, 325-332
9. Abe, R., Shimizu, T., Yamagishi, S., Shibaki, A., Amano, S., Inagaki, Y., Watanabe, H., Sugawara, H., Nakamura, H., Takeuchi, M., Imaizumi, T., and Shimizu, H. (2004) Overexpression of pigment epithelium-derived factor decreases angiogenesis and inhibits the growth of human malignant melanoma cells in vivo. Am. J. Pathol. 164, 1225-1232
10. Ek, E. T., Dass, C. R., Contreras, K. G., and Choong, P. F. (2007) Pigment epithelium-derived factor overexpression inhibits orthotopic osteosarcoma growth, angiogenesis and metastasis. Cancer Gene Ther. 14, 616-626
11. Chen, J. F., Zhao, W., Zhang, J. Z., Jiang, W. G., and Zhang, L. J. (2009) Effects of pigment epithelial derived factor gene on growth of lung cancer cell and neovascularization: experiments with lung cancer cells and chick embryos. Zhonghua Yi Xue Za Zhi 89, 485-490
12. He, S. S., Shi, H. S., Yin, T., Li, Y. X., Luo, S. T., Wu, Q. J., Lu, L., Wei, Y. Q., and Yang, L. (2012) AAV-mediated gene transfer of human pigment epitheliumderived factor inhibits Lewis lung carcinoma growth in mice. Oncol. Rep. 27, 1142-1148
13. Chen, J., Ye, L., Zhang, L., and Jiang, W. G. (2009) The molecular impact of pigment epithelium-derived factor, PEDF, on lung cancer cells and the clinical significance. Int. J. Oncol. 35, 159-166
14. Peter, M. E., Legembre, P., and Barnhart, B. C. (2005) Does CD95 have tumor promoting activities? Biochim. Biophys. Acta 1755, 25-36
15. Volpert, O. V., Zaichuk, T., Zhou, W., Reiher, F., Ferguson, T. A., Stuart, P. M., Amin, M., Bouck, N. P. (2002) Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat. Med. 8, 349-357
16. Ho, T. C., Chen, S. L., Yang, Y. C., Lo, T. H., Hsieh, J. W., Cheng, H. C., and Tsao, Y. P. (2009) Cytosolic phospholipase A2-γ is an early apoptotic activator in PEDF-induced endothelial cell apoptosis. Am. J. Physiol. Cell Physiol. 296, C273-C284
17. Ho, T. C., Chen, S. L., Yang, Y. C., Liao, C. L., Cheng, H. C., and Tsao, Y. P. (2007) PEDF induces p53-mediated apoptosis through PPAR γ signaling in human umbilical vein endothelial cells. Cardiovasc. Res. 76, 213-223
18. Müschen, M., Warskulat, U., and Beckmann, M. W. (2000) Defining CD95 as a tumor suppressor gene. J. Mol. Med. 78, 312-325
19. Owen-Schaub, L. B., Radinsky, R., Kruzel, E., Berry, K., and Yonehara, S. (1994) Anti-Fas on nonhematopoietic tumors: levels of Fas/APO-1 and bcl-2 are not predictive of biological responsiveness. Cancer Res. 54, 1580-1586
20. Nambu, Y., Hughes, S. J., Rehemtulla, A., Hamstra, D., Orringer, M. B., and Beer, D. G. (1998) Lack of cell surface Fas/APO-1 expression in pulmonary adenocarcinomas. J. Clin. Invest. 101, 1102-1110
21. Viard-Leveugle, I., Veyrenc, S., French, L. E., Brambilla, C., and Brambilla, E. (2003) Frequent loss of Fas expression and function in human lung tumours with overexpression of FasL in small cell lung carcinoma. J. Pathol. 201, 268-277
22. Yang, H., Cheng, R., Liu, G., Zhong, Q., Li, C., Cai, W., Yang, Z., Ma, J., Yang, X., and Gao, G. (2009) PEDF inhibits growth of retinoblastoma by anti-angiogenic activity. Cancer Sci. 100, 2419-2425
23. Lin, C. S., Xie, S. B., Liu, J., Zhao, Z. X., Chong, Y. T., and Gao, Z. L. (2010) Effect of revaccination using different schemes among adults with low or undetectable anti-HBs titers after hepatitis B virus vaccination. Clin. Vaccine Immunol. 17, 1548-1551
24. Zheng, J., Jiang, H. Y., Li, J., Tang, H. C., Zhang, X. M., Wang, X. R., Du, J. T., Li, H. B., and Xu, G. (2012) MicroRNA-23b promotes tolerogenic properties of dendritic cells in vitro through inhibiting Notch1/NF-κB signalling pathways. Allergy 67, 362-370
25. Xu, G., Cheng, L., Wen, W., Oh, Y., Mou, Z., Shi, J., Xu, R., Li, H. (2007) Inverse association between T-cell immunoglobulin and mucin domain-1 and T-bet in a mouse model of allergic rhinitis. Laryngoscope 117, 960-964
26. Weidner, N., Semple, J. P., Welch, W. R., and Folkman, J. (1991) Tumor angiogenesis and metastasis: correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8
27. Chen, M., and Wang, J. (2002) Initiator caspases in apoptosis signaling pathways. Apoptosis 7, 313-319
28. Ehrenschwender, M., and Wajant, H. (2009) The role of FasL and Fas in health and disease. Adv. Exp. Med. Biol. 647, 64-93
29. Kawasaki, M., Kuwano, K., Nakanishi, Y., Hagimoto, N., Takayama, K., Pei, X. H., Maeyama, T., Yoshimi, M., and Hara, N. (2000) Analysis of Fas and Fas ligand expression and function in lung cancer cell lines. Eur. J. Cancer 36, 656-663
30. Bennett, M., Macdonald, K., Chan, S. W., Luzio, J. P., Simari, R., and Weissberg, P. (1998) Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science 282, 290-293
31. Ungefroren, H., Kruse, M. L., Trauzold, A., Roeschmann, S., Roeder, C., Arlt, A., Henne-Bruns, D., and Kalthoff, H. (2001) FAP-1 in pancreatic cancer cells: functional and mechanistic studies on its inhibitory role in CD95-mediated apoptosis. J. Cell Sci. 114, 2735-2746
32. Villa-Morales, M., and Fernández-Piqueras J. (2012) Targeting the Fas/FasL signaling pathway in cancer therapy. Expert Opin. Ther. Targets 16, 85-101
33. Dawson, D. W., Volpert, O. V., Gillis, P., Crawford, S. E., Xu, H., Benedict, W., and Bouck, N. P. (1999) Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285, 245-248
34. Rho, J. K., Choi, Y. J., Ryoo, B. Y., Na, I. I., Yang, S. H., Kim, C. H., Lee, J. C. (2007). p53 enhances gefitinib-induced growth inhibition and apoptosis by regulation of Fas in non-small cell lung cancer. Cancer Res. 67, 1163-1169
35. Müller, M., Strand, S., Hug, H., Heinemann, E. M., Walczak, H., Hofmann, W. J., Stremmel, W., Krammer, P. H., and Galle, P. R. (1997) Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J. Clin. Invest. 99, 403-413
36. Sodeman, T., Bronk, S. F., Roberts, P. J., Miyoshi, H., and Gores, G. J. (2000) Bile salts mediate hepatocyte apoptosis by increasing cell surface trafficking of Fas. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G992-G999
37. Beltinger, C., Fulda, S., Kammertoens, T., Meyer, E., Uckert, W., and Debatin, K. M. (1999) Herpes simplex virus thymidine kinase/ganciclovirinduced apoptosis involves ligand-independent death receptor aggregation and activation of caspases. Proc. Natl. Acad. Sci. U. S. A. 96, 8699-8704
38. Weller, M., Malipiero, U., Rensing-Ehl, A., Barr, P. J., and Fontana, A. (1995) Fas/APO-1 gene transfer for human malignant glioma. Cancer Res. 55, 2936-2944
39. Müller, M., Wilder, S., Bannasch, D., Israeli, D., Lehlbach, K., Li-Weber, M., Friedman, S. L., Galle, P. R., Stremmel, W., Oren, M., Krammer, P. H. (1998) p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med. 188, 2033-2045
40. Munsch, D., Watanabe-Fukunaga, R., Bourdon, J. C., Nagata, S., May, E., Yonish-Rouach, E., and Reisdorf, P. (2000) Human and mouse Fas (APO-1/CD95) death receptor genes each contain a p53-responsive element that is activated by p53 mutants unable to induce apoptosis. J. Biol. Chem. 275, 3867-3872
41. Lee, S. H., Shin, M. S., Park, W. S., Kim, S. Y., Kim, H. S., Han, J. Y., Park, G. S., Dong, S. M., Pi, J. H., Kim, C. S., Kim, S. H., Lee, J. Y., and Yoo, N. J. (1999) Alterations of Fas (Apo-1/CD95) gene in non-small cell lung cancer. Oncogene 18, 3754-3760
42. Pratesi, G., Perego, P., Polizzi, D., Righetti, S. C., Supino, R., Caserini, C., Manzotti, C., Giuliani, F. C., Pezzoni, G., Tognella, S., Spinelli, S., Farrell, N., and Zunino, F. (1999) A novel charged trinuclear platinum complex effective against cisplatin-resistant tumours: hypersensitivity of p53-mutant human tumour xenografts. Br. J. Cancer 80, 1912-1919
43. Buqué, A., Muhialdin, J. Sh., Muñoz, A., Calvo, B., Carrera, S., Aresti, U., Sancho, A., Rubio, I., and López-Vivanco, G. (2012) Molecular mechanism implicated in Pemetrexed-induced apoptosis in human melanoma cells. Mol. Cancer 11, 25
44. Cai, J., Jiang, W. G., Grant, M. B., and Boulton, M. (2006) Pigment epithelium-derived factor inhibits angiogenesis via regulated intracellular proteolysis of vascular endothelial growth factor receptor 1. J. Biol. Chem. 281, 3604-3613
45. Siegel, R. M., Frederiksen, J. K., Zacharias, D. A., Chan, F. K., Johnson, M., Lynch, D., Tsien, R. Y., and Lenardo, M. J. (2000) Fas preassociation required for apoptosis signaling and dominant inhibition by pathogenic mutations. Science 288, 2354-2357
46. Haynes, A. P., Daniels, I., Abhulayha, A. M., Carter, G. I., Metheringham, R., Gregory, C. D., and Thomson, B. J. (2002) CD95 (Fas) expression is regulated by sequestration in the Golgi complex in B-cell lymphoma. Br. J. Haematol. 118, 488-494
47. Ivanov, V. N., Lopez Bergani, P., Maulit, G., Sato, T. A., Sassoon, D., and Ronai, Z. (2003) FAP-1 association with Fas (Apo-1) inhibits Fas expression on the cell surface. Mol. Cell Biol. 23, 3623-3635
48. Yamada, T., Maruyama, M., Fujita, T., Miyabayashi, K., Shinoda, C., Kawagishi, Y., Fujishita, T., Hayashi, R., Miwa, T., Arai, N., Matsui, S., Sugiyama, E., and Kobayashi, M. (2006) Ionizing radiation suppresses FAP-1 mRNA level in A549 cells via p53 activation. FEBS Lett. 580, 4387-4391
49. Irie, S., Li, Y., Kanki, H., Ohyama, T., Deaven, L. L., Somlo, S., and Sato, T. A. (2001) Identification of two Fas-associated phosphatase-1 (FAP-1) promoters in human cancer cells. DNA Seq. 11, 519-526
50. Friesen, C., Herr, I., Krammer, P. H., and Debatin, K. M. (1996) Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat. Med. 2, 574-577
51. Roy, J., Pallepati, P., Bettaieb, A., and Averill-Bates, D. A. (2010) Acrolein induces apoptosis through the death receptor pathway in A549 lung cells: role of p53. Can J. Physiol. Pharmacol. 88, 353-368
52. Bonofiglio, D., Gabriele, S., Aquila, S., Qi, H., Belmonte, M., Catalano, S., and Andò, S. (2009) Peroxisome proliferator-activated receptor γ activates fas ligand gene promoter inducing apoptosis in human breast cancer cells. Breast Cancer Res. Treat 113, 423-434
53. Li, L., Yang, J., Wang, W. W., Yao, Y. C., Fang, S. H., Dai, Z. Y., Hong, H. H., Yang, X., Shuai, X. T., and Gao, G. Q. (2012) Pigment epithelium-derived factor gene loaded in cRGD-PEG-PEI suppresses colorectal cancer growth by targeting endothelial cells. Int. J. Pharm. 438, 1-10