PIAS1-modulated Smad2/4 complex activation is involved in zinc-induced cancer cell apoptosis

Cell Death and Disease

Volumn 4, Issue 9, 2013, Pages

  Yang, N ^a   Zhao, B ^a   Rasul, A ^a   Qin, H ^a   Li, J ^b   Li, X ^a  

^a NORTHEAST NORMAL UNIVERSITY   (China)

^b JILIN UNIVERSITY   (China)

Author keywords

PIAS1; Prostate cancer; Smad2; Smad4; Zinc

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN P53; SMAD2 PROTEIN; SMAD4 PROTEIN; ZINC;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CELL STRAIN LNCAP; CHEMOPROPHYLAXIS; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; MULTIPLE CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; THERAPY EFFECT; TRANSACTIVATION;

APOPTOSIS; CELL LINE, TUMOR; CELL NUCLEUS; CLONE CELLS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENE SILENCING; HUMANS; MALE; MODELS, BIOLOGICAL; NEOPLASMS; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN TRANSPORT; SMAD2 PROTEIN; SMAD4 PROTEIN; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; ZINC;

EID: 84885001106     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.333     Document Type: Article

References (52)

1. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012; 62: 220-241
2. Sim HG, Cheng CW. Changing demography of prostate cancer in Asia. Eur J Cancer 2005; 41: 834-845
3. Franklin RB, Costello LC. Zinc as an anti-Tumor agent in prostate cancer and in other cancers. Arch Biochem Biophys 2007; 463: 211-217
4. Costello LC, Franklin RB, Feng P, Tan M, Bagasra O. Zinc and prostate cancer: A critical scientific, medical, and public interest issue (United States). Cancer Causes Control 2005; 16: 901-915
5. Huang L, Kirschke CP, Zhang Y. Decreased intracellular zinc in human tumorigenic prostate epithelial cells: A possible role in prostate cancer progression. Cancer Cell Int 2006; 6: 10
6. Johnson LA, Kanak MA, Kajdacsy-Balla A, Pestaner JP, Bagasra O. Differential zinc accumulation and expression of human zinc transporter 1 (hZIP1) in prostate glands. Methods 2010; 52: 316-321
7. Kelleher SL, McCormick NH, Velasquez V, Lopez V. Zinc in specialized secretory tissues: Roles in the pancreas, prostate, and mammary gland. Adv Nutr 2011; 2: 101-111
8. Feng P, Li T, Guan Z, Franklin RB, Costello LC. The involvement of Bax in zinc-induced mitochondrial apoptogenesis in malignant prostate cells. Mol Cancer 2008; 7: 25
9. Feng P, Li TL, Guan ZX, Franklin RB, Costello LC. Direct effect of zinc on mitochondrial apoptogenesis in prostate cells. Prostate 2002; 52: 311-318
10. Liang JY, Liu YY, Zou J, Franklin RB, Costello LC, Feng P. Inhibitory effect of zinc on human prostatic carcinoma cell growth. Prostate 1999; 40: 200-207
11. Boulaire J, Fotedar A, Fotedar R. The functions of the cdk-cyclin kinase inhibitor p21WAF1. Pathol Biol (Paris) 2000; 48: 190-202
12. Chi XZ, Yang JO, Lee KY, Ito K, Sakakura C, Li QL et al. RUNX3 suppresses gastric epithelial cell growth by inducing p21(WAF1/Cip1) expression in cooperation with transforming growth factor {beta}-Activated SMAD. Mol Cell Biol 2005; 25: 8097-8107
13. Derynck R, Akhurst RJ, Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 2001; 29: 117-129
14. Pardali K, Kowanetz M, Heldin CH, Moustakas A. Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J Cell Physiol 2005; 204: 260-272
15. Saramaki A, Banwell CM, Campbell MJ, Carlberg C. Regulation of the human p21(waf1/ cip1) gene promoter via multiple binding sites for p53 and the vitamin D3 receptor. Nucleic Acids Res 2006; 34: 543-554
16. de Caestecker MP, Piek E, Roberts AB. Role of transforming growth factor-beta signaling in cancer. J Natl Cancer Inst 2000; 92: 1388-1402
17. Perttu MC, Martikainen PM, Huhtala HS, Blauer M, Tammela TL, Tuohimaa PJ et al. Altered levels of Smad2 and Smad4 are associated with human prostate carcinogenesis. Prostate Cancer Prostatic Dis 2006; 9: 185-189
18. Tu WH, Thomas TZ, Masumori N, Bhowmick NA, Gorska AE, Shyr Y et al. The loss of TGFbeta signaling promotes prostate cancer metastasis. Neoplasia 2003; 5: 267-277
19. Yang J, Wahdan-Alaswad R, Danielpour D. Critical role of Smad2 in tumor suppression and transforming growth factor-beta-induced apoptosis of prostate epithelial cells. Cancer Res 2009; 69: 2185-2190
20. Yang G, Yang X. Smad4-mediated TGF-beta signaling in tumorigenesis. Int J Biol Sci 2010; 6: 1-8
21. Liang M, Melchior F, Feng XH, Lin X. Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1. J Biol Chem 2004; 279: 22857-22865
22. Long J, Matsuura I, He D, Wang G, Shuai K, Liu F. Repression of Smad transcriptional activity by PIASy, an inhibitor of activated STAT. Proc Natl Acad Sci USA 2003; 100: 9791-9796
23. Long J, Wang G, Matsuura I, He D, Liu F. Activation of Smad transcriptional activity by protein inhibitor of activated STAT3 (PIAS3). Proc Natl Acad Sci USA 2004; 101: 99-104
24. Gross M, Liu B, Tan J, French FS, Carey M, Shuai K. Distinct effects of PIAS proteins on androgen-mediated gene activation in prostate cancer cells. Oncogene 2001; 20: 3880-3887
25. Megidish T, Xu JH, Xu CW. Activation of p53 by protein inhibitor of activated Stat1 (PIAS1). J Biol Chem 2002; 277: 8255-8259
26. Shuai K. Regulation of cytokine signaling pathways by PIAS proteins. Cell Res 2006; 16: 196-202
27. Linja MJ, Porkka KP, Kang Z, Savinainen KJ, Janne OA, Tammela TL et al. Expression of androgen receptor coregulators in prostate cancer. Clin Cancer Res 2004; 10: 1032-1040
28. Chen P, Zhao D, Sun Y, Huang L, Zhang S, Yuan Y. Protein inhibitor of activated STAT-1 is downregulated in gastric cancer tissue and involved in cell metastasis. Oncol Rep 2012; 28: 2149-2155
29. Coppola D, Parikh V, Boulware D, Blanck G. Substantially reduced expression of PIAS1 is associated with colon cancer development. J Cancer Res Clin Oncol 2009; 135: 1287-1291
30. Wei J, Costa C, Ding Y, Zou Z, Yu L, Sanchez JJ et al. mRNA expression of BRCA1, PIAS1, and PIAS4 and survival after second-line docetaxel in advanced gastric cancer. J Natl Cancer Inst 2011; 103: 1552-1556
31. Feng P, Liang JY, Li TL, Guan ZX, Zou J, Franklin R et al. Zinc induces mitochondria apoptogenesis in prostate cells. Mol Urol 2000; 4: 31-36
32. Iguchi K, Hamatake M, Ishida R, Usami Y, Adachi T, Yamamoto H et al. Induction of necrosis by zinc in prostate carcinoma cells and identification of proteins increased in association with this induction. Eur J Biochem 1998; 253: 766-770
33. Liang JY, Liu YY, Zou J, Franklin RB, Costello LC, Feng P. Inhibitory effect of zinc on human prostatic carcinoma cell growth. Prostate 1999; 40: 200-207
34. Timofeeva O, Nadler JV. Facilitation of granule cell epileptiform activity by mossy fiberreleased zinc in the pilocarpine model of temporal lobe epilepsy. Brain Res 2006; 1078: 227-234
35. Moustakas A, Kardassis D. Regulation of the human p21/WAF1/Cip1 promoter in hepatic cells by functional interactions between Sp1 and Smad family members. Proc Natl Acad Sci USA 1998; 95: 6733-6738
36. Tang MR, Wang YX, Guo S, Han SY, Wang D. CSMD1 exhibits antitumor activity in A375 melanoma cells through activation of the Smad pathway. Apoptosis 2012; 17: 927-937
37. Franklin RB, Costello LC. The important role of the apoptotic effects of zinc in the development of cancers. J Cell Biochem 2009; 106: 750-757
38. Costello LC, Franklin RB. Novel role of zinc in the regulation of prostate citrate metabolism and its implications in prostate cancer. Prostate 1998; 35: 285-296
39. Yan M, Hardin K, Ho E. Differential response to zinc-induced apoptosis in benign prostate hyperplasia and prostate cancer cells. J Nutr Biochem 2010; 21: 687-694
40. Zaichick V, Sviridova TV, Zaichick SV. Zinc in the human prostate gland: Normal, hyperplastic and cancerous. Int Urol Nephrol 1997; 29: 565-574
41. Klein C, Creach K, Irintcheva V, Hughes KJ, Blackwell PL, Corbett JA et al. Zinc induces ERK-dependent cell death through a specific Ras isoform. Apoptosis 2006; 11: 1933-1944
42. Song K, Cornelius SC, Reiss M, Danielpour D. Insulin-like growth factor-I inhibits transcriptional responses of transforming growth factor-beta by phosphatidylinositol 3-kinase/Akt-dependent suppression of the activation of Smad3 but not Smad2. J Biol Chem 2003; 278: 38342-38351
43. Petersen M, Pardali E, van der Horst G, Cheung H, van den Hoogen C, van der Pluijm G et al. Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis. Oncogene 2010; 29: 1351-1361
44. Tannehill-Gregg SH, Kusewitt DF, Rosol TJ, Weinstein M. The roles of Smad2 and Smad3 in the development of chemically induced skin tumors in mice. Vet Pathol 2004; 41: 278-282
45. Chang CC, Lin DY, Fang HI, Chen RH, Shih HM. Daxx mediates the small ubiquitin-like modifierdependent transcriptional repression of Smad4. J Biol Chem 2005; 280: 10164-10173
46. Levy C, Sonnenblick A, Razin E. Role played by microphthalmia transcription factor phosphorylation and its Zip domain in its transcriptional inhibition by PIAS3. Mol Cell Biol 2003; 23: 9073-9080
47. Prigge JR, Schmidt EE. Interaction of protein inhibitor of activated STAT (PIAS) proteins with the TATA-binding protein, TBP. J Biol Chem 2006; 281: 12260-12269
48. Datto MB, Yu Y, Wang XF. Functional analysis of the transforming growth factor beta responsive elements in the WAF1/Cip1/p21 promoter. J Biol Chem 1995; 270: 28623-28628
49. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-Type 1 gene. EMBO J 1998; 17: 3091-3100
50. Sui G, Soohoo C, Affar el B, Gay F, Shi Y, Forrester WC. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc Natl Acad Sci USA 2002; 99: 5515-5520
51. Rasul A, Ding C, Li X, Khan M, Yi F, Ali M et al. Dracorhodin perchlorate inhibits PI3K/Akt and NF-kappaB activation, up-regulates the expression of p53, and enhances apoptosis. Apoptosis 2012; 17: 1104-1119
52. Mattia M, Gottifredi V, McKinney K, Prives C. p53-Dependent p21 mRNA elongation is impaired when DNA replication is stalled. Mol Cell Biol 2007; 27: 1309-1320