Cadmium down-regulates expression of XIAP at the post-transcriptional level in prostate cancer cells through an NF-κB-independent, proteasome-mediated mechanism

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Golovine, Konstantin ^a   Makhov, Peter ^a   Uzzo, Robert G ^a   Kutikov, Alexander ^a   Kaplan, David J ^a   Fox, Eric ^a   Kolenko, Vladimir M ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; METAL ION; PROTEASOME; TUMOR NECROSIS FACTOR ALPHA; X LINKED INHIBITOR OF APOPTOSIS; XIAP PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER RESISTANCE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; MALE; PHENOTYPIC VARIATION; PROSTATE CANCER; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RNA PROCESSING; TUMOR CELL LINE;

APOPTOSIS; CADMIUM; CELL LINE, TUMOR; DOWN-REGULATION; HUMANS; MALE; POLYMERASE CHAIN REACTION; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 77954332110     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-183     Document Type: Article

References (59)

1. Huff J, Lunn RM, Waalkes MP, Tomatis L, Infante PF. Cadmium-induced cancers in animals and in humans. Int J Occup Environ Health 2007, 13:202-212.
2. Krone CA, Wyse EJ, Ely JT. Cadmium in zinc-containing mineral supplements. Int J Food Sci Nutr 2001, 52:379-382. 10.1080/09637480120057602, 11474903.
3. Kim BJ, Kim MS, Kim KB, Kim KW, Hong YM, Kim IK, Lee HW, Jung YK. Sensitizing effects of cadmium on TNF-alpha- and TRAIL-mediated apoptosis of NIH3T3 cells with distinct expression patterns of p53. Carcinogenesis 2002, 23:1411-1417. 10.1093/carcin/23.9.1411, 12189181.
4. Achanzar WE, Achanzar KB, Lewis JG, Webber MM, Waalkes MP. Cadmium induces c-myc, p53, and c-jun expression in normal human prostate epithelial cells as a prelude to apoptosis. Toxicol Appl Pharmacol 2000, 164:291-300. 10.1006/taap.1999.8907, 10799339.
5. Bakshi S, Zhang X, Godoy-Tundidor S, Cheng RY, Sartor MA, Medvedovic M, Ho SM. Transcriptome analyses in normal prostate epithelial cells exposed to low-dose cadmium: oncogenic and immunomodulations involving the action of tumor necrosis factor. Environ Health Perspect 2008, 116:769-776. 10.1289/ehp.11215, 2430233, 18560533.
6. Nakamura K, Yasunaga Y, Ko D, Xu LL, Moul JW, Peehl DM, Srivastava S, Rhim JS. Cadmium-induced neoplastic transformation of human prostate epithelial cells. Int J Oncol 2002, 20:543-547.
7. Waalkes MP, Rehm S, Cherian MG. Repeated cadmium exposures enhance the malignant progression of ensuing tumors in rats. Toxicol Sci 2000, 54:110-120. 10.1093/toxsci/54.1.110, 10746938.
8. Waalkes MP, Rehm S, Perantoni AO, Coogan TP. Cadmium exposure in rats and tumours of the prostate. IARC Sci Publ 1992, 391-400.
9. Martin JJ, Martin R, Codesal J, Fraile B, Paniagua R, Santamaria L. Cadmium chloride-induced dysplastic changes in the ventral rat prostate: an immunohistochemical and quantitative study. Prostate 2001, 46:11-20. 10.1002/1097-0045(200101)46:1<11::AID-PROS1003>3.0.CO;2-K, 11170127.
10. Brys M, Nawrocka AD, Miekos E, Zydek C, Foksinski M, Barecki A, Krajewska WM. Zinc and cadmium analysis in human prostate neoplasms. Biol Trace Elem Res 1997, 59:145-152. 10.1007/BF02783239, 9522056.
11. Goyer RA, Liu J, Waalkes MP. Cadmium and cancer of prostate and testis. Biometals 2004, 17:555-558. 10.1023/B:BIOM.0000045738.59708.20, 15688863.
12. Deveraux QL, Takahashi R, Salvesen GS, Reed JC. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 1997, 388:300-304. 10.1038/40901, 9230442.
13. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006, 7:988-994. 10.1038/sj.embor.7400795, 1618369, 17016456.
14. Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, de Martin R. Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 2000, 275:22064-22068. 10.1074/jbc.M910346199, 10807933.
15. Uren AG, Beilharz T, O'Connell MJ, Bugg SJ, van Driel R, Vaux DL, Lithgow T. Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc Natl Acad Sci USA 1999, 96:10170-10175. 10.1073/pnas.96.18.10170, 17861, 10468581.
16. Yang Y, Fang S, Jensen JP, Weissman AM, Ashwell JD. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000, 288:874-877. 10.1126/science.288.5467.874, 10797013.
17. Schimmer AD, Dalili S, Batey RA, Riedl SJ. Targeting XIAP for the treatment of malignancy. Cell Death Differ 2006, 13:179-188. 10.1038/sj.cdd.4401826, 16322751.
18. Kashkar H, Deggerich A, Seeger JM, Yazdanpanah B, Wiegmann K, Haubert D, Pongratz C, Kronke M. NF-kappaB-independent down-regulation of XIAP by bortezomib sensitizes HL B cells against cytotoxic drugs. Blood 2007, 109:3982-3988. 10.1182/blood-2006-10-053959, 17185461.
19. Krajewska M, Kim H, Kim C, Kang H, Welsh K, Matsuzawa S, Tsukamoto M, Thomas RG, Assa-Munt N, Piao Z, et al. Analysis of apoptosis protein expression in early-stage colorectal cancer suggests opportunities for new prognostic biomarkers. Clin Cancer Res 2005, 11:5451-5461. 10.1158/1078-0432.CCR-05-0094, 16061861.
20. Hofmann HS, Simm A, Hammer A, Silber RE, Bartling B. Expression of inhibitors of apoptosis (IAP) proteins in non-small cell human lung cancer. J Cancer Res Clin Oncol 2002, 128:554-560. 10.1007/s00432-002-0364-z, 12384799.
21. Mizutani Y, Nakanishi H, Li YN, Matsubara H, Yamamoto K, Sato N, Shiraishi T, Nakamura T, Mikami K, Okihara K, et al. Overexpression of XIAP expression in renal cell carcinoma predicts a worse prognosis. Int J Oncol 2007, 30:919-925.
22. Shiraki K, Sugimoto K, Yamanaka Y, Yamaguchi Y, Saitou Y, Ito K, Yamamoto N, Yamanaka T, Fujikawa K, Murata K, Nakano T. Overexpression of X-linked inhibitor of apoptosis in human hepatocellular carcinoma. Int J Mol Med 2003, 12:705-708.
23. Berezovskaya O, Schimmer AD, Glinskii AB, Pinilla C, Hoffman RM, Reed JC, Glinsky GV. Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells. Cancer Res 2005, 65:2378-2386. 10.1158/0008-5472.CAN-04-2649, 15781653.
24. Nomura T, Yamasaki M, Nomura Y, Mimata H. Expression of the inhibitors of apoptosis proteins in cisplatin-resistant prostate cancer cells. Oncol Rep 2005, 14:993-997.
25. Cao C, Mu Y, Hallahan DE, Lu B. XIAP and survivin as therapeutic targets for radiation sensitization in preclinical models of lung cancer. Oncogene 2004, 23:7047-7052. 10.1038/sj.onc.1207929, 15258565.
26. Meplan C, Mann K, Hainaut P. Cadmium induces conformational modifications of wild-type p53 and suppresses p53 response to DNA damage in cultured cells. J Biol Chem 1999, 274:31663-31670. 10.1074/jbc.274.44.31663, 10531375.
27. Ogunlewe JO, Osegbe DN. Zinc and cadmium concentrations in indigenous blacks with normal, hypertrophic, and malignant prostate. Cancer 1989, 63:1388-1392. 10.1002/1097-0142(19890401)63:7<1388::AID-CNCR2820630725>3.0.CO;2-M, 2465818.
28. Stehlik C, de Martin R, Kumabashiri I, Schmid JA, Binder BR, Lipp J. Nuclear factor (NF)-kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J Exp Med 1998, 188:211-216. 10.1084/jem.188.1.211, 2525542, 9653098.
29. Inoue T, Shiraki K, Fuke H, Yamanaka Y, Miyashita K, Yamaguchi Y, Yamamoto N, Ito K, Sugimoto K, Nakano T. Proteasome inhibition sensitizes hepatocellular carcinoma cells to TRAIL by suppressing caspase inhibitors and AKT pathway. Anticancer Drugs 2006, 17:261-268. 10.1097/00001813-200603000-00004, 16520654.
30. Zhao J, Tenev T, Martins LM, Downward J, Lemoine NR. The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J Cell Sci 2000, 113(Pt 23):4363-4371.
31. Shumilla JA, Wetterhahn KE, Barchowsky A. Inhibition of NF-kappa B binding to DNA by chromium, cadmium, mercury, zinc, and arsenite in vitro: evidence of a thiol mechanism. Arch Biochem Biophys 1998, 349:356-362. 10.1006/abbi.1997.0470, 9448725.
32. Hyun JS, Satsu H, Shimizu M. Cadmium induces interleukin-8 production via NF-kappaB activation in the human intestinal epithelial cell, Caco-2. Cytokine 2007, 37:26-34. 10.1016/j.cyto.2007.02.011, 17391980.
33. Jeong EM, Moon CH, Kim CS, Lee SH, Baik EJ, Moon CK, Jung YS. Cadmium stimulates the expression of ICAM-1 via NF-kappaB activation in cerebrovascular endothelial cells. Biochem Biophys Res Commun 2004, 320:887-892. 10.1016/j.bbrc.2004.05.218, 15240131.
34. Giuliano M, Lauricella M, Calvaruso G, Carabillo M, Emanuele S, Vento R, Tesoriere G. The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res 1999, 59:5586-5595.
35. Golovine K, Makhov P, Uzzo RG, Shaw T, Kunkle D, Kolenko VM. Overexpression of the zinc uptake transporter hZIP1 inhibits nuclear factor-kappaB and reduces the malignant potential of prostate cancer cells in vitro and in vivo. Clin Cancer Res 2008, 14:5376-5384. 10.1158/1078-0432.CCR-08-0455, 2587298, 18765529.
36. Mufti AR, Burstein E, Csomos RA, Graf PC, Wilkinson JC, Dick RD, Challa M, Son JK, Bratton SB, Su GL, et al. XIAP Is a copper binding protein deregulated in Wilson's disease and other copper toxicosis disorders. Mol Cell 2006, 21:775-785. 10.1016/j.molcel.2006.01.033, 16543147.
37. Freedman LP, Luisi BF, Korszun ZR, Basavappa R, Sigler PB, Yamamoto KR. The function and structure of the metal coordination sites within the glucocorticoid receptor DNA binding domain. Nature 1988, 334:543-546. 10.1038/334543a0, 3043231.
38. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 2003, 3:46-54. 10.1038/nrc968, 12509766.
39. Srinivasula SM, Ashwell JD. IAPs: what's in a name?. Mol Cell 2008, 30:123-135. 10.1016/j.molcel.2008.03.008, 2677451, 18439892.
40. Makhov P, Golovine K, Uzzo RG, Rothman J, Crispen PL, Shaw T, Scoll BJ, Kolenko VM. Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis. Cell Death Differ 2008, 15:1745-1751. 10.1038/cdd.2008.106, 2585550, 18617897.
41. Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS, Reed JC. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 1999, 18:5242-5251. 10.1093/emboj/18.19.5242, 1171595, 10508158.
42. Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003, 192:95-117. 10.1016/S0300-483X(03)00305-6, 14580780.
43. Joseph P. Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol 2009, 238:272-279. 10.1016/j.taap.2009.01.011, 19371617.
44. Waalkes MP, Diwan BA. Cadmium-induced inhibition of the growth and metastasis of human lung carcinoma xenografts: role of apoptosis. Carcinogenesis 1999, 20:65-70. 10.1093/carcin/20.1.65, 9934851.
45. Waalkes MP, Diwan BA, Weghorst CM, Bare RM, Ward JM, Rice JM. Anticarcinogenic effects of cadmium in B6C3F1 mouse liver and lung. Toxicol Appl Pharmacol 1991, 110:327-335. 10.1016/S0041-008X(05)80015-8, 1891777.
46. Schimmer AD, Welsh K, Pinilla C, Wang Z, Krajewska M, Bonneau MJ, Pedersen IM, Kitada S, Scott FL, Bailly-Maitre B, et al. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 2004, 5:25-35. 10.1016/S1535-6108(03)00332-5, 14749124.
47. Belyaeva EA, Dymkowska D, Wieckowski MR, Wojtczak L. Mitochondria as an important target in heavy metal toxicity in rat hepatoma AS-30D cells. Toxicol Appl Pharmacol 2008, 231:34-42. 10.1016/j.taap.2008.03.017, 18501399.
48. Saelens X, Festjens N, Walle LV, van Gurp M, van Loo G, Vandenabeele P. Toxic proteins released from mitochondria in cell death. Oncogene 2004, 23:2861-2874. 10.1038/sj.onc.1207523, 15077149.
49. Althaus J, Siegelin MD, Dehghani F, Cilenti L, Zervos AS, Rami A. The serine protease Omi/HtrA2 is involved in XIAP cleavage and in neuronal cell death following focal cerebral ischemia/reperfusion. Neurochem Int 2007, 50:172-180. 10.1016/j.neuint.2006.07.018, 16978742.
50. Yang QH, Church-Hajduk R, Ren J, Newton ML, Du C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev 2003, 17:1487-1496. 10.1101/gad.1097903, 196079, 12815069.
51. Yang QH, Du C. Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. J Biol Chem 2004, 279:16963-16970. 10.1074/jbc.M401253200, 14960576.
52. Shi YH, Ding WX, Zhou J, He JY, Xu Y, Gambotto AA, Rabinowich H, Fan J, Yin XM. Expression of X-linked inhibitor-of-apoptosis protein in hepatocellular carcinoma promotes metastasis and tumor recurrence. Hepatology 2008, 48:497-507. 10.1002/hep.22393, 2768766, 18666224.
53. Hwang C, Oetjen KA, Kosoff D, Wojno KJ, Albertelli MA, Dunn RL, Robins DM, Cooney KA, Duckett CS. X-linked inhibitor of apoptosis deficiency in the TRAMP mouse prostate cancer model. Cell Death Differ 2008, 15:831-840. 10.1038/cdd.2008.15, 2710036, 18259199.
54. Seligson DB, Hongo F, Huerta-Yepez S, Mizutani Y, Miki T, Yu H, Horvath S, Chia D, Goodglick L, Bonavida B. Expression of X-linked inhibitor of apoptosis protein is a strong predictor of human prostate cancer recurrence. Clin Cancer Res 2007, 13:6056-6063. 10.1158/1078-0432.CCR-07-0960, 17947468.
55. Seeger JM, Brinkmann K, Yazdanpanah B, Haubert D, Pongratz C, Coutelle O, Kronke M, Kashkar H. Elevated XIAP expression alone does not confer chemoresistance. Br J Cancer 102:1717-1723. 10.1038/sj.bjc.6605704, 20485285.
56. Albrecht AL, Singh RK, Somji S, Sens MA, Sens DA, Garrett SH. Basal and metal-induced expression of metallothionein isoform 1 and 2 genes in the RWPE-1 human prostate epithelial cell line. J Appl Toxicol 2008, 28:283-293. 10.1002/jat.1277, 17590860.
57. Kolenko VM, Uzzo RG, Dulin N, Hauzman E, Bukowski R, Finke JH. Mechanism of apoptosis induced by zinc deficiency in peripheral blood T lymphocytes. Apoptosis 2001, 6:419-429. 10.1023/A:1012497926537, 11595831.
58. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
59. Webster LC, Zhang K, Chance B, Ayene I, Culp JS, Huang WJ, Wu FY, Ricciardi RP. Conversion of the E1A Cys4 zinc finger to a nonfunctional His2, Cys2 zinc finger by a single point mutation. Proc Natl Acad Sci USA 1991, 88:9989-9993. 10.1073/pnas.88.22.9989, 52852, 1835093.