Influence of zinc deficiency on Akt-Mdm2-p53 and Akt-p21 signaling axes in normal and malignant human prostate cells

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 5, 2009, Pages

  Han, Chung Ting ^a,d   Schoene, Norberta W ^b   Lei, D Kai Y ^a,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Cell cycle progression; Signal transduction; Zinc status

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN P21; PROTEIN P53;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CELL STRAIN LNCAP; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; PRIORITY JOURNAL; PROSTATE EPITHELIUM; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; ZINC DEFICIENCY;

BLOTTING, WESTERN; CELL CYCLE; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOPLASM; FLOW CYTOMETRY; HUMANS; MALE; PHOSPHORYLATION; PROSTATE; PROSTATIC NEOPLASMS; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MDM2; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; ZINC;

EID: 70449625426     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00042.2009     Document Type: Article

References (52)

1. Alshatwi AA, Han CT, Schoene NW, Lei KY. Nuclear accumulations of p53 and Mdm2 are accompanied by reductions in c-Abl and p300 in zinc-depleted human hepatoblastoma cells. Exp Biol Med (Maywood) 231: 611-618, 2006.
2. Ayala G, Thompson T, Yang G, Frolov A, Li R, Scardino P, Ohori M, Wheeler T, Harper W. High levels of phosphorylated form of Akt-1 in prostate cancer and non-neoplastic prostate tissues are strong predictors of biochemical recurrence. Clin Cancer Res 10: 6572-6578, 2004. (Pubitemid 39346553)
3. Bao S, Knoell DL. Zinc modulates airway epithelium susceptibility to death receptor-mediated apoptosis. Am J Physiol Lung Cell Mol Physiol 290: L433-L441, 2006. (Pubitemid 43725087)
4. 1 phase of the on-going cell cycle. J Cell Biochem 90: 244-252, 2003.
5. 2+. Biochem J 308: 659-664, 1995.
6. Chou SS, Clegg MS, Momma TY, Niles BJ, Duffy JY, Daston GP, Keen CL. Alterations in protein kinase C activity and processing during zinc-deficiency-induced cell death. Biochem J 383: 63-71, 2004. (Pubitemid 39389451)
7. Clegg MS, Hanna LA, Niles BJ, Momma TY, Keen CL. Zinc deficiency-induced cell death. IUBMB Life 57: 661-669, 2005.
8. Costello LC, Franklin RB. Novel role of zinc in the regulation of prostate citrate metabolism and its implications in prostate cancer. Prostate 35: 285-296, 1998.
9. Datta K, Bellacosa A, Chan TO, Tsichlis PN. Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J Biol Chem 271: 30835-30839, 1996. (Pubitemid 26404106)
10. Desouki M, Geradts J, Milon B, Franklin R, Costello L. hZip2 and hZip3 zinc transporters are down regulated in human prostate adenocarcinomatous glands. Mol Cancer 6: 37, 2007. (Pubitemid 46939545)
11. Fanzo JC, Reaves SK, Cui L, Zhu L, Lei KY. p53 protein and p21 mRNA levels and caspase-3 activity are altered by zinc status in aortic endothelial cells. Am J Physiol Cell Physiol 283: C631-C638, 2002. (Pubitemid 34787546)
12. Fanzo JC, Reaves SK, Cui L, Zhu L, Wu JYJ, Wang YR, Lei KY. Zinc status affects p53, gadd45, and c-fos expression and caspase-3 activity in human bronchial epithelial cells. Am J Physiol Cell Physiol 281: C751-C757, 2001. (Pubitemid 32880879)
13. Feustel A, Wennrich R. Zinc and cadmium in cell fractions of prostatic cancer tissues of different histological grading in comparison to BPH and normal prostate. Urol Res 12: 147-150, 1984. (Pubitemid 14138954)
14. Franklin RB, Ma J, Zou J, Guan Z, Kukoyi BI, Feng P, Costello LC. Human ZIP1 is a major zinc uptake transporter for the accumulation of zinc in prostate cells. J Inorg Biochem 96: 435-442, 2003. (Pubitemid 36900381)
15. Gallus S, Foschi R, Negri E, Talamini R, Franceschi S, Montella M, Ramazzotti V, Tavani A, Dal Maso L, La Vecchia C. Dietary zinc and prostate cancer risk: a case-control study from Italy. Eur Urol 52: 1052-1056, 2007. (Pubitemid 47337030)
16. Gao N, Zhang Z, Jiang BH, Shi X. Role of PI3K/AKT/mTOR signaling in the cell cycle progression of human prostate cancer. Biochem Biophys Res Commun 310: 1124-1132, 2003. (Pubitemid 37237653)
17. Gendimenico GJ, Bouquin PL, Tramposch KM. Diphenylamine-colorimetric method for DNA assay: a shortened procedure by incubating samples at 50° C. Anal Biochem 173: 45-48, 1988.
18. Gottlieb TM, Leal JF, Seger R, Taya Y, Oren M. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene 21: 1299-1303, 2002. (Pubitemid 34185247)
19. Gottschalk AR, Doan A, Nakamura JL, Haas-Kogan DA, Stokoe D. Inhibition of phosphatidylinositol-3-kinase causes cell death through a protein kinase B (PKB)-dependent mechanism and growth arrest through a PKB-independent mechanism. Int J Radiat Oncol Biol Phys 61: 1183-1188, 2005. (Pubitemid 40340914)
20. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, Nakatani Y, Livingston DM. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 300: 342-344, 2003. (Pubitemid 36433728)
21. Harreman MT, Kline TM, Milford HG, Harben MB, Hodel AE, Corbett AH. Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J Biol Chem 279: 20613-20621, 2004.
22. Hasumi M, Suzuki K, Matsui H, Koike H, Ito K, Yamanaka H. Regulation of metallothionein and zinc transporter expression in human prostate cancer cells and tissues. Cancer Lett 200: 187-195, 2003. (Pubitemid 38366101)
23. Iguchi K, Hamatake M, Ishida R, Usami Y, Adachi T, Yamamoto H, Koshida K, Uchibayashi T, Hirano K. Induction of necrosis by zinc in prostate carcinoma cells and identification of proteins increased in association with this induction. Eur J Biochem 253: 766-770, 1998. (Pubitemid 28223546)
24. Kim S, Jung Y, Kim D, Koh H, Chung J. Extracellular zinc activates p70 S6 kinase through the phosphatidylinositol 3-kinase signaling pathway. J Biol Chem 275: 25979-25984, 2000. (Pubitemid 30676637)
25. 473) is an excellent predictor of poor clinical outcome in prostate cancer. Cancer Res 64: 5232-5236, 2004.
26. Leitzmann MF, Stampfer MJ, Wu K, Colditz GA, Willett WC, Giovannucci EL. Zinc supplement use and risk of prostate cancer. J Natl Cancer Inst 95: 1004-1007, 2003. (Pubitemid 36896718)
27. Li Y, Dowbenko D, Lasky LA. Akt/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/WAF1 and promotes cell survival. J Biol Chem 277: 11352-11361, 2002. (Pubitemid 34952901)
28. Liang JY, Liu YY, Zou J, Franklin RB, Costello LC, Feng P. Inhibitory effect of zinc on human prostatic carcinoma cell growth. Prostate 40: 200-207, 1999. (Pubitemid 29334868)
29. Mackenzie GG, Keen CL, Oteiza PI. Microtubules are required for NF-κB nuclear translocation in neuroblastoma IMR-32 cells: modulation by zinc. J Neurochem 99: 402-415, 2006.
30. Mayo LD, Dixon JE, Durden DL, Tonks NK, Donner DB. PTEN protects p53 from Mdm2 and sensitizes cancer cells to chemotherapy. J Biol Chem 277: 5484-5489, 2002.
31. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 98: 11598-11603, 2001.
32. Momand J, Wu HH, Dasgupta G. MDM2-master regulator of the p53 tumor suppressor protein. Gene 242: 15-29, 2000. (Pubitemid 30064488)
33. Ogawara Y, Kishishita S, Obata T, Isazawa Y, Suzuki T, Tanaka K, Masuyama N, Gotoh Y. Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J Biol Chem 277: 21843-21850, 2002. (Pubitemid 34952337)
34. Ostrakhovitch EA, Cherian MG. Differential regulation of signal transduction pathways in wild type and mutated p53 breast cancer epithelial cells by copper and zinc. Arch Biochem Biophys 423: 351-361, 2004.
35. Reaves SK, Fanzo JC, Arima K, Wu JYJ, Wang YR, Lei KY. Expression of the p53 tumor suppressor gene is up-regulated by depletion of intracellular zinc in HepG2 cells. J Nutr 130: 1688-1694, 2000. (Pubitemid 30451054)
36. Rosoff B. Studies of zinc in normal and neoplastic prostatic tissues. Prog Clin Biol Res 75A: 447-457, 1981.
37. 2/M blockage and the enhanced phosphorylation of p53 and p38 in zinc supplemented normal human bronchial epithelial cells. Exp Biol Med (Maywood) 233: 317-327, 2008.
38. Suhy DA, Simon KD, Linzer DIH, O'Halloran TV. Metallothionein is part of a zinc-scavenging mechanism for cell survival under conditions of extreme zinc deprivation. J Biol Chem 274: 9183-9192, 1999. (Pubitemid 129517880)
39. Tang Xh, Shay NF. Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. J Nutr 131: 1414-1420, 2001.
40. Testa JR, Bellacosa A. Akt plays a central role in tumorigenesis. Proc Natl Acad Sci USA 98: 10983-10985, 2001. (Pubitemid 32928669)
41. Torres J, Pulido R. The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J Biol Chem 276: 993-998, 2001. (Pubitemid 32096519)
42. Uzzo RG, Crispen PL, Golovine K, Makhov P, Horwitz EM, Kolenko VM. Diverse effects of zinc on NF-κB and AP-1 transcription factors: implications for prostate cancer progression. Carcinogenesis 27: 1980-1990, 2006.
43. Uzzo RG, Leavis P, Hatch W, Gabai VL, Dulin N, Zvartau N, Kolenko VM. Zinc inhibits nuclear factor-κB activation and sensitizes prostate cancer cells to cytotoxic agents. Clin Cancer Res 8: 3579-3583, 2002. (Pubitemid 35340736)
44. Vazquez F, Grossman SR, Takahashi Y, Rokas MV, Nakamura N, Sellers WR. Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J Biol Chem 276: 48627-48630, 2001. (Pubitemid 37370556)
45. Vazquez F, Ramaswamy S, Nakamura N, Sellers WR. Phosphorylation of the PTEN tail regulates protein stability and function. Mol Cell Biol 20: 5010-5018, 2000. (Pubitemid 30431555)
46. Warbrick E. The puzzle of PCNA's many partners. Bioessays 22: 997-1006, 2000.
47. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, Vessella RL, Said JW, Isaacs WB, Sawyers CL. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci USA 95: 5246-5250, 1998. (Pubitemid 28208583)
48. Wu JYJ, Wu Y, Reaves SK, Wang YR, Lei PP, Lei KY. Apolipoprotein A-I gene expression is regulated by cellular zinc status in Hep G2 cells. Am J Physiol Cell Physiol 277: C537-C544, 1999. (Pubitemid 29458188)
49. Wu JYJ, Zhang JJ, Wang Y, Reaves SK, Wang YR, Lei PP, Lei KY. Regulation of apolipoprotein A-I gene expression in Hep G2 cells depleted of Cu by cupruretic tetramine. Am J Physiol Cell Physiol 273: C1362-C1370, 1997. (Pubitemid 27479161)
50. Wu W, Wang X, Zhang W, Reed W, Samet JM, Whang YE, Ghio AJ. Zinc-induced PTEN protein degradation through the proteasome pathway in human airway epithelial cells. J Biol Chem 278: 28258-28263, 2003. (Pubitemid 36900027)
51. Zaichick V, Sviridova TV, Zaichick SV. Zinc in the human prostate gland: normal, hyperplastic and cancerous. Int Urol Nephrol 29: 565-574, 1997. (Pubitemid 27489811)
52. Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, Hung MC. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat Cell Biol 3: 973-982, 2001. (Pubitemid 34428742)