Beryllium sulfate induces p21 CDKN1A expression and a senescence-like cell cycle arrest in susceptible cancer cell types

BioMetals

Volumn 23, Issue 6, 2010, Pages 1061-1073

  Gorjala, Priyatham ^a   Gary, Ronald K ^a  

^a UNIVERSITY OF NEVADA   (United States)

Author keywords

Beryllium sulfate; Cell cycle arrest; Glioma; p53; Senescence

Indexed keywords

BERYLLIUM SULFATE; BETA GALACTOSIDASE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; PROTEIN P53;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL TYPE; COLON CARCINOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; GLIOBLASTOMA; GROWTH INHIBITION; GROWTH REGULATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENESCENCE; SIGNAL TRANSDUCTION; WILD TYPE;

BERYLLIUM; BETA-GALACTOSIDASE; CELL AGING; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENES, P53; GLIOBLASTOMA; HUMANS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 78349308691     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10534-010-9352-y     Document Type: Article

References (50)

1. J Ashby M Ishidate Jr GD Stoner MA Morgan F Ratpan RD Callander 1990 Studies on the genotoxicity of beryllium sulphate in vitro and in vivo Mutat Res 240 217 225 1:CAS:528:DyaK3cXhsFemsrk%3D 10.1016/0165-1218(90)90061-6 2179717
2. CJ Bakkenist R Drissi J Wu MB Kastan JS Dome 2004 Disappearance of the telomere dysfunction-induced stress response in fully senescent cells Cancer Res 64 3748 3752 1:CAS:528:DC%2BD2cXksVKguro%3D 10.1158/0008-5472.CAN-04-0453 15172978 (Pubitemid 38697281)
3. J Bartek J Lukas 2001 Pathways governing G1/S transition and their response to DNA damage FEBS Lett 490 117 122 1:CAS:528:DC%2BD3MXht1Ortrs%3D 10.1016/S0014-5793(01)02114-7 11223026 (Pubitemid 32171930)
4. SE Beard SR Capaldi P Gee 1996 Stress responses to DNA damaging agents in the human colon carcinoma cell line, RKO Mutat Res 371 1 13 1:CAS:528:DyaK28Xms1eks74%3D 10.1016/S0165-1218(96)90089-0 8950345 (Pubitemid 26386332)
5. I Ben-Porath RA Weinberg 2005 The signals and pathways activating cellular senescence Int J Biochem Cell Biol 37 961 976 1:CAS:528: DC%2BD2MXhvVGjs7c%3D 10.1016/j.biocel.2004.10.013 15743671 (Pubitemid 40311739)
6. JM Bland DG Altman 1996 Transformations, means, and confidence intervals BMJ 312 1079 1:STN:280:DyaK283gs1ymsA%3D%3D 8616417
7. M Caicedo JJ Jacobs A Reddy NJ Hallab 2008 Analysis of metal ion-induced DNA damage, apoptosis, and necrosis in human (Jurkat) T-cells demonstrates Ni2 + and V3 + are more toxic than other metals: Al3+, Be2+, Co2+, Cr3+, Cu2+, Fe3+, Mo5+, Nb5+, Zr2+ J Biomed Mater Res A 86 905 913 18050301
8. SS Coates BE Lehnert S Sharma SM Kindell RK Gary 2007 Beryllium induces premature senescence in human fibroblasts J Pharmacol Exp Ther 322 70 79 1:CAS:528:DC%2BD2sXntl2jtr4%3D 10.1124/jpet.106.118018 17395767 (Pubitemid 46956349)
9. TL DeWeese JC Walsh LE Dillehay TD Kessis L Hedrick KR Cho WG Nelson 1997 Human papillomavirus E6 and E7 oncoproteins alter cell cycle progression but not radiosensitivity of carcinoma cells treated with low-dose-rate radiation Int J Radiat Oncol Biol Phys 37 145 154 1:CAS:528:DyaK2sXhvValu78%3D 9054890
10. GP Dimri X Lee G Basile M Acosta G Scott C Roskelley EE Medrano M Linskens I Rubelj O Pereira-Smith, et al. 1995 A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proc Natl Acad Sci USA 92 9363 9367 1:CAS:528:DyaK2MXosVWlur0%3D 10.1073/pnas.92.20.9363 7568133
11. NA Franken C Van Bree J Haveman 2004 Differential response to radiation of TP53-inactivated cells by overexpression of dominant-negative mutant TP53 or HPVE6 Radiat Res 161 504 510 1:CAS:528:DC%2BD2cXjs1yhsLo%3D 10.1667/RR3160 15161374 (Pubitemid 40754218)
12. RK Gary SM Kindell 2005 Quantitative assay of senescence-associated beta-galactosidase activity in mammalian cell extracts Anal Biochem 343 329 334 1:CAS:528:DC%2BD2MXmvVWltLg%3D 10.1016/j.ab.2005.06.003 16004951 (Pubitemid 41074047)
13. R Gilsbach M Kouta H Bonisch M Bruss 2006 Comparison of in vitro and in vivo reference genes for internal standardization of real-time PCR data Biotechniques 40 173 177 1:CAS:528:DC%2BD28XhsFWntbs%3D 10.2144/000112052 16526406 (Pubitemid 46542637)
14. V Gire D Wynford-Thomas 1998 Reinitiation of DNA synthesis and cell division in senescent human fibroblasts by microinjection of anti-p53 antibodies Mol Cell Biol 18 1611 1621 1:CAS:528:DyaK1cXhtlehs7o%3D 9488478
15. T Gordon D Bowser 2003 Beryllium: genotoxicity and carcinogenicity Mutat Res 533 99 105 1:CAS:528:DC%2BD3sXpt1erurg%3D 14643414
16. M Gorospe X Wang NJ Holbrook 1998 p53-dependent elevation of p21Waf1 expression by UV light is mediated through mRNA stabilization and involves a vanadate-sensitive regulatory system Mol Cell Biol 18 1400 1407 1:CAS:528:DyaK1cXhtleiu78%3D 9488455
17. T Hara M Omura-Minamisawa Y Kang C Cheng T Inoue 2008 Flavopiridol potentiates the cytotoxic effects of radiation in radioresistant tumor cells in which p53 is mutated or Bcl-2 is overexpressed Int J Radiat Oncol Biol Phys 71 1485 1495 1:CAS:528:DC%2BD1cXoslWqsLY%3D 18640498
18. BA Hart M Absher D Sylwester 1982 The effect of beryllium on the growth of human lung fibroblasts Environ Res 27 150 158 1:CAS:528:DyaL38XhtFOjtbk%3D 10.1016/0013-9351(82)90065-2 7067673 (Pubitemid 12106170)
19. CE Helt WA Cliby PC Keng RA Bambara MA O'Reilly 2005 Ataxia telangiectasia mutated (ATM) and ATM and Rad3-related protein exhibit selective target specificities in response to different forms of DNA damage J Biol Chem 280 1186 1192 1:CAS:528:DC%2BD2MXitFCnsw%3D%3D 10.1074/jbc.M410873200 15533933
20. U Herbig WA Jobling BP Chen DJ Chen JM Sedivy 2004 Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a) Mol Cell 14 501 513 1:CAS:528:DC%2BD2cXksl2jsrk%3D 10.1016/S1097-2765(04)00256-4 15149599 (Pubitemid 38648803)
21. R Hill E Bodzak MD Blough PW Lee 2008 p53 Binding to the p21 promoter is dependent on the nature of DNA damage Cell Cycle 7 2535 2543 1:CAS:528:DC%2BD1cXht1elsbjN 10.4161/cc.7.16.6440 18719376
22. N Ishii D Maier A Merlo M Tada Y Sawamura AC Diserens EG Van Meir 1999 Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines Brain Pathol 9 469 479 1:CAS:528:DyaK1MXkvFGjtL4%3D 10.1111/j.1750-3639.1999.tb00536.x 10416987
23. K Itahana G Dimri J Campisi 2001 Regulation of cellular senescence by p53 Eur J Biochem 268 2784 2791 1:CAS:528:DC%2BD3MXktVSktro%3D 10.1046/j.1432-1327. 2001.02228.x 11358493 (Pubitemid 32862960)
24. LQ Jia M Osada C Ishioka M Gamo S Ikawa T Suzuki H Shimodaira T Niitani T Kudo M Akiyama N Kimura M Matsuo H Mizusawa N Tanaka H Koyama M Namba R Kanamaru T Kuroki 1997 Screening the p53 status of human cell lines using a yeast functional assay Mol Carcinog 19 243 253 1:CAS:528:DyaK2sXlslWlsbw%3D 10.1002/(SICI)1098-2744(199708)19:4<243::AID-MC5>3.0.CO;2-D 9290701 (Pubitemid 27392003)
25. N Keshava G Zhou M Spruill M Ensell TM Ong 2001 Carcinogenic potential and genomic instability of beryllium sulphate in BALB/c-3T3 cells Mol Cell Biochem 222 69 76 1:CAS:528:DC%2BD3MXnvVeht74%3D 10.1023/A:1017911306449 11678613 (Pubitemid 32910322)
26. TD Kessis RJ Slebos WG Nelson MB Kastan BS Plunkett SM Han AT Lorincz L Hedrick KR Cho 1993 Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage Proc Natl Acad Sci USA 90 3988 3992 1:CAS:528:DyaK3sXkt1Glsbc%3D 10.1073/pnas.90.9.3988 8387205
27. T Komata Y Kondo S Koga SC Ko LW Chung S Kondo 2000 Combination therapy of malignant glioma cells with 2-5A-antisense telomerase RNA and recombinant adenovirus p53 Gene Ther 7 2071 2079 1:CAS:528:DC%2BD3MXis1yjtQ%3D%3D 10.1038/sj.gt.3301327 11223987 (Pubitemid 32118075)
28. N Kubota S Okada T Inada K Ohnishi T Ohnishi 2000 Wortmannin sensitizes human glioblastoma cell lines carrying mutant and wild type TP53 gene to radiation Cancer Lett 161 141 147 1:CAS:528:DC%2BD3cXot12rtLg%3D 10.1016/S0304-3835(00)00614-5 11090962
29. ND Lakin SP Jackson 1999 Regulation of p53 in response to DNA damage Oncogene 18 7644 7655 1:CAS:528:DC%2BD3cXmt1Srsw%3D%3D 10.1038/sj.onc.1203015 10618704
30. NM Lehnert RK Gary BL Marrone BE Lehnert 2001 Inhibition of normal human lung fibroblast growth by beryllium Toxicology 160 119 127 1:CAS:528: DC%2BD3MXhvVajtLc%3D 10.1016/S0300-483X(00)00439-X 11246132 (Pubitemid 32200472)
31. JN Li M Gorospe FJ Chrest TS Kumaravel MK Evans WF Han ES Pizer 2001 Pharmacological inhibition of fatty acid synthase activity produces both cytostatic and cytotoxic effects modulated by p53 Cancer Res 61 1493 1499 1:CAS:528:DC%2BD3MXhvVeltLg%3D 11245456
32. Y Liu WF Bodmer 2006 Analysis of P53 mutations and their expression in 56 colorectal cancer cell lines Proc Natl Acad Sci USA 103 976 981 1:CAS:528:DC%2BD28XhsVKgtL0%3D 10.1073/pnas.0510146103 16418264 (Pubitemid 43212207)
33. Mendenhall W (1983) Introduction to probability and statistics. Duxbury Press, Boston, p 342
34. R Mirzayans A Scott M Cameron D Murray 2005 Induction of accelerated senescence by gamma radiation in human solid tumor-derived cell lines expressing wild-type TP53 Radiat Res 163 53 62 1:CAS:528:DC%2BD2MXhslGltQ%3D%3D 10.1667/RR3280 15606307 (Pubitemid 40039944)
35. A Noda Y Ning SF Venable OM Pereirasmith JR Smith 1994 Cloning of senescent cell-derived inhibitors of DNA-synthesis using an expression screen Exp Cell Res 211 90 98 1:CAS:528:DyaK2cXis1ans7g%3D 10.1006/excr.1994.1063 8125163 (Pubitemid 24167339)
36. J Olivier WD Johnson GD Marshall 2008 The logarithmic transformation and the geometric mean in reporting experimental IgE results: what are they and when and why to use them? Ann Allergy Asthma Immunol 100 333 337 10.1016/S1081-1206(10)60595-9 18450118
37. VH Parker C Stevens 1979 Binding of beryllium to nuclear acidic proteins Chem Biol Interact 26 167 177 1:CAS:528:DyaE1MXlsFahsb4%3D 10.1016/0009-2797(79) 90020-6 455565 (Pubitemid 9233224)
38. DW Parsons S Jones X Zhang JC Lin RJ Leary P Angenendt P Mankoo H Carter IM Siu GL Gallia, et al. 2008 An integrated genomic analysis of human glioblastoma multiforme Science 321 1807 1812 1:CAS:528:DC%2BD1cXhtFCrtLrE 10.1126/science.1164382 18772396
39. O Potapova M Gorospe RH Dougherty NM Dean WA Gaarde NJ Holbrook 2000 Inhibition of c-Jun N-terminal kinase 2 expression suppresses growth and induces apoptosis of human tumor cells in a p53-dependent manner Mol Cell Biol 20 1713 1722 1:CAS:528:DC%2BD3cXhtF2nt7Y%3D 10.1128/MCB.20.5.1713-1722.2000 10669748 (Pubitemid 30100190)
40. DW Seol Q Chen ML Smith R Zarnegar 1999 Regulation of the c-met proto-oncogene promoter by p53 J Biol Chem 274 3565 3572 1:CAS:528: DyaK1MXhtVemsbw%3D 10.1074/jbc.274.6.3565 9920903 (Pubitemid 29077198)
41. JW Shay AF Gazdar 1997 Telomerase in the early detection of cancer J Clin Pathol 50 106 109 1:STN:280:DyaK2szgtVKluw%3D%3D 10.1136/jcp.50.2.106 9155689
42. SY Shieh M Ikeda Y Taya C Prives 1997 DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2 Cell 91 325 334 1:CAS:528: DyaK2sXnt1CltLY%3D 10.1016/S0092-8674(00)80416-X 9363941 (Pubitemid 27467963)
43. GH Stein LF Drullinger A Soulard V Dulic 1999 Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts Mol Cell Biol 19 2109 2117 1:CAS:528:DyaK1MXhsFequrY%3D 10022898
44. FJ Stott S Bates MC James BB McConnell M Starborg S Brookes I Palmero K Ryan E Hara KH Vousden G Peters 1998 The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2 EMBO J 17 5001 5014 1:CAS:528:DyaK1cXmt1CmtLc%3D 10.1093/emboj/17.17.5001 9724636 (Pubitemid 28408466)
45. The Cancer Genome Atlas Research Network 2008 Comprehensive genomic characterization defines human glioblastoma genes and core pathways Nature 455 1061 1068 10.1038/nature07385
46. W Wang H Furneaux H Cheng MC Caldwell D Hutter Y Liu N Holbrook M Gorospe 2000 HuR regulates p21 mRNA stabilization by UV light Mol Cell Biol 20 760 769 1:CAS:528:DC%2BD3cXmt1ShtQ%3D%3D 10.1128/MCB.20.3.760-769.2000 10629032 (Pubitemid 30044212)
47. HO Weber T Samuel P Rauch JO Funk 2002 Human p14(ARF)-mediated cell cycle arrest strictly depends on intact p53 signaling pathways Oncogene 21 3207 3212 1:CAS:528:DC%2BD38XktFGjsro%3D 10.1038/sj.onc.1205429 12082636
48. K Webley JA Bond CJ Jones JP Blaydes A Craig T Hupp D Wynford-Thomas 2000 Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage Mol Cell Biol 20 2803 2808 1:CAS:528:DC%2BD3cXit1ylsr8%3D 10.1128/MCB.20.8.2803-2808.2000 10733583 (Pubitemid 30183499)
49. HP Witschi WN Aldridge 1968 Uptake, distribution and binding of beryllium to organelles of the rat liver cell Biochem J 106 811 820 1:CAS:528: DyaF1cXosFOqtg%3D%3D 5637364
50. Q Zhan F Carrier AJ Fornace Jr 1993 Induction of cellular p53 activity by DNA-damaging agents and growth arrest Mol Cell Biol 13 4242 4250 1:CAS:528:DyaK3sXlvFyltrg%3D 8321226