Two-dimensional gel analysis of apoptosis-specific p53 isoforms induced by 2-methoxyestradiol in human lung cancer cells

Apoptosis

Volumn 3, Issue 6, 1998, Pages 421-430

  Mukhopadhyay, T ^a   Roth, J A ^a   Acosta, S A ^b   Maxwell, S A ^b,c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Apoptosis; Non small cell lung carcinoma; p53; Phosphorylation

Indexed keywords

ADENOVIRIDAE;

EID: 0000775988     PISSN: 13608185     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1009610603068     Document Type: Article

References (62)

1. Tarunina M, Jenkins JR. Human p53 binds DNA as a protein homodimer but monomeric variants retain full transcriptional transactivation. Oncogene 1993; 8: 3165-3173.
2. Vogelstein B, Kinzler KW. p53 function and dysfunction. Cell 1992; 70: 523-526.
3. Finlay CA, Hinds PW, Levine AJ. The p53 proto-oncogene can act as a suppressor of transformation. Cell 1989; 57: 1083-1093.
4. Johnson P, Gray D, Mowat M, Benchimol S. Expression of wild-type p53 is not compatible with continued growth of p53-negative tumor cells. Mol Cell Biol 1991; 11: 1-11.
5. Yonish-Rouach E, Grunwald D, Wilder S, et al. p53-mediated cell death: relationship to cell cycle control. Mol Cell Biol 1993; 13: 1415-1423.
6. Debbas M, White E. Wild-type p53 mediates apoptosis by ElA, which is inhibited by E1B. Genes Develop 1993; 7: 546-554.
7. Merritt AJ, Potten CS, Kemp CJ, et al. The role of p53 in spon7 taneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res 1994; 54: 614-617.
8. Bendori R, Resnitzky D, Kimchi A. Changes in p53 mRNA expression during terminal differentiation of murine erythroleukemia cells. Virology 1987; 161: 607-611.
9. Oren M, Reich NC, Levine AJ. Regulation of the cellular p53 tumor antigen in teratocarcinoma cells and their differentiated progeny. Mol Cell Biol 1983; 2: 443-449.
10. Aloni-Grinstein R, Zan-Bar I, Alboum I, Goldfinger N, Rotter V. Wild type p53 functions as a control protein in the differentiation pathway of the B-cell lineage. Oncogene 1993; 8: 3297-3305.
11. Lane DP. p53, guardian of the genome. Nature 1992; 358: 15-16.
12. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW Participation of p53 protein in the cellular response to DNA damage. Cancer Res 1991; 51: 6304-6311.
13. Zhan Q, Carrier F, Fornace AJ. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol Cell Biol 1993; 13: 4242-4250.
14. Livingstone LR, White A, Sprouse J, Livanos E, Jacks T, Tlsty TD. Altered cell cyce arrest and gene amplification potential accompany loss of wild-type p53. Cell 1992; 70: 923-925.
15. Yin Y, Tainsky MA, Bischoff FZ, Strong LC, Wahl GM. Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 1992; 70: 937-948.
16. Greenblatt MS, Bennett WP, Hollstein M, Harris CC. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res 1994; 54: 4855-4878.
17. Chen P-L, Chen YM, Bookstein R, Lee W-H. Genetic mechanisms of tumor suppression by the human p53 gene. Science 1990; 250: 1576-1580.
18. Fukasawa K, Sakoulas G, Pollack RE, Chen S. Excess wild-type p53 blocks initiation and maintenance of simian virus 40 transformation. Mol Cell Biol 1991; 11: 3472-3483.
19. Eliyahu D, Raz A, Gruss P, Givol D, Oren M. Participation of p53 cellular tumour antigen in transformation of normal embryonic cells. Nature 1984; 312: 646-649.
20. Hinds PW, Finlay CA, Quartin RS, et al. Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the "hot-spot" mutant phenotypes. Cell Growth Diff 1990; 1: 571-580.
21. Shaulsky G, Goldfinger N, Rotter V. Alterations in tumor development in vivo mediated by expression of wild-type or mutant p53 proteins. Cancer Res 1991; 51: 5232-5237.
22. Dittmer D, Pati S, Zambetti G, et al. Gain of function mutations in p53. Nature Genet 1993; 4: 42-45.
23. Selkirk JK, He CY, Patterson RM, Merrick BA. Tumor suppressor p53 gene forms multiple isoforms - evidence for single locus origin and cytoplasmic complex formation with heat shock proteins. Electrophoresis 1996; 17: 1764-1771.
24. Milne DM, Palmer RH, Campbell DG, Meek DW. Phosphorylation of the p53 tumour-suppressor protein at three N-terminal sites by a novel casein kinase I-like enzyme. Oncogene 1992; 7: 1361-1369.
25. Herrmann CP, Kraiss S, Montenarh M. Association of casein kinase II with immunopurified p53. Oncogene 1991; 6: 877-884.
26. Meek DW, Simon S, Kikkawa U, Eckhart W. The p53 tumour suppressor protein is phosphorylated at serine 389 by casein kinase II. EMBO J 1990; 9: 3253-3200.
27. Addison C, Jenkins JR, Sturzbecher HW. The p53 nuclear localisation signal is structurally linked to a p34cdc2 kinase motif. Oncogene 1990; 5: 423-426.
28. Bischoff JR, Friedman PN, Marshak DR, Prives C, Beach D. Human p53 is phosphorylated by p60-cdc2 and cyclin B-cdc2. Proc Natl Acad Sci USA 1990; 87: 4766-4770.
29. Milner J, Cook A, Mason J. p53 is associated with p34cdc2 in transformed cells. EMBO J 1990; 9: 2885-2889.
30. Price BD, Hughes-Davies L, Park SJ. Cdk2 kinase phosphorylates serine 315 of human p53 in vitro. Oncogene 1995; 11: 73-80.
31. Lees-Miller SP, Sakaguchi K, Ullrich SJ, Appella E, Anderson CW. Human DNA-activated protein kinase phosphorylates sennes 15 and 37 in the ammo-terminal transactivation domain of p53. Mol Cell Biol 1992; 12: 5041-5049.
32. Milne DM, Campbell DG, Caudwell FB, Meek DW. Phosphorylation of the tumor suppressor protein p53 by mitogen-activated protein kinases. J Biol Chem 1994; 269: 9253-9260.
33. Milne DM, Campbell LE, Campbell DG, Meek DW. p53 is phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-Jun kinase, JNK1. J Biol Chem 1995; 270: 5511-5518.
34. Baudier J, Delphin C, Grunwald D, Khochbin S, Lawrence JJ. Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc Natl Acad Sci USA 1992; 89: 11627-11631.
35. Takenaka I, Morin F, Seizinger BR, Kley N. Regulation of the sequence-specific DNA binding function of p53 by protein kinase C and protein phosphatases. J Biol Chem 1995; 270: 5405-5411.
36. Jamal S, Ziff EB. Raf phosphorylates p53 in vitro and potentiates p53-dependent transcriptional transactivation in vivo. Oncogene 1995; 10: 2095-2101.
37. Mayr GA, Reed M, Wang P, Wang Y, Schweds JF, Tegtmeyer P. Serine phosphorylation in the NH2 terminus of p53 facilitates transactivation. Cancer Res 1995; 55: 2410-2417.
38. Hecker D, Page G, Lohrum M, Weiland S, Scheidtmann KH. Complex regulation of the DNA-binding activity of p53 by phosphorylation: differential effects of individual phosphorylation sites on the interaction with different binding motifs. Oncogene 1996; 12: 953-961.
39. Hupp TR, Meek DW, Midgley CA, Lane DP. Regulation of the specific DNA binding function of p53. Cell 1992; 71: 875-886.
40. Hao M, Lowy AM, Kapoor M, Deffie A, Liu G, Lozano G. Mutation of phosphoserine 389 affects p53 function in vivo. J Biol Chem 1996; 271: 29380-29385.
41. Lohrum M, Scheidtmann KH. Differential effects of phosphorylation of rat p53 on transactivation of promoters derived from different p53 responsive genes. Oncogene 1996; 13: 2527-2539.
42. Hall SR, Campbell LE, Meek DW. Phosphorylation of p53 at the casein kinase II site selectively regulates p53-dependent transcriptional repression but not transactivation. Nucleic Acids Res 1996; 24: 1119-1126.
43. Yan Y, Shay JW, Wright WE, Mumby MC. Inhibition of protein phosphatase activity induces p53-dependent apoptosis in the absence of p53 transactivation. J Biol Chem 1997; 272: 15220-15226.
44. Mukhopadhyay T, Roth JA. Induction of apoptosis in human lung cancer cells after wild-type p53 activation by methoxyestradiol. Oncogene 1997; 14: 379-384.
45. Maxwell SA, Roth JA, Mukhopadhyay T. Analysis of phosphorylated isoforms of the p53 tumor suppressor protein in human lung carcinoma cells undergoing apoptosis. Electrophoresis 1996; 17: 1772-1775.
46. Takahashi T, Nau MM, Chiba I, et al. p53: a frequent target for genetic abnormalities in lung cancer. Science 1989; 246: 491-494.
47. Maxwell SA, Mukhopadhyay T. Transient stabilization of p53 in non-small cell lung carcinoma cultures arrested for growth by retinoic acid. Exp Cell Res 1994; 214: 67-74.
48. Zhang WW, Fang X, Branch CD, Mazur W, French BA, Roth JA. Generation and indentification of recombinant adenovirus by liposome-mediated transfection and PCR analysis. Biotechniques 1993; 15: 868-872.
49. Maxwell SA, Zhang W-W. Cell type-specific regulation of p53 expression in non-small cell lung carcinoma cells. Oncol Repts 1995; 2: 81-87.
50. Fujiwara T, Grimm EA, Mukhopadhyay T, Zhang WW, Owen-Schaub LB, Roth JA. Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res 1994; 54: 2287-2291.
51. Patterson RM, He C, Selkirk JK, Merrick BA. Human p53 expressed in baculovirus-infected Sf9 cells displays a two-dimensional isoform pattern identical to wild-type p53 from human cells. Arch Biochem Biophys 1996; 330: 71-79.
52. Selkirk JK, He C, Patterson RM, Merrick BA. Tumor suppressor p53 gene forms multiple isoforms: evidence for single locus origin and cytoplasmic complex formation with heat shock proteins. Electrophoresis 1996; 17: 1764-1771.
53. Price BC, Youmell MB. The phosphatidylinositol 3-kinase inhibitor wortmannin sensitizes murine fibroblasts and human tumor cels to radiattion and blocks induction of p53 following DNA damage. Cancer Res 1996; 56: 246-250.
54. Gabai VL, Zamulaeva IV, Mosin AF, et al. Resistance of Ehrlich tumor cells to apoptosis can be due to accumulation of heat shock proteins. FEBS Letts 1995; 375: 21-26.
55. Tishler RB, Lamppu DM, Park S, Price BD. Microtubule-active drugs taxol, vinblastine, and nocodazole increase the levels of transcriptionally active p53. Cancer Res 1995; 55: 6021-6025.
56. Tishler RB, Calderwood SK, Coleman CN, Price BD. Increases in sequence-specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents. Cancer Res 1993; 53: 2212-2216.
57. Tsukidate K, Yamamoto K, Snyder JW, Farber JL. Microtubule antagonists activate programmed cell death (apoptosis) in cultured rat hepatocytes. Am J Path 1993; 143: 918-925.
58. Kessis TD, Slebos RJ, Nelson WG, et al. Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc Natl Acad Sci USA 1993; 90: 3988-3992.
59. TSUJI K, Ogawa K. Recovery from ultraviolet-induced growth arrest of primary rat hepatocytes by p53 antisense oligonucleotide treatment. Mol Carcinogen 1994; 9: 167-174.
60. Maxwell SA. Two-dimensional gel analysis of p53-mediated changes in protein expression. Anticancer Res 1994; 14: 2549-2556.
61. Knippschild U, Milne D, Campbell L, Meek D. p53 N-terminus-targeted protein kinase activity is stimulated in response to wild-type p53 and DNA damage. Oncogene 1996; 13: 1387-1393.
62. Scheidtmann KH, Landsberg G. UV irradiation leads to transient changes in phosphorylation and stability of tumor suppressor protein p53. Int J Oncol 1996; 9: 1277-1285.