DNA-damaging agents induce both p53-dependent and p53-independent apoptosis in immature thymocytes

Molecular Pharmacology

Volumn 50, Issue 4, 1996, Pages 900-911

  Macfarlane, Marion ^a,c   Jones, Neil A ^b   Dive, Caroline ^b   Cohen, Gerald M ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; ETOPOSIDE; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MATURATION; CYTOPATHOGENIC EFFECT; DNA STRAND BREAKAGE; DRUG EFFECT; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL DIVISION; DEXAMETHASONE; DNA; DNA DAMAGE; ETOPOSIDE; GAMMA RAYS; MALE; MICE; MOLECULAR SEQUENCE DATA; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, INBRED F344; T-LYMPHOCYTES; THYMUS GLAND; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0029860159     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Kerr, J. F. R., A. H. Wyllie, and A. R. Currie. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239-245 (1972).
2. Wyllie, A. H., R. G. Morris, A. L. Smith, and D. Dunlop. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142:67-77 (1984).
3. Arends, M. J., R. G. Morris, and A. H. Wyllie. Apoptosis: the role of the endonuclease. Am. J. Pathol. 136:593-608 (1990).
4. Arends, M. J., and A. H. Wyllie. Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32:223-254 (1991).
5. Ellis, R. E., J. Yuan, and H. R. Horvitz. Mechanisms and functions of cell death. Annu. Rev. Cell. Biol. 7:663-698 (1991).
6. Cohen, J. J., R. C. Duke, V. A. Fadok, and K. S. Sellins. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293 (1992).
7. Wyllie, A. H., J. F. R. Kerr, and A. R. Currie. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306 (1980).
8. Wyllie, A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature (Lond.) 284:555-556 (1980).
9. Walker, P. R., C. Smith, T. Youdale, J. Leblanc, J. F. Whitfield, and M. Sikorska. Topoisomerase II-reactive chemotherapeutic drugs induce apoptosis in thymocytes. Cancer Res. 51:1078-1085 (1991).
10. Brown, D. G., X.-M. Sun, and G. M. Cohen. Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J. Biol. Chem. 268:3037-3039 (1993).
11. Oberhammer, F., J. W. Wilson, C. Dive, I. D. Morris, J. A. Hickman, A. E. Wakeling, P. R. Walker, and M. Sikorska. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J. 12:3679-3684 (1993).
12. Cohen, G. M., X. M. Sun, H. O. Fearnhead, M. MacFarlane, D, G. Brown, R. T. Snowden, and D. Dinsdale. Formation of large molecular weight fragments of DNA is a key committed step of apoptosis in thymocytes. J. Immunol. 153:507-516 (1994).
13. Cohen, J. J., and R. C. Duke. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132:38-42 (1984).
14. Wyllie, A. H., and R. G. Morris. Hormone-induced cell death: purification and properties of thymocytes undergoing apoptosis after glucocorticoid treatment. Am. J. Pathol. 109:78-87 (1982).
15. Sellins, K. S., and J. J. Cohen. Gene induction by γ-irradiation leads to DNA fragmentation in lymphocytes. J. Immunol. 39:3199-3206 (1987).
16. Smith, C. A., G. T. Williams, R. Kingston, E. J. Jenkinson, and J. J. T. Owen. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature (Lond.) 337:181-184 (1989).
17. Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C Hancock. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128 (1992).
18. Evans, C. A., P. J. Owen-Lynch, A. D. Whetton, and C. Dive. Activation of the Abelson tyrosine kinase activity is associated with suppression of apoptosis in hemopoietic cells. Cancer Res. 53:1735-1738 (1993).
19. Rao, L., M. Debbas, P. Sabbatini, D. Hockenbery, S. Korsmeyer, and E. White. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89: 7742-7746 (1992).
20. Hockenbery, D., G. Nun̄ez, C. Milliman, R. D. Schreiber, and S. J. Korsmeyer. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond.) 348:334-336 (1990).
21. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature (Lond.) 352:345-347 (1991).
22. Finlay, C. A., P. W. Hinds, and A. J. Levine. The p53 proto-oncogene can act as a suppressor of transformation. Cell 57:1083-1093 (1989).
23. Lane, D. P. A death in the life of p53. Nature (Lond.) 358:15-16 (1992).
24. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311 (1991).
25. Lowe, S. W., H. E. Ruley, T. Jacks, and D. E. Housman. p53-Dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957-967 (1993).
26. Clarke, A. R., C. A. Purdie, D. J. Harrison, R. G. Morris, C. C. Bird, M. L. Hooper, and A. H. Wyllie. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature (Lond.) 362:849-852 (1993).
27. Harper, J. W., G. M. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816 (1993).
28. 1 arrest and apoptosis. Cancer Res. 54:1169-1174 (1994).
29. Baker, S. J., S. Markowitz, E. R. Fearon, J. K. V. Wilson, and B. Vogelstein. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science (Washington D. C.) 249:912-915 (1990).
30. Shaw, P., R. Bovey, S. Tardy, R. Sahli, B. Sordat, and J. Costa. Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc. Natl. Acad. Sci. USA 89:4495-4499 (1992).
31. Lowe, S. W., E. M. Schmitt, S. W. Smith, B. A. Osborne, and T. Jacks. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature (Lond.) 362:847-849 (1993).
32. Fearnhead, H. O., M. Chwalinski, R. T. Snowden, M. G. Ormerod, and G. M. Cohen. Dexamethasone and etoposide induce apoptosis in rat thymocytes from different phases of the cell cycle. Biochem. Pharmacol. 48:1073-1079 (1994).
33. Bruno, S., P. Lassota, W. Giaretti, and Z. Darzynkiewicz. Apoptosis of rat thymocytes triggered by prednisolone, camptothecin, or teniposide is selective to G0 cells and is prevented by inhibitors of proteases. Oncol. Res. 4:29-35 (1992).
34. Cohen, G. M., X.-M. Sun, R. T. Snowden, M. G. Ormerod, and D. Dinsdale. Identification of a transitional preapoptotic population of thymocytes. J. Immunol. 151:566-574 (1993).
35. Sun, X.-M., R. T. Snowden, D. N. Skilleter, D. Dinsdale, M. G. Ormerod, and G. M. Cohen. A flow cytometric method for the separation and quantitation of normal and apoptotic thymocytes. Anal. Biochem. 204:351-356 (1992).
36. Hudson L., and F. C. Hay. Practical Immunology. Blackwell Scientific Publications, London (1980).
37. Kemp, C. J., L. A. Donehower, A. Bradley, and A. Balmain. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumours. Cell 74:813-822 (1993).
38. Paterson, D. J., J. R. Green, W. A. Jefferies, M. Puklavec, and A. F. Williams. The MRC OX-44 antigen marks a functionally relevant subset among rat thymocytes. J. Exp. Med. 166:1-13 (1987).
39. Sorenson, C. M., M. A. Barry, and A. Eastman. Analysis of events associated with cell cycle arrest at G2 phase and cell death induced by cisplatin. J. Natl. Cancer Inst. 82:749-755 (1990).
40. Harlow, E., and D. Lane. Antibodies: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, NY (1988).
41. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 227:680-685 (1970).
42. Ormerod, M. G., X.-M. Sun, R. T. Snowden, R. Davies, H. Fearnhead, and G. M. Cohen. Increased membrane permeability of apoptotic thymocytes: a flow cytometric study. Cytometry 14:595-602 (1993).
43. Ullrich, S. J., W. E. Mercer, and E. Appella. Human wild-type p53 adopts a unique conformational and phosphorylation state in vivo during growth arrest of glioblastoma cells. Oncogene 7:1635-1643 (1992).
44. Gannon, J. V., R. Greaves, R. Iggo, and D. Lane. Activating mutations in p53 produce a common conformational effect: a monoclonal antibody specific for the mutant form. EMBO J. 9:1595-1602 (1990).
45. Miyashita, T., and J. C Reed. Tumour suppressor p53 is a direct transcriptional activator of the human box gene. Cell 80:293-299 (1995).
46. Veis, D. J., C. L. Sentman, E. A. Bach, and S. J. Korsmeyer. Expression of the Bcl-2 protein in murine and human thymocytes and in peripheral T lymphocytes. J. Immunol. 151:2546-2554 (1993).
47. Oltvai, Z. N., C. L. Milliman, and S. J. Korsmeyer. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619 (1993).
48. Selvakumaran, M., H.-S. Lin, T. Miyashita, H. G. Wang, S. Krajewski, J. C. Reed, B. Hoffman, and D. Liebermann. Immediate up-regulation of box expression by p53 but not TGF 66 1: a paradigm for distinct apoptotic pathways. Oncogene 9:1791-1798 (1994).
49. Zhan, Q., S. Fan, I. Bae, C. Guillof, D. A. Liebermann, P. M. O'Connor, and A. J. Fornace, Jr. Induction of box by genotoxic stress in human cells correlates with normal p53 status. Oncogene 9:3743-3751 (1994).
50. Tamura, T., M. Ishihara, M. S. Lamphier, N. Tanaka, I. Oishi, S. Aizawa, T. Matsuyama, T. W. Mak, S, Taki, and T. Tanaguchi. An IRF-1-dependent pathway of DNA damage-induced apoptosis in mitogen-activated T lymphocytes. Nature (Lond.) 376:596-599 (1995).
51. Krajewski, S., M. Krajewski, A., Shabaik, T. Miyashita, H. G. Wang, and J. C. Reed. Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1323-1336 (1994).
52. Allday, M. J., A. Sinclair, G. Parker, D. H. Crawford, and P. J. Farrell. Epstein-Barr virus immortalizes human B cells without neutralizing the functions the function of p53. EMBO. J. 14:1382-1391 (1995).
53. Knudson, C. M., K. S. K. Tung, W. G. Tourtellotte, G. A. J. Brown, and S. J. Korsmeyer. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science (Washington D. C.) 270:96-98 (1995).
54. Strasser, A., A. W. Harris, T. Jacks, and S. Cory. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79:329-339 (1994).
55. Tanaka, N., M. Ishihara, M. Kitagawa, H. Harada, T. Kimura, T. Matsuyama, M. S. Lamphier, S. Aizawa, T. W. Mak, and T. Taniguchi. Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1. Cell 77:829-839 (1994).
56. Snedecor, G. W., and W. G. Cochran. Statistical Methods. Iowa State University Press, Ames (1980).