Mutations in exons 5-8 of the p53 gene, independent of their type and location, are associated with increased apoptosis and mitosis in invasive breast carcinoma

Journal of Pathology

Volumn 189, Issue 4, 1999, Pages 504-513

  Van Slooten, Henk Jan ^a   Van De Vijver, Marc J ^a   Børresen, Anne Lise ^b   Eyfjörd, Jorunn E ^c   Valgardsdóttir, Rut ^c   Scherneck, Siegfried ^d   Nesland, Jahn M ^b   Devilee, Peter ^a   Cornelisse, Cees J ^a   Van Dierendonck, Jan Hein ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c ICELANDIC CANCER SOCIETY   (Iceland)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Apoptosis; Bc1 2; Breast cancer; P53; Proliferation

Indexed keywords

PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER GRADING; CANCER GROWTH; CANCER INVASION; CELL PROLIFERATION; DISEASE ASSOCIATION; EXON; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MITOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR NECROSIS;

APOPTOSIS; BREAST NEOPLASMS; CHI-SQUARE DISTRIBUTION; DNA MUTATIONAL ANALYSIS; EXONS; FEMALE; FRAMESHIFT MUTATION; GENE DELETION; GENES, BCL-2; GENES, P53; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MIDDLE AGED; MITOTIC INDEX; MUTATION; MUTATION, MISSENSE;

EID: 0032696081     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9896(199912)189:4<504::AID-PATH483>3.0.CO;2-A     Document Type: Article

References (65)

1. Gottlieb TM, Oren M. P53 in growth control and neoplasia. Biochim Biophys Acta 1996; 1287: 77-102.
2. Ko LJ, Prives C. p53: puzzle and paradigm. Genes Dev 1996; 10: 1054-1072.
3. Linke SP, Clarkin KC, Wahl GM. p53 mediates permanent arrest over multiple cell cycles in response to gamma irradiation. Cancer Res 1997; 57: 1171-1179.
4. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16(ink4a). Cell 1997; 88: 593-602.
5. Symonds H, Krall L, Remington L, et al. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 1994; 78: 703-711.
6. Howes KA, Ransom N, Papermaster DS, Lasudry JG, Albert DM, Windle JJ. Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53 [published erratum appears in Genes Dev 1994; 8:1738]. Genes Dev 1994; 8: 1300-1310.
7. Pan H, Griep AE. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev 1994; 8: 1285-1299.
8. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes [see comments]. Nature 1993; 362: 847-849.
9. Merrill AJ, Potten CS, Kemp CJ, et al. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res 1994; 54: 614-617.
10. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993; 74: 957-967.
11. Fukasawa K, Wiener F, Van de Woude G, Mai S. Genomic instability and apoptosis are frequent in p53-deficient young mice. Oncogene 1997; 15: 1295-1302.
12. Mummenbrauer T, Janus F, Muller B, Wiesmuller L, Deppert W, Grosse F. p53 protein exhibits 3′- to 5′-exonuclease activity. Cell 1996; 85: 1089-1099.
13. Schwartz D, Almog N, Peled A, Goldfinger N, Rotter V. Role of wild type p53 in the G2 phase: regulation of the gamma-irradiation-induced delay and DNA repair. Oncogene 1997; 15: 2597-2607.
14. Sugrue MM, Shin DY, Lee SW, Aaronson SA. Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc Natl Acad Sci USA 1997; 94: 9648-9653.
15. Almog N, Rotter V. Involvement of p53 in cell differentiation and development. Biochim Biophys Acta 1997; 1333: F1-F27.
16. Sabbatini P, Lin J, Levine AJ, White E. Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev 1995; 9: 2184-2192.
17. Attardi LD, Lowe SW, Brugarolas J, Jacks T. Transcriptional activation by p53, but not induction of the p21 gene, is essential for oncogene-mediated apoptosis. EMBO J 1996; 15: 3693-3701.
18. Amundson SA, Myers TG, Fornace AJ Jr. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 1998; 17: 3287-3299.
19. Haldar S, Negrini M, Monne M, Sabbioni S, Croce CM. Down-regulation of bcl-2 by p53 in breast cancer cells. Cancer Res 1994; 54: 2095-2097.
20. Selvakumaran M, Lin HK, Miyashita T, et al. Immediate early up-regulation of bax expression by p53 but not TGF beta 1: a paradigm for distinct apoptotic pathways. Oncogene 1994; 9: 1791-1798.
21. Cunningham JM, Ingle JN, Jung SH, et al. p53 gene expression in node-positive breast cancer: relationship to DNA ploidy and prognosis. J Natl Cancer Inst. 1994; 86: 1871-1873.
22. Allred DC, Clark GM, Elledge R, et al. Association of p53 protein expression with tumor cell proliferation rate and clinical outcome in node-negative breast cancer. J Natl Cancer Inst 1993; 85: 200-206.
23. Clahsen PC, Van de Velde CJH, Duval C, et al. p53 expression and response to chemotherapy in premenopausal node-negative women with early breast cancer. J Clin Oncol 1998; 16: 470-479.
24. Bergh J, Norberg T, Sjogren S, Lindgren A, Holmberg L. Complete sequencing of the p53 gene provides prognostic information in breast cancer patients, particularly in relation to adjuvant systemic therapy and radiotherapy. Nature Med 1995; 1: 1029-1034.
25. Hainaut P, Soussi T, Shomer B, et al. Database of p53 gene somatic mutations in human tumors and cell lines: updated compilation and future prospects. Nucleic Acids Res 1997; 25: 151-157.
26. Kern SE, Kinzler KW, Baker SJ, et al. Mutant p53 proteins bind DNA abnormally in vitro. Oncogene 1991; 6: 131-136.
27. Cho Y, Gorina S, Jeffrey PD, Pavletich NP. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations [see comments]. Science 1994; 265: 346-355.
28. Srinivasan R, Maxwell SA. A cellular protein activates the sequence-specific DNA-binding of p53 by interacting with the central conserved region. Oncogene 1996; 12: 193-200.
29. Gorina S, Pavletich NP. Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2 [see comments]. Science 1996; 274: 1001-1005.
30. Naumovski L, Cleary ML. The p53-binding protein 53BP2 also interacts with Bcl2 and impedes cell cycle progression at G2/M. Mol Cell Biol 1996; 16: 3884-3892.
31. Børresen A, Andersen TI, Eyfjörd JE, et al. TP53 mutations and breast cancer prognosis: particularly poor survival rates for cases with mutations in the zinc-binding domains. Genes Chromosomes Cancer 1996; 14: 71-75.
32. Aas T, Børresen AL, Geisler S, et al. Specific P53 mutations are associated with de now resistance to doxorubicin in breast cancer patients. Nature Med 1996; 2: 811-814.
33. Berns EMJJ, van Staveren IL, Look MP, Smid M, Klijn JGM, Foekens JA. Mutations in residues of TP53 that directly contact DNA predict poor outcome in human primary breast cancer. Br J Cancer 1998; 77: 1130-1136.
34. Andersen TI, Holm R, Nesland JM, Heimdal KR, Ottestad L, Børresen AL. Prognostic significance of TP53 alterations in breast carcinoma. Br J Cancer 1993; 68: 540-548.
35. Thorlacius S, Børresen AL, Eyfjörd JE. Somatic p53 mutations in human breast carcinomas in an Icelandic population: a prognostic factor. Cancer Res 1993; 53: 1637-1641.
36. van Slooten H, van de Vijver MJ, Van de Velde CJH, Van Dierendonck J. Loss of Bcl-2 in invasive breast cancer is associated with high rates of cell death, but also with increased proliferative activity. Br J Cancer 1998; 77: 789-796.
37. Negoescu A, Lorimier P, Labat Moleur F, et al. In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. J Histochem Cytochem 1996; 44: 959-968.
38. Moll UM, Chumas J. Morphologic effects of neoadjuvant chemotherapy in locally advanced breast cancer. Pathol Res Practice 1997; 193: 187-196.
39. van Slooten H, Clahsen PC, van Dierendonck JH. el al. Expression of Bcl-2 in node-negative breast cancer is associated with various prognostic factors, but does not predict response to one course of perioperative chemotherapy. Br J Cancer 1996; 74: 78-85.
40. Vojtesek B, Bartek J, Midgley CA, Lane DP. An immunochemical analysis of the human nuclear phosphoprotein p53. New monoclonal antibodies and epitope mapping using recombinant p53. J Immunol Methods 1992; 151: 237-244.
41. Chen X, Ko LJ, Jayaraman L, Prives C. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev 1996; 10: 2438-2451.
42. Ronen D, Schwartz D, Teitz Y, Goldfinger N, Rotter V. Induction of HL-60 cells to undergo apoptosis is determined by high levels of wild-type p53 protein whereas differentiation of the cells is mediated by lower p53 levels. Cell Growth Differ 1996; 7: 21-30.
43. Thor AD, Moore DH II, Edgerton SM, et al. Accumulation of p53 tumor suppressor gene protein: an independent marker of prognosis in breast cancers. J Natl Cancer Inst 1992; 84: 845-855.
44. Silvestrini R, Benini E, Veneroni S, et al. p53 and bcl-2 expression correlates with clinical outcome in a series of node-positive breast cancer patients. J Clin Oncol 1996; 14: 1604-1610.
45. Kucera E, Speiser P, Gnant M, et al. Prognostic significance of mutations in the p53 gene, particularly in the zinc-binding domains, in lymph node- and steroid receptor positive breast cancer patients. Eur J Cancer 1999; 35: 398-405.
46. Naik P, Karrim J, Hanahan D. The rise and fall of apoptosis during multistage tumorigenesis: down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev 1996; 10: 2105-2116.
47. Fazeli A, Steen RG, Dickinson SL, et al. Effects of p53 mutations on apoptosis in mouse intestinal and human colonic adenomas. Proc Natl Acad Sci USA 1997; 94: 10 199-10 204.
48. Elson A, Deng C, Campos Torres J, Donehower LA, Leder P. The MMTV/c-myc transgene and p53 null alleles collaborate to induce T-cell lymphomas, but not mammary carcinomas in transgenic mice. Oncogene 1995; 11: 181-190.
49. Hundley JE, Koester SK, Troyer DA, Hilsenbeck SG, Subler MA, Windle JJ. Increased tumor proliferation and genomic instability without decreased apoptosis in MMTV/ras mice deficient in p53. Mol Cell Biol 1997; 17: 723-731.
50. Hsu B, Marin MC, el Naggar AK, Stephens LC, Brisbay S, McDonnell TJ. Evidence that c-myc mediated apoptosis does not require wild-type p53 during lymphomagenesis. Oncogene 1995; 11: 175-179.
51. Li B, Rosen JM, McMenamin Balano J, Muller WJ, Perkins AS. Neu/ ERBB2 cooperates with p53-172H during mammary tumorigenesis in transgenic mice. Mol Cell Biol 1997; 17: 3155-3163.
52. Donehower LA, Godley LA. Aldaz CM. et al. Deficiency of p53 accelerates mammary tumorigenesis in Wnt-1 transgenic mice and promotes chromosomal instability. Genes Dev 1995; 9: 882-895.
53. Bodis S, Siziopikou KP, Schnitt SJ, Harris JR, Fisher DE. Extensive apoptosis in ductal carcinoma in situ of the breast. Cancer 1996; 77: 1831-1835.
54. Du M, Singh N, Husseuin A, Isaacson PG, Pan L. Positive correlation between apoptotic and proliferative indices in gastrointestinal lymphomas of mucosa-associated lymphoid tissue (MALT). J Pathol 1996; 178: 379-384.
55. Aihara M, Scardino PT, Truong LD, et al. The frequency of apoptosis correlates with the prognosis of Gleason grade 3 adenocarcinoma of the prostate. Cancer 1995; 75: 522-529.
56. Isacson C, Kessis TD, Hedrick L, Cho KR. Both cell proliferation and apoptosis increase with lesion grade in cervical neoplasia but do not correlate with human papillomavirus type. Cancer Res 1996; 56: 669-674.
57. Shoji Y, Saegusa M, Takano Y, Ohbu M, Okayasu I. Correlation of apoptosis with tumour cell differentiation, progression, and HPV infection in cervical carcinoma. J Clin Pathol 1996; 49: 134-138.
58. Koshida Y, Saegusa M, Okayasu I. Apoptosis, cell proliferation and expression of Bcl-2 and Bax in gastric carcinomas: immunohistochemical and clinicopathological study. Br J Cancer 1997; 75: 367-373.
59. Lipponen PK, Aaltomaa S. Apoptosis in bladder cancer as related to standard prognostic factors and prognosis. J Pathol 1994; 173: 333-339.
60. Hundley JE, Koester SK, Troyer DA, Hilsenbeck SG, Barrington RE, Windle JJ. Differential regulation of cell cycle characteristics and apoptosis in mmtv myc and mmtv ras mouse mammary tumors. Cancer Res 1997; 57: 600-603.
61. Chiou S-K, Rao L, White E. Bcl-2 blocks p53-dependent apoptosis. Mol Cell Biol 1994; 14: 2556-2563.
62. Lin Y, Benchimol S. p53-mediated cell cycle arrest and apoptosis. Leukemia 1997; 11: 324-326.
63. Miyashita T, Harigai M, Hanada M, Reed JC. Identification of a p53-dependent negative response element in the Bcl-2 gene. Cancer Res 1994; 54: 3131-3135.
64. Miyashita T, Krajewski S, Krajewska M. et al. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 1994; 9: 1799-1805.
65. Nowell PC. The clonal evolution of tumor cell populations. Science 1976; 194: 23-28.