Gemcitabine-mediated tumour regression and p53-dependent gene expression: Implications for colon and pancreatic cancer therapy

Cell Death and Disease

Volumn 4, Issue 9, 2013, Pages

  Hill, R ^a,b   Rabb, M ^b   Madureira, P A ^a   Clements, D ^b   Gujar, S A ^b   Waisman, D M ^c   Giacomantonio, C A ^b,c   Lee, P W K ^a,b  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b DALHOUSIE UNIVERSITY   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Apoptosis; Bax; Chromium; Gemcitabine; p53; PUMA

Indexed keywords

CHROMIUM; GEMCITABINE; PROTEIN BAX; PROTEIN P53; PUMA PROTEIN;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER THERAPY; CELL KILLING; COLON CANCER; DNA DAMAGE; DRUG MECHANISM; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; TUMOR REGRESSION;

14-3-3 PROTEINS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CHROMIUM; COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DEOXYCYTIDINE; DNA DAMAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, SCID; MODELS, BIOLOGICAL; PANCREATIC NEOPLASMS; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS; REMISSION INDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84885001092     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.307     Document Type: Article

References (44)

1. Vogelstein B, Kinzler KW. p53 function and dysfunction. Cell 1992; 70: 523-526
2. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55: 5187-5190
3. Wahl GM, Carr AM. The evolution of diverse biological responses to DNA damage: Insights from yeast and p53. Nat Cell Biol 2001; 3: E277-E286
4. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445: 656-660
5. Pietenpol JA, Tokino T, Thiagalingam S, el-Deiry WS, Kinzler KW, Vogelstein B. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc Natl Acad Sci USA 1994; 91: 1998-2002
6. Zupnick A, Prives C. Mutational analysis of the p53 core domain L1 loop. J Biol Chem 2006; 281: 20464-20473
7. Qian H, Wang T, Naumovski L, Lopez CD, Brachmann RK. Groups of p53 target genes involved in specific p53 downstream effects cluster into different classes of DNA binding sites. Oncogene 2002; 21: 7901-7911
8. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7: 683-694
9. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 2003; 100: 1931-1936
10. Chipuk JE, Green DR. Cytoplasmic p53: Bax and forward. Cell Cycle 2004; 3: 429-431
11. Chipuk JE, Green DR. p53's believe it or not: Lessons on transcription-independent death. J Clin Immunol 2003; 23: 355-361
12. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11: 577-590
13. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303: 1010-1014
14. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 2004; 24: 6728-6741
15. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 2004; 6: 443-450
16. Abbruzzese JL. New applications of gemcitabine and future directions in the management of pancreatic cancer. Cancer 2002; 95(4 Suppl): 941-945
17. Macdonald JS. Clinical overview: Adjuvant therapy of gastrointestinal cancer. Cancer Chemother Pharmacol 2004; 54(Suppl 1): S4-11
18. Okusaka T, Ishii H, Funakoshi A, Ueno H, Furuse J, Sumii T. A phase I/II study of combination chemotherapy with gemcitabine and 5-fluorouracil for advanced pancreatic cancer. Jpn J Clin Oncol 2006; 36: 557-563
19. Marsman DS, Barrett JC. Apoptosis and chemical carcinogenesis. Risk Anal 1994; 14: 321-326
20. O'Brien TJ, Fornsaglio JL, Ceryak S, Patierno SR. Effects of hexavalent chromium on the survival and cell cycle distribution of DNA repair-deficient S. cerevisiae. DNA Repair (Amst) 2002; 1: 617-627
21. Salnikow K, Zhitkovich A, Costa M. Analysis of the binding sites of chromium to DNA and protein in vitro and in intact cells. Carcinogenesis 1992; 13: 2341-2346
22. O'Brien TJ, Ceryak S, Patierno SR. Complexities of chromium carcinogenesis: Role of cellular response, repair and recovery mechanisms. Mutat Res 2003; 533: 3-36
23. Laronga C, Yang HY, Neal C, Lee MH. Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J Biol Chem 2000; 275: 23106-23112
24. Hill R, Leidal AM, Madureira PA, Gillis LD, Cochrane HK, Waisman DM et al. Hypersensitivity to chromium-induced DNA damage correlates with constitutive deregulation of upstream p53 kinases in p21-/-HCT116 colon cancer cells. DNA Repair (Amst) 2008; 7: 239-252
25. Javelaud D, Besancon F. Inactivation of p21WAF1 sensitizes cells to apoptosis via an increase of both p14ARF and p53 levels and an alteration of the Bax/Bcl-2 ratio. J Biol Chem 2002; 277: 37949-37954
26. Taylor WR, Stark GR. Regulation of the G2/M transition by p53. Oncogene 2001; 20: 1803-1815
27. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997; 1: 3-11
28. Chan TA, Hermeking H, Lengauer C, Kinzler KW, Vogelstein B. 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 1999; 401: 616-620
29. Hill R, Leidal AM, Madureira PA, Gillis LD, Waisman DM, Chiu A et al. Chromium-mediated apoptosis: Involvement of DNA-dependent protein kinase (DNA-PK) and differential induction of p53 target genes. DNA Repair (Amst) 2008; 7: 1484-1499
30. Hill R, Madureira PA, Waisman DM, Lee PW. DNA-PKCS binding to p53 on the p21WAF1/CIP1 promoter blocks transcription resulting in cell death. Oncotarget 2011; 2: 1094-1108
31. 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(23 Pt 1): 6304-6311
32. Price BD, Youmell MB. The phosphatidylinositol 3-kinase inhibitor wortmannin sensitizes murine fibroblasts and human tumor cells to radiation and blocks induction of p53 following DNA damage. Cancer Res 1996; 56: 246-250
33. Suzuki A, Tsutomi Y, Akahane K, Araki T, Miura M. Resistance to Fas-mediated apoptosis: Activation of caspase 3 is regulated by cell cycle regulator p21WAF1 and IAP gene family ILP. Oncogene 1998; 17: 931-939
34. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253: 49-53
35. Erster S, Slade N, Moll UM. Mutational analysis of p53 in human tumors: Direct DNA sequencing and SSCP. Methods Mol Biol 2003; 234: 219-230
36. Singh J, Carlisle DL, Pritchard DE, Patierno SR. Chromium-induced genotoxicity and apoptosis: Relationship to chromium carcinogenesis (review). Oncol Rep 1998; 5: 1307-1318
37. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL. Doxorubicininduced cardiomyopathy: From molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 2012; 52: 1213-1225
38. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments: What the cardiologist needs to know. Nat Rev Cardiol 2010; 7: 564-575
39. Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S et al. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: A phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 2007; 25: 1960-1966
40. Van CE, Verslype C, Grusenmeyer PA. Lessons learned in the management of advanced pancreatic cancer. J Clin Oncol 2007; 25: 1949-1952
41. Okusaka T, Furuse J, Funakoshi A, Ioka T, Yamao K, Ohkawa S et al. Phase II study of erlotinib plus gemcitabine in Japanese patients with unresectable pancreatic cancer. Cancer Sci 2011; 102: 425-431
42. Kindler HL, Ioka T, Richel DJ, Bennouna J, Letourneau R, Okusaka T et al. Axitinib plus gemcitabine versus placebo plus gemcitabine in patients with advanced pancreatic adenocarcinoma: A double-blind randomised phase 3 study. Lancet Oncol 2011; 12: 256-262
43. Grayson S, Elias PM. Human epidermal proteolipids: Isolation, partial characterization, and subcellular localization. J Invest Dermatol 1988; 90: 185-192
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408