Aspirin inhibits camptothecin-induced p21CIP1 levels and potentiates apoptosis in human breast cancer cells

International Journal of Oncology

Volumn 34, Issue 3, 2009, Pages 597-608

  Alfonso, Lloyd F ^a   Srivenugopal, Kalkunte S ^a   Arumugam, Thiruma V ^a   Abbruscato, Thomas J ^a   Weidanz, Jon A ^a   Bhat, G Jayarama ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Apoptosis; Aspirin; Breast cancer; Chemoprevention; Chemotherapy; Gene expression

Indexed keywords

ACETYLSALICYLIC ACID; CAMPTOTHECIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; MESSENGER RNA; PROTEIN BAX;

ACETYLATION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL NUCLEUS; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION;

ACETYLATION; ANTINEOPLASTIC AGENTS; APOPTOSIS; ASPIRIN; BCL-2-ASSOCIATED X PROTEIN; BREAST NEOPLASMS; CAMPTOTHECIN; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA, NEOPLASM; DRUG SYNERGISM; HUMANS; RNA, MESSENGER; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 64549161198     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000185     Document Type: Article

References (70)

1. Vane JR: The fight against rheumatism: from willow bark to COX-1 sparing drugs. J Physiol Pharmacol 51: 573-586, 2000.
2. Vane JR and Botting RM: The mechanism of action of aspirin. Thrombosis Res 110: 255-258, 2003.
3. Vane JR: Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nature New Biology 231: 232-235, 1971.
4. Ferreira SH, Moncada S and Vane JR: Indomethacin and aspirin abolish prostaglandin release from spleen. Nature 231: 237-239, 1971.
5. Thun MJ, Henley SJ and Patrono C: Non-steroidal anti-inflammatory drugs as anti-cancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 94: 252-266, 2002.
6. Rao CV and Reddy BS: NSAIDs and chemoprevention. Curr Cancer Drug Targets 4: 29-42, 2004.
7. Schiff SJ, Shivaprasad P and Santini DL: Cyclooxygenase inhibitors: drugs for cancer prevention. Curr Opin Pharmacol 3: 352-361, 2003.
8. Moyad MA: An introduction to aspirin, NSAIDs and COX-2 inhibitors for the primary prevention of cardiovascular events and cancer and their potential preventive role in bladder carcinogenesis: part II. Semin Urol Oncol 19: 306-316, 2001.
9. Gupta RA and Dubois RN: Aspirin, NSAIDs and colon cancer prevention. Gastroenterology 114: 1095-1098, 1998.
10. Baron JA, Cole BF, Sandler RS, Haile RW, Ahnen D, Bresalier R, McKeown-Eyssen G, Summers RW, Rothstein R, Burke CA, Snover DC, Church TR, Allen JI, Beach M, Bech CJ, Bond JH, Byers T, Greenberg ER, Mandal JS, Marcon N, Mott LA, Pearson L, Saibil F and van Stolk RU: A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 348: 891-899, 2003.
11. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Curhan GC and Fuchs CS: Long-term use of aspirin and nonsteroidal anti-inflammatory drugs and risk of colorectal cancer. JAMA 294: 914-923, 2005.
12. Harris RE, Beebe-Donk J, Doss H and Burr Doss D: Aspirin, ibuprofen, and other non-steroidal anti-inflammatory drugs in cancer prevention: a critical review of non-selective COX-2 blockade. Oncol Rep 13: 559-583, 2005.
13. Leshno M, Moshkowitz M and Arber N: Aspirin is clinically effective in chemoprevention of colorectal neoplasia: point. Cancer Epidemiol Biomarkers Prev 17: 1558-1561, 2008.
14. Sawaoka H, Tsuji M, Gunawan ES, Sasaki Y, Kawano S and Hori M: Cyclooxygenase inhibitors suppress angiogenesis and reduce tumor growth in vivo. Lab Invest 79: 1469-1477, 1999.
15. Addelrahim M and Safe S: Cyclooxygenase-2 inhibitors decrease vascular endothelial growth factor expression in colon cancer cells by enhanced degradation of Sp1 and Sp4 proteins. Mol Pharamacol 68: 317-329, 2005.
16. Zhou XM, Wong BC, Fan XM, Zhang HB, Lin MC, Kung HF, Fan DM and Lam SK: Non-steroidal anti-inflammatory drugs induce apoptosis in gastric cancer cells through up-regulation of bax and bak. Carcinogenesis 22: 1393-1397, 2001.
17. Gu Q, Wang JD, Xia HH, Lin MC, He H, Zou B, Tu SP, Yang Y, Liu XG, Lam SK, Wong WM, Chan AOO, Yuen MF, Kung HF and Wong BCY: Activation of the capsase-8/Bid and Bax pathways in aspirin-induced apoptosis in gastric cancer. Carcinogenesis 26: 541-546, 2005.
18. Gao J, Niwa K, Sun W, Takemura M, Lian Z, Onogi K, Seishima M, Mori H and Tamaya T: Non-steroidal anti-inflammatory drugs inhibit cellular proliferation and upregulate cyclooxygenase-2 protein expression in endometrial cancer cells. Cancer Sci 95: 901-907, 2004.
19. Zhang L, Yu J, Park BH, Kinzler KW and Vegelstein B: Role of Bax in the apoptotic response to anti-cancer drugs. Science 290: 989-992, 2000.
20. Pique M, Barragan M, Dalmau M, Bellosillo B, Pons G and Gil J: Aspirin induces apoptosis through mitochondrial cytochrome c release. FEBS Lett 480: 193-196, 2000.
21. Bellosillo B, Pique M, Barragan M, Castano E, Villamor N, Colomer D, Montserrat E, Pons G and Gil J: Aspirin and salicylate induce apoptosis and activation of capsases in B-cell chronic lymphocytic leukemia cells. Blood 92: 1406-1414, 1998.
22. Zimmerman KC, Waterhouse NJ, Goldstein JC, Schuler M and Green DR: Aspirin induces apoptosis through release of cytocrome c from mitochondria. Neoplasia 2: 505-513, 2000.
23. Dikshit P, Chatterjee M, Goswami A, Mishra A and Jana NR: Aspirin induces apoptosis through the inhibition of proteosome function. J Biol Chem 281: 29228-29235, 2006.
24. Ho C-C, Yang XW, Lee T-L, Liao P-H, Yang S-H, Tsai C-H and Chou M-Y: Activation of p53 signaling in acetyl salicylic acid-induced apoptosis in OC2 human oral cancer cells. Eur J Clin Invest 33: 875-882, 2003.
25. Chan TA, Morin PJ, Vogelstein B and Kinzler KW: Mechanisms underlying non-steroidal anti-inflammatory drug-mediated apoptosis. Proc Natl Acad Sci USA 95: 681-686, 1998.
26. Roth GJ, Machuga ET and Ozols J: Isolation and covalent structure of the aspirin-modified, active-site region of prostaglandin synthetase. Biochemistry 22: 4672-4675, 1983.
27. DeWitt DL, el-Harith EA, Kraemer SA, Andrews MJ, Yao EF, Armstrong RL and Smith WL: The aspirin and heme binding sites of ovine and murine prostaglandin endoperoxide synthases. J Biol Chem 265: 5192-5198, 1990.
28. Zhang X, Morham SG, Langenbach R and Young DA: Malignant transformation and anti-neoplastic actions of nonsteroidal anti-inflammatory drugs (NSAIDs) on cyclooxygenasenull embryo fibroblasts. J Exp Med 190: 451-459, 1999.
29. Hanif R, Pittas A, Feng Y, Koutsos MI, Qiao L, Staiano-Coico L, Shiff SI and Rigas B: Effects of nonsteroidal anti-inflammatory drugs on proliferation and on apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol 52: 237-245, 1996.
30. Pincard RN, Hawkins D and Farr RS: In vitro acetylation of plasma proteins, enzymes and DNA by aspirin. Nature 219: 68-69, 1968.
31. Gartel AL and Tyner AL: The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Therapeutics 1: 639-649, 2002.
32. Harris SL and Levine AJ: The p53 pathway: positive and negative feed back loops. Oncogene 24: 2899-2908, 2005.
33. Slee EA, O'Conner DJ and Lu X: To die or not to die: how does p53 decide. Oncogene 23: 2809-2818, 2004.
34. Bode AM and Dong Z: Post-translational modification of p53 in tumorigenesis. Nature 4: 793-805, 2004.
35. Gu W and Roeder RG: Activation of P53 sequence specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90: 595-606, 1997.
36. Krishna SB, Alfonso LF, Thekkumkara TJ, Abbruscato TJ and Bhat GJ: Angiotensin II induces phosphorylation of glucose regulated protein-75 in WB rat liver cells. Arch Biochem Biophys 457: 16-28, 2007.
37. Miyashita T and Reed JC: Tumor suppressor p53 is a direct transactivator of the human bax gene. Cell 80: 293-299, 1995.
38. Bhat GJ, Thekkumkara TJ, Thomas WG, Conrad KM and Baker KM: Angiotensin II stimulates sis-inducing factor-like DNA binding activity. J Biol Chem 269: 31443-31449, 1994.
39. Gunaje JJ and Bhat GJ: Distinct mechanisms of inhibition of interleukin-6-induced Stat3 signaling by TGF-beta and alpha-thrombin in CCL39 cells. Mol Cell Biol Res Commun 4: 151-157, 2000.
40. Levin DS, Bai W, Yao N, O'Donnell M and Tomkinson AE: An interaction between DNA ligase I and proliferating cell nuclear antigen: implications for okazaki fragment synthesis and joining. Proc Natl Acad Sci USA 94: 12863-12868, 1997.
41. Vikis HG and Guan KL: Glutathione-S-transferase-fusion based assays for studying protein-protein interactions. Methods Mol Biol 261: 175-186, 2004.
42. Moridani MY: Biochemical basis of 4-hydroxyanisole induced cell toxicity towards B16-F0 melanoma cells. Cancer Lett 243: 235-245, 2006.
43. Franken NAP, Rodermond HM, Stap J, Haveman J and Bree C: Clonogenic assay of cells in vitro. Nature Protocols 1: 2315-2319, 2006.
44. Munshi A, Hobbs M and Meyn RE: Clonogenic cell survival assay. Methods Mol Med 110: 21-28, 2005.
45. Luo J, Li M, Tang Y, Laszkowska M, Roeder RG and Gu W: Acetylation of p53 augments its site specific DNA binding both in vitro and in vivo. Proc Natl Acad Sci USA 101: 2259-2264, 2004.
46. Roberts MS, Rumble RH, Wanwimolruk S, Thomas D and Brooks PM: Pharmacokinetics of aspirin and salicylate in elderly subjects and in patients with alcoholic liver disease. Eur J Clin Pharmacol 25: 253-261, 1983.
47. Zhang R, Li Y, Cai Q, Liu T, Sun H and Chambless B: Preclinical pharmacology of the natural prodict anticancer agent 10-hydroxycamptothecin, an inhibitor of topoisomerase I. Cancer Chemother Pharmacol 41: 257-267, 1998.
48. Han Z, Wei W, Dunaway S, Darnowski JW, Calabresi P, Sedivy J, Hendrickson EA, Balan KV, Pantazis P and Wyche JH: Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin. J Biol Chem 277: 17154-17160, 2002.
49. ARF and p53 levels and an alteration of the Bax/Blc-2 ratio. J Biol Chem 277: 37949-37954, 2002.
50. Waldman T, Lengauer C, Wang X, Seth P, Capogrossi MC and Holbrook NJ: Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381: 713-716, 1997.
51. CIP1 can protect human carcinoma cells against p53-dependent and p53-independent apoptosis induced by natural chemopreventive and therapeutic agents. Oncogene 20: 3387-3398, 2001.
52. WAF1 in human malignant mesothelioma. Clin Cancer Res 14: 5099-5107, 2008.
53. Mangiapane S, Blettner M and Schlattmann P: Aspirin use and breast cancer risk:a meta-analysis and meta-regression of observational studies from 2001-2005. Pharmacoepidemiol Drug Saf 17: 115-124, 2007.
54. Harris RE, Chlebowski RT, Jackson RD, Frid DJ, Ascenseo JL, Anderson G, Loar A, Rodabough RJ, White E and McTiernan A: Breast cancer and nonsteroidal anti-inflammatory drugs: prospective results from women's health initiative. Cancer Res 63: 6096-6101, 2003.
55. McCormick DL, Madigan MJ and Moon RC: Modulation of rat mammary carcinogenesis by indomethacin. Cancer Res 45: 1803-1808, 1985.
56. Johnson TW, Anderson KE, Lazovich D and Folsom A: Association of aspirin and nonsteroidal anti-inflammatory drug use with breast cancer. Cancer Epidemiol Biomarkers Prev 11: 1586-1591, 2002.
57. DuBois RN: Aspirin and breast cancer prevention the estrogen connection. JAMA 291: 2488-2489, 2008.
58. Kopp E and Ghosh S: Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265: 956-959, 1994.
59. McCarty MF and Block KI: Preadministration of high dose salicylates. Supressors of NF-κB activation may increase the chemosensitivity of many cancers: An example of proapoptotic signal modulation therapy. Integr Cancer Ther 5: 252-268, 2006.
60. Hui L, Zheng Y, Yan Y, Bargonetti J and Foster DA: Mutant p53 in MDA-MB-231 breast cancer cells is stabilized by elevated phospholipase D activity and contributes to survival signals generated by phospholipase D. Oncogene 25: 7305-7310, 2006.
61. O'Connor PM, Jackman J, Bae I, Myers T, Fan S, Mutoh M, Scudiero D, Monks A, Weinstein JN, Friend S, Fornace A and Kohn KW: Characterization of the p53 tumor suppressor pathway in cell lines of the national cancer institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer drugs. Cancer Res 57: 4285-4300, 1997.
62. Mody M, Dharker N, Bloomston M, Wang P, Chou F, Glickman TS, McCaffrey T, Yang Z, Pumfrey A, Lee D, Ringel MD and Pinzone JJ: Rosiglitazone sensitizes MDA-MB-231 breast cancer cell to anti-tumor eefcts of tumor necrosis factor-a, CH11 and CYC202. Endocr Relat Cancer 14: 305-315, 2007.
63. Campomenosi P, Monti P, Aprile A, Abbondandolo A, Frebourg T, Gold B, Crook T, Inga A, Resnick MA, Iggo R and Fronza G: p53 mutants can often transactivate promoters containing a p21 but not Bax or PIG3 responsive elements. Oncogene 20: 3573-3579, 2001.
64. Ludwig RL, Bates S and Vousden KH: Differential activation of target cellular promoters by p53 mutants with impaired apoptotic function. Mol Cell Biol 16: 4952-4960, 1996.
65. Lee DH and Goldberg HL: Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8: 397-403, 1998.
66. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M and Green DR: Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014, 2004.
67. Qiao L, Hanif R, Sphicas E, Shiff SJ and Rigas B: Effect of aspirin on induction of apoptosis in HT-29 human colon adenocarcinoma cells. Biochem Pharmacol 55: 53-64, 1998.
68. Luciani MG, Campregher C and Gasche C: Aspirin blocks proliferation in colon cells by inducing G1 arrest and apoptosis through activation of the checkpoint kinase ATM. Carcinogenesis 28: 2207-2217, 2007.
69. Lu M, Strohecker A, Chen F, Kwan T, Bosman J, Jordan VC and Cryns VL: Aspirin sensitizes cancer cells to TRAIL-induced apoptosis by reducing survivin levels. Clin Cancer Res 14: 3168-3176, 2008.
70. Sandler RS: Aspirin should not be promoted for colon cancer prevention. Cancer Epidemiol Biomarkers Prev 17: 1562-1563, 2008.