Identification of aspirin analogues that repress NF-κB signalling and demonstrate anti-proliferative activity towards colorectal cancer in vitro and in vivo

Oncology Reports

Volumn 32, Issue 4, 2014, Pages 1670-1680

  Claudius, Ann Katrin ^b   Kankipati, Chandra S ^a   Kilari, Rajagopal S ^a   Hassan, Sadiya ^a   Guest, Kerry ^c   Russell, Steven T ^c   Perry, Chris J ^a   Stark, Lesley A ^b   Nicholl, Iain D ^a  

^a UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c ASTON UNIVERSITY   (United Kingdom)

Author keywords

Anti proliferative activity; Cyclin D1; Diaspirin; Fumaryl diaspirin; Implantable colorectal cancer model; NF B; Tumour cell lines

Indexed keywords

2 BROMOBENZOYLSALICYLATE; 4 METHYL BENZOYLSALICYLATE; ACETYLSALICYLIC ACID; ACETYLSALICYLIC ACID DERIVATIVE; DIASPIRIN; DIASPIRIN,BIS(2 CARBOXYPHENYL)SUCCINATE; FUMARYLDIASPIRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOPROPYL (2 BROMOBENZOYLSALICYLATE); METHYL BENZOYLSALICYLATE; PN 508; PN 511; PN 512; PN 517; PN 524; PN 525; PN 528; PN 529; SEBACOYLDIASPIRIN; TEREPHTHALOYLDIASPIRIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; BIS(2,3-DIBROMOSALICYL)FUMARATE; CYCLIN D; NONSTEROID ANTIINFLAMMATORY AGENT; SUCCINYLDISALICYLIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BIOACCUMULATION; CANCER GROWTH; CANCER INHIBITION; CELL PROLIFERATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; DRUG IDENTIFICATION; DRUG STRUCTURE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; TOXICITY TESTING; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; TREATMENT OUTCOME; ADENOCARCINOMA; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; CELL CYCLE; COLORECTAL TUMOR; DRUG EFFECTS; DRUG SCREENING; METABOLISM; NUDE MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADENOCARCINOMA; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; ASPIRIN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYCLIN D; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; MICE; MICE, NUDE; NF-KAPPA B; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84923068523     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2014.3373     Document Type: Article

References (51)

1. Ferlay J, Parkin DM and Steliarova-Foucher E: Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 46: 765-781, 2010.
2. Thun MJ, Namboodiri MM and Heath CW Jr: Aspirin use and reduced risk of fatal colon cancer. N Engl J Med 325: 1593-1596, 1991.
3. Logan RF, Little J, Hawtin PG and Hardcastle JD: Effect of aspirin and non-steroidal anti-inflammatory drugs on colorectal adenomas: case-control study of subjects participating in the Nottingham faecal occult blood screening programme. BMJ 307: 285-289, 1993. (Pubitemid 23220843)
4. Baron JA, Cole BF, Sandler RS, et al: A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 348: 891-899, 2003. (Pubitemid 36297997)
5. Din FV, Theodoratou E, Farrington SM, et al: Effect of aspirin and NSAIDs on risk and survival from colorectal cancer. Gut 59: 1670-1679, 2010.
6. La Vecchia C, Negri E, Franceschi S, et al: Aspirin and colorectal cancer. Br J Cancer 76: 675-677, 1997. (Pubitemid 27354684)
7. Corpet DE and Pierre F: Point: from animal models to prevention of colon cancer. Systematic review of chemoprevention in min mice and choice of the model system. Cancer Epidemiol Biomarkers Prev 12: 391-400, 2003. (Pubitemid 36578475)
8. Liu Y, Ju J, Xiao H, et al: Effects of combination of calcium and aspirin on azoxymethane-induced aberrant crypt foci formation in the colons of mice and rats. Nutr Cancer 60: 660-665, 2008.
9. Bousserouel S, Gosse F, Bouhadjar M, Soler L, Marescaux J and Raul F: Long-term administration of aspirin inhibits tumour formation and triggers anti-neoplastic molecular changes in a pre-clinical model of colon carcinogenesis. Oncol Rep 23: 511-517, 2010.
10. Sansom OJ, Stark LA, Dunlop MG and Clarke AR: Suppression of intestinal and mammary neoplasia by lifetime administration of aspirin in Apc(Min/+) and Apc(Min/+), Msh2(-/-) mice. Cancer Res 61: 7060-7064, 2001. (Pubitemid 32946497)
11. Lal G, Ash C, Hay K, et al: Suppression of intestinal polyps in Msh2-deficient and non-Msh2-deficient multiple intestinal neoplasia mice by a specific cyclooxygenase-2 inhibitor and by a dual cyclooxygenase-1/2 inhibitor. Cancer Res 61: 6131-6136, 2001. (Pubitemid 32762549)
12. Rothwell PM, Fowkes FG, Belch JF, Ogawa H, Warlow CP and Meade TW: Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet 377: 31-41, 2011.
13. Burn J, Gerdes AM, Macrae F, et al: Long-term effect of aspirin on cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2 randomised controlled trial. Lancet 378: 2081-2087, 2011.
14. Rothwell PM, Wilson M, Price JF, Belch JF, Meade TW and Mehta Z: Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet 379: 1591-1601, 2012.
15. Chan AT, Ogino S and Fuchs CS: Aspirin use and survival after diagnosis of colorectal cancer. JAMA 302: 649-658, 2009.
16. Laine L: The gastrointestinal effects of nonselective NSAIDs and COX-2-selective inhibitors. Semin Arthritis Rheum 32: 25-32, 2002.
17. Gasche C, Goel A, Natarajan L and Boland CR: Mesalazine improves replication fidelity in cultured colorectal cells. Cancer Res 65: 3993-3997, 2005. (Pubitemid 40775634)
18. Campregher C, Honeder C, Chung H, Carethers JM and Gasche C: Mesalazine reduces mutations in transforming growth factor β receptor II and activin type II receptor by improvement of replication fidelity in mononucleotide repeats. Clin Cancer Res 16: 1950-1956, 2010.
19. McIlhatton MA, Tyler J, Burkholder S, et al: Nitric oxide-donating aspirin derivatives suppress microsatellite instability in mismatch repair-deficient and hereditary nonpolyposis colorectal cancer cells. Cancer Res 67: 10966-10975, 2007. (Pubitemid 350145926)
20. Tesei A, Zoli W, Fabbri F, et al: NCX 4040, an NO-donating acetylsalicylic acid derivative: efficacy and mechanisms of action in cancer cells. Nitric Oxide 19: 225-236, 2008.
21. Selvendiran K, Bratasz A, Tong L, Ignarro LJ and Kuppusamy P: NCX-4016, a nitro-derivative of aspirin, inhibits EGFR and STAT3 signaling and modulates Bcl-2 proteins in cisplatin-resistant human ovarian cancer cells and xenografts. Cell Cycle 7: 81-88, 2008.
22. Zhao W, Mackenzie GG, Murray OT, Zhang Z and Rigas B: Phosphoaspirin (MDC-43), a novel benzyl ester of aspirin, inhibits the growth of human cancer cell lines more potently than aspirin: a redox-dependent effect. Carcinogenesis 30: 512-519, 2009.
23. Wang D and DuBois RN: Pro-inflammatory prostaglandins and progression of colorectal cancer. Cancer Lett 267: 197-203, 2008.
24. Sheng H, Shao J, Morrow JD, Beauchamp RD and DuBois RN: Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res 58: 362-366, 1998. (Pubitemid 28047080)
25. Harris RE, Beebe-Donk J and Alshafie GA: Similar reductions in the risk of human colon cancer by selective and nonselective cyclooxygenase-2 (COX-2) inhibitors. BMC Cancer 8: 237, 2008.
26. Elwood PC, Gallagher AM, Duthie GG, Mur LA and Morgan G : Aspirin, salicylates, and cancer. Lancet 373: 1301-1309, 2009.
27. Dibra HK, Perry CJ and Nicholl ID: Non-steroidal anti-inflammatory drugs, DNA repair and cancer. In: DNA Repair and Human Health. Vengrova S (ed.). InTech, pp743-776, 2011. http://cdn.intechopen.com/pdfs-wm/22182.pdf.
28. Kopp E and Ghosh S: Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265: 956-959, 1994.
29. Thoms HC, Dunlop MG and Stark LA: p38-mediated inactivation of cyclin D1/cyclin-dependent kinase 4 stimulates nucleolar translocation of RelA and apoptosis in colorectal cancer cells. Cancer Res 67: 1660-1669, 2007. (Pubitemid 46383392)
30. Yu HG, Huang JA, Yang YN, et al: The effects of acetylsalicylic acid on proliferation, apoptosis, and invasion of cyclooxygenase-2 negative colon cancer cells. Eur J Clin Invest 32: 838-846, 2002.
31. Luciani MG, Campregher C and Gasche C: Aspirin blocks proliferation in colon cells by inducing a G1 arrest and apoptosis through activation of the checkpoint kinase ATM. Carcinogenesis 28: 2207-2217, 2007. (Pubitemid 47543383)
32. Shureiqi I, Chen D, Lotan R, et al: 15-Lipoxygenase-1 mediates nonsteroidal anti-inflammatory drug-induced apoptosis independently of cyclooxygenase-2 in colon cancer cells. Cancer Res 60: 6846-6850, 2000. (Pubitemid 32059150)
33. Goel A, Chang DK, Ricciardiello L, Gasche C and Boland CR: A novel mechanism for aspirin-mediated growth inhibition of human colon cancer cells. Clin Cancer Res 9: 383-390, 2003. (Pubitemid 36109756)
34. Pangburn HA, Kraus H, Ahnen DJ and Rice PL: Sulindac metabolites inhibit epidermal growth factor receptor activation and expression. J Carcinog 4: 16, 2005.
35. Pangburn HA, Ahnen DJ and Rice PL: Sulindac metabolites induce proteosomal and lysosomal degradation of the epidermal growth factor receptor. Cancer Prev Res 3: 560-572, 2010.
36. Ruschoff J, Wallinger S, Dietmaier W, et al: Aspirin suppresses the mutator phenotype associated with hereditary nonpolyposis colorectal cancer by genetic selection. Proc Natl Acad Sci USA 95: 11301-11306, 1998. (Pubitemid 28450123)
37. Deb J, Dibra H, Shan S, et al: Activity of aspirin analogues and vanillin in a human colorectal cancer cell line. Oncol Rep 26: 557-565, 2011.
38. Hussey HJ and Tisdale MJ: Effect of polyunsaturated fatty acids on the growth of murine colon adenocarcinomas in vitro and in vivo. Br J Cancer 70: 6-10, 1994. (Pubitemid 24203620)
39. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63, 1983.
40. Carmichael J, DeGraff WG, Gazdar AF, Minna JD and Mitchell J B: Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 47: 936-942, 1987. (Pubitemid 17027905)
41. Stark LA and Dunlop MG: Nucleolar sequestration of RelA (p65) regulates NF-κB-driven transcription and apoptosis. Mol Cell Biol 25: 5985-6004, 2005. (Pubitemid 40946553)
42. Stark LA, Din FV, Zwacka RM and Dunlop MG: Aspirin-induced activation of the NF-κB signaling pathway: a novel mechanism for aspirin-mediated apoptosis in colon cancer cells. FASEB J 15: 1273-1275, 2001.
43. Loveridge CJ, MacDonald AD, Thoms HC, Dunlop MG and Stark LA: The proapoptotic effects of sulindac, sulindac sulfone and indomethacin are mediated by nucleolar translocation of the RelA(p65) subunit of NF-κB. Oncogene 27: 2648-2655, 2008. (Pubitemid 351550873)
44. Campbell KJ, Rocha S and Perkins ND: Active repression of antiapoptotic gene expression by RelA(p65) NF-κB. Mol Cell 13: 853-865, 2004. (Pubitemid 38438480)
45. Walder JA, Zaugg RH, Walder RY, Steele JM and Klotz IM: Diaspirins that cross-link beta chains of hemoglobin: bis(3,5-dibromosalicyl) succinate and bis(3,5-dibromosalicyl) fumarate. Biochemistry 18: 4265-4270, 1979. (Pubitemid 10247831)
46. Alfonso LF, Srivenugopal KS and Bhat GJ : Does aspirin acetylate multiple cellular proteins? (Review). Mol Med Rep 2: 533-537, 2009.
47. Schwenger P, Alpert D, Skolnik EY and Vilcek J: Cell type-specific activation of c-Jun N-terminal kinase by salicylates. J Cell Physiol 179: 109-114, 1999. (Pubitemid 29108931)
48. Kojima M, Morisaki T, Sasaki N, et al: Increased nuclear factor-kB activation in human colorectal carcinoma and its correlation with tumor progression. Anticancer Res 24: 675-681, 2004. (Pubitemid 38625006)
49. Greenspan EJ, Madigan JP, Boardman LA and Rosenberg DW: Ibuprofen inhibits activation of nuclear β-catenin in human colon adenomas and induces the phosphorylation of GSK-β. Cancer Prev Res 4: 161-171, 2011.
50. Thoms HC, Loveridge CJ, Simpson J, et al: Nucleolar targeting of RelA(p65) is regulated by COMMD1-dependent ubiquitination. Cancer Res 70: 139-149, 2010.
51. Meltzer PC, Blundell P, Yong YF, et al: 2-Carbomethoxy-3-aryl-8- bicyclo[3.2.1]octanes: potent non-nitrogen inhibitors of monoamine transporters. J Med Chem 43: 2982-2991, 2000. (Pubitemid 30626757)