Mechanisms of the antitumoural effects of aspirin in the gastrointestinal tract

Best Practice and Research: Clinical Gastroenterology

Volumn 26, Issue 4, 2012, Pages e1-

  Bruno, Annalisa ^a,b   Dovizio, Melania ^a,b   Tacconelli, Stefania ^a,b   Patrignani, Paola ^a,b  

^a UNIVERSITY OF CHIETI   (Italy)

^b Center of Excellence on Aging (CeSI)   (Italy)

Author keywords

Aspirin; Cyclooxygenase; Platelets; Tumourigenesis

Indexed keywords

ACETYLSALICYLIC ACID; CYCLOOXYGENASE 1; PLACEBO;

ANTINEOPLASTIC ACTIVITY; CARCINOGENESIS; COLORECTAL CARCINOMA; DRUG BLOOD LEVEL; DRUG HALF LIFE; EPITHELIUM CELL; GASTROINTESTINAL TUMOR; HUMAN; NONHUMAN; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; STROMA CELL; THROMBOCYTE ACTIVATION;

EID: 84870450832     PISSN: 15216918     EISSN: 15321916     Source Type: Journal    
DOI: 10.1016/j.bpg.2012.10.001     Document Type: Article

References (87)

1. P.M. Rothwell, F.G. Fowkes, J.F. Belch, H. Ogawa, C.P. Warlow, and T.W. Meade Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials Lancet 377 2011 31 41
2. M.J. Thun, S.J. Henley, and C. Patrono Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues J Natl Cancer Inst 94 2002 252 266
3. C. Patrono, L.A. García Rodríguez, R. Landolfi, and C. Baigent Low-dose aspirin for the prevention of atherothrombosis N Engl J Med 353 2005 2373 2383
4. C. Baigent Antithrombotic Trialists' Collaboration Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high-risk patients BMJ 324 2002 71 86
5. T. Grosser, S. Fries, and G.A. FitzGerald Biological basis for the cardiovascular consequences of COX-2 inhibition: therapeutic challenges and opportunities J Clin Invest 116 2006 4 15
6. D.G. Menter, J.M. Onoda, D. Moilanen, B.F. Sloane, J.D. Taylor, and K.V. Honn Inhibition by prostacyclin of the tumor cell-induced platelet release reaction and platelet aggregation J Natl Cancer Inst 78 1987 961 969
7. J. Cuzick, F. Otto, J.A. Baron, P.H. Brown, J. Burn, and P. Greenwald Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement Lancet Oncol 10 2009 501 507
8. E. Giovannucci, K.M. Egan, D.J. Hunter, M.J. Stampfer, G.A. Colditz, and W.C. Willett Aspirin and the risk of colorectal cancer in women N Engl J Med 333 1995 609 614
9. P.H. Gann, J.E. Manson, R.J. Glynn, J.E. Buring, and C.H. Hennekens Low-dose aspirin and incidence of colorectal tumors in a randomized trial J Natl Cancer Inst 85 1993 1220 1224
10. N.R. Cook, I.M. Lee, J.M. Gaziano, D. Gordon, P.M. Ridker, and J.E. Manson Low-dose aspirin in the primary prevention of cancer: the Women's Health Study: a randomized controlled trial JAMA 294 2005 47 55
11. J.A. Baron, B.F. Cole, R.S. Sandler, R.W. Haile, D. Ahnen, and R. Bresalier A randomized trial of aspirin to prevent colorectal adenomas N Engl J Med 348 2003 891 899
12. R.S. Sandler, S. Halabi, J.A. Baron, S. Budinger, E. Paskett, and R. Keresztes A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer N Engl J Med 348 2003 883 890
13. R. Benamouzig, J. Deyra, A. Martin, B. Girard, E. Jullian, and B. Piednoir Daily soluble aspirin and prevention of colorectal adenoma recurrence: one-year results of the APACC trial Gastroenterology 125 2003 328 336
14. R. Benamouzig, B. Uzzan, J. Deyra, A. Martin, B. Girard, and J. Little Prevention by daily soluble aspirin of colorectal adenoma recurrence: 4-year results of the APACC randomised trial Gut 61 2012 255 261
15. R.F. Logan, M.J. Grainge, V.C. Shepherd, N.C. Armitage, K.R. Muir ukCAP Trial Group Aspirin and folic acid for the prevention of recurrent colorectal adenomas Gastroenterology 134 2008 29 38
16. J. Burn, D.T. Bishop, P.D. Chapman, F. Elliott, L. Bertario, and M.G. Dunlop A randomized placebo-controlled prevention trial of aspirin and/or resistant starch in young people with familial adenomatous polyposis Cancer Prev Res 4 5 2011 655 665
17. J. Burn, A.M. Gerdes, F. Macrae, J.P. Mecklin, G. Moeslein, and S. Olschwang Long-term effect of aspirin on cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2 randomised controlled trial Lancet 378 2011 2081 2087
18. A.T. Chan Aspirin and familial adenomatous polyposis: coming full circle Cancer Prev Res 4 5 2011 623 627
19. P.M. Rothwell, M. Wilson, C.E. Elwin, B. Norrving, A. Algra, and C.P. Warlow Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials Lancet 376 2010 1741 1750
20. T.W. Meade, and The Medical Research Council's General Practice Research Framework Thrombosis prevention trial: randomised trial of low-intensity oral anticoagulation with warfarin and low-dose aspirin in the primary prevention of ischaemic heart disease in men at increased risk Lancet 351 1998 233 241
21. W.N. Charman, S.A. Charman, D.C. Monkhouse, S.E. Frisbee, E.A. Lockhart, and S. Weisman Biopharmaceutical characterisation of a low-dose (75 mg) controlled-release aspirin formulation Br J Clin Pharmacol 36 1993 470 473
22. R.J. Clarke, G. Mayo, P. Price, and G.A. FitzGerald Suppression of thromboxane A2 but not of systemic prostacyclin by controlled-release aspirin N Engl J Med 325 1991 1137 1141
23. K. Kawakami, J. Brabender, R.V. Lord, S. Groshen, B.D. Greenwald, and M.J. Krasna Hypermethylated APC DNA in plasma and prognosis of patients with esophageal adenocarcinoma J Natl Cancer Inst 92 2000 1805 1811
24. T. Tsuchiya, G. Tamura, K. Sato, Y. Endoh, K. Sakata, and Z. Jin Distinct methylation patterns of two APC gene promoters in normal and cancerous gastric epithelium Oncogene 19 2000 3642 3646
25. G.A. FitzGerald COX-2 and beyond: approaches to prostaglandin inhibition in human disease Nat Rev Drug Discov 2 2003 879 890
26. C. Patrono, P. Patrignani, and L.A. García Rodríguez Cyclooxygenase-selective inhibition of prostanoid formation: transducing biochemical selectivity into clinical read-outs J Clin Invest 108 2001 7 13
27. E.M. Smyth, T. Grosser, M. Wang, Y. Yu, and G.A. FitzGerald Prostanoids in health and disease J Lipid Res 50 2009 S423 S428
28. C.D. Funk Prostaglandins and leukotrienes: advances in eicosanoid biology Science 294 2001 1871 1875
29. W.L. Smith, D.L. DeWitt, and R.M. Garavito Cyclooxygenases: structural, cellular, and molecular biology Annu Rev Biochem 69 2000 145 182
30. M.L. Capone, S. Tacconelli, L. Di Francesco, A. Sacchetti, M.G. Sciulli, and P. Patrignani Pharmacodynamic of cyclooxygenase inhibitors in humans Prostaglandins Other Lipid Mediat 82 2007 85 94
31. S. McClelland, M. Gawaz, E. Kennerknecht, C.S. Konrad, S. Sauer, and K. Schuerzinger Contribution of cyclooxygenase-1 to thromboxane formation, platelet-vessel wall interactions and atherosclerosis in the ApoE null mouse Atherosclerosis 202 2009 84 91
32. P.C. Chulada, M.B. Thompson, J.F. Mahler, C.M. Doyle, B.W. Gaul, and C. Lee Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice Cancer Res 60 2000 4705 4708
33. T. Daikoku, D. Wang, S. Tranguch, J.D. Morrow, S. Orsulic, and R.N. DuBois Cyclooxygenase-1 is a potential target for prevention and treatment of ovarian epithelial cancer Cancer Res 65 2005 3735 3744
34. F.A. Fitzpatrick Cyclooxygenase enzymes: regulation and function Curr Pharm Des 10 2004 577 588
35. J.N. Topper, J. Cai, D. Falb, and M.A. Gimbrone Jr. Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress PNAS 93 1996 10417 10422
36. L. Di Francesco, L. Totani, M. Dovizio, A. Piccoli, A. Di Francesco, and T. Salvatore Induction of prostacyclin by steady laminar shear stress suppresses tumor necrosis factor-alpha biosynthesis via heme oxygenase-1 in human endothelial cells Circ Res 104 2009 506 513
37. D. Wang, and R.N. Dubois Eicosanoids and cancer Nat Rev Cancer 10 2000 181 193
38. H. Sheng, J. Shao, S.C. Kirkland, P. Isakson, R.J. Coffey, and J. Morrow Inhibition of human colon cancer cell growth by selective inhibition of cyclooxygenase-2 J Clin Invest 99 1997 2254 2259
39. H. Sheng, J. Shao, J.D. Morrow, R.D. Beauchamp, and R.N. DuBois Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells Cancer Res 58 1998 362 366
40. H. Sheng, J. Shao, M.K. Washington, and R.N. DuBois Prostaglandin E2 increases growth and motility of colorectal carcinoma cells J Biol Chem 276 2001 18075 18081
41. Y. Sun, X.M. Tang, E. Half, M.T. Kuo, and F.A. Sinicrope Cyclooxygenase-2 overexpression reduces apoptotic susceptibility by inhibiting the cytochrome c-dependent apoptotic pathway in human colon cancer cells Cancer Res 62 2002 6323 6328
42. C. Yuan, C.J. Rieke, G. Rimon, B.A. Wingerd, and W.L. Smith Partnering between monomers of cyclooxygenase-2 homodimers Proc Natl Acad Sci U S A 103 2006 6142 6147
43. C. Yuan, R.S. Sidhu, D.V. Kuklev, Y. Kado, M. Wada, and I. Song Cyclooxygenase allosterism, fatty acid-mediated cross-talk between monomers of cyclooxygenase homodimers J Biol Chem 284 2009 10046 10055
44. C. Patrono, C. Baigent, J. Hirsh, G. Roth American College of Chest Physicians Antiplatelet drugs: American College of Chest Physicians evidence-based clinical practice guidelines (8th edition) Chest 133 2008 199S 233S
45. M. Lecomte, O. Laneuville, C. Ji, D.L. DeWitt, and W.L. Smith Acetylation of human prostaglandin endoperoxide synthase-2 (cyclooxygenase-2) by aspirin J Biol Chem 269 1994 13207 13215
46. N.P. Sharma, L. Dong, C. Yuan, K.R. Noon, and W.L. Smith Asymmetric acetylation of the cyclooxygenase-2 homodimer by aspirin and its effects on the oxygenation of arachidonic, eicosapentaenoic, and docosahexaenoic acids Mol Pharmacol 77 2010 979 986
47. D.W. Gilroy The role of aspirin-triggered lipoxins in the mechanism of action of aspirin Prostaglandins Leukot Essent Fatty Acids 73 2005 203 210
48. C.N. Serhan Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution Prostaglandins Leukot Essent Fatty Acids 73 2005 141 162
49. M. Romano Lipid mediators: lipoxin and aspirin-triggered 15-epi-lipoxins Inflamm Allergy Drug Targets 5 2006 81 90
50. V. Evangelista, S. Manarini, A. Di Santo, M.L. Capone, E. Ricciotti, and L. Di Francesco De novo synthesis of cyclooxygenase-1 counteracts the suppression of platelet thromboxane biosynthesis by aspirin Circ Res 98 2006 593 595
51. P. Patrignani, P. Filabozzi, and C. Patrono Selective cumulative inhibition of platelet thromboxane production by low-dose aspirin in healthy subjects J Clin Invest 69 1982 1366 1372
52. M. Dovizio, A. Bruno, S. Tacconelli, and P. Patrignani Mode of action of aspirin as a chemopreventive agent Recent Results Cancer Res 191 2012 39 65
53. C. Patrono, G. Ciabattoni, E. Pinca, F. Pugliese, G. Castrucci, and A. De Salvo Low dose aspirin and inhibition of thromboxane B2 production in healthy subjects Thromb Res 17 1980 317 327
54. K. Iwamoto, M. Takei, and J. Watanabe Gastrointestinal and hepatic first-pass metabolism of aspirin in rats J Pharm Pharmacol 34 1982 176 180
55. A. Hatori, A. Shigematsu, and A. Tsuya The metabolism of aspirin in rats; localisation, absorption, distribution and excretion Eur J Drug Metab Pharmacokinet 9 1984 205 214
56. P. Minuz, L. Fumagalli, S. Gaino, R.M. Tommasoli, M. Degan, and C. Cavallini Rapid stimulation of tyrosine phosphorylation signals downstream of G-protein-coupled receptors for thromboxane A2 in human platelets Biochem J 400 2006 127 134
57. M.L. Capone, S. Tacconelli, L. Garcia Rodriguez, and P. Patrignani NSAIDs and cardiovascular disease: transducing human pharmacology results into clinical read-outs in the general population Pharmacol Rep 62 2010 530 535
58. L.A. García Rodríguez, S. Tacconelli, and P. Patrignani Role of dose potency in the prediction of risk of myocardial infarction associated with nonsteroidal anti-inflammatory drugs in the general population J Am Coll Cardiol 52 2008 1628 1636
59. M.L. Capone, S. Tacconelli, M.G. Sciulli, M. Grana, E. Ricciotti, and P. Minuz Clinical pharmacology of platelet, monocyte, and vascular cyclooxygenase inhibition by naproxen and low-dose aspirin in healthy subjects Circulation 109 2004 1468 1471
60. P. Anzellotti, M.L. Capone, A. Jeyam, S. Tacconelli, A. Bruno, and P. Tontodonati Low-dose naproxen interferes with the antiplatelet effects of aspirin in healthy subjects: recommendations to minimize the functional consequences Arthritis Rheum 63 2011 850 859
61. G.A. FitzGerald, J.A. Oates, J. Hawiger, R.L. Maas, L.J. Roberts 2nd, and J.A. Lawson Endogenous biosynthesis of prostacyclin and thromboxane and platelet function during chronic administration of aspirin in man J Clin Invest 71 1983 676 688
62. L.A. García Rodríguez, S. Hernández-Díaz, and F.J. de Abajo Association between aspirin and upper gastrointestinal complications: systematic review of epidemiologic studies Br J Clin Pharmacol 52 2001 563 571
63. L.A. García Rodríguez, K.J. Lin, S. Hernández- Díaz, and S. Johansson Risk of upper gastrointestinal bleeding with low-dose acetylsalicylic acid alone and in combination with clopidogrel and other medications Circulation 123 2011 1108 1115
64. C. Sostres, and A. Lanas Gastrointestinal effects of aspirin Nat Rev Gastroenterol Hepatol 8 2011 385 394
65. L.J. Gay, and B. Felding-Habermann Contribution of platelets to tumour metastasis Nat Rev Cancer 11 2011 123 134
66. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, and S. Johansson Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int J Cancer 113 2005 752 760
67. J.E. Italiano Jr., J.L. Richardson, S. Patel-Hett, E. Battinelli, A. Zaslavsky, and S. Short Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released Blood 111 2008 1227 1233
68. D.A. Dixon, N.D. Tolley, K. Bemis-Standoli, M.L. Martinez, A.S. Weyrich, and J.D. Morrow Expression of COX-2 in platelet-monocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signaling J Clin Invest 116 2006 2727 2738
69. S.F. Mause, and C. Weber Microparticles: protagonists of a novel communication network for intercellular information exchange Circ Res 107 2010 1047 1057
70. H.G. Zhang, and W.E. Grizzle Exosomes and cancer: a newly described pathway of immune suppression Clin Cancer Res 17 2011 959 964
71. D.D. Taylor, and C. Gercel-Taylor MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer Gynecol Oncol 110 2008 13 21
72. P. Pradono, R. Tazawa, M. Maemondo, M. Tanaka, K. Usui, and Y. Saijo Gene transfer of thromboxane A(2) synthase and prostaglandin I(2) synthase antithetically altered tumor angiogenesis and tumor growth Cancer Res 62 2002 63 66
73. K. Honn Inhibition of tumor cell metastasis by modulation of the vascular prostacyclin/thromboxane A2 system Clin Exp Metastasis 1 1983 103 114
74. G.A. FitzGerald, A.K. Pedersen, and C. Patrono Analysis of prostacyclin and thromboxane biosynthesis in cardiovascular disease Circulation 67 1983 1174 1177
75. M. Dovizio, S. Tacconelli, E. Ricciotti, A. Bruno, T.J. Maier, and P. Anzellotti Effects of celecoxib on prostanoid biosynthesis and circulating angiogenesis proteins in familial adenomatous polyposis J Pharmacol Exp Ther 341 2012 242 250
76. F. Catella, and G.A. FitzGerald Paired analysis of urinary thromboxane B2 metabolites in humans Thromb Res 47 1987 647 656
77. M.G. Sciulli, P. Filabozzi, S. Tacconelli, R. Padovano, E. Ricciotti, and M.L. Capone Platelet activation in patients with colorectal cancer Prostaglandins Leukot Essent Fatty Acids 72 2005 79 83
78. A.R. Moser, C. Luongo, K.A. Gould, M.K. McNeley, A.R. Shoemaker, and W.F. Dove ApcMin: a mouse model for intestinal and mammary tumorigenesis Eur J Cancer 31A 1995 1061 1064
79. J.A. Coppinger, R. O'Connor, K. Wynne, M. Flanagan, M. Sullivan, and P.B. Maguire Moderation of the platelet releasate response by aspirin Blood 109 2007 4786 4792
80. D. Hanahan, and J. Folkman Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis Cell 86 1996 353 364
81. W. Jiang, S. Hiscox, K. Matsumoto, and T. Nakamura Hepatocyte growth factor/scatter factor, its molecular, cellular and clinical implications in cancer Crit Rev Oncol Hematol 29 1999 209 248
82. M.M. Bertagnolli, C.J. Eagle, A.G. Zauber, M. Redston, S.D. Solomon, and K. Kim Celecoxib for the prevention of sporadic colorectal adenomas N Engl J Med 355 2006 873 884
83. G. Steinbach, P.M. Lynch, R.K. Phillips, M.H. Wallace, E. Hawk, and G.B. Gordon The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis N Engl J Med 342 2000 1946 1952
84. M. Oshima, J.E. Dinchuk, S.L. Kargman, H. Oshima, B. Hancock, and E. Kwong Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2) Cell 87 5 1996 803 809
85. R. Hanif, A. Pittas, Y. Feng, M.I. Koutsos, L. Qiao, and L. Staiano-Coico Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway Biochem Pharmacol 52 1996 237 245
86. C.L. Bos, L.L. Kodach, G.R. van den Brink, S.H. Diks, M.M. van Santen, and D.J. Richel Effect of aspirin on the Wnt/beta-catenin pathway is mediated via protein phosphatase 2A Oncogene 25 2006 6447 6456
87. N.R. Jana NSAIDs and apoptosis Cell Mol Life Sci 65 2008 1295 1301