Aspirin-induced chemoprevention and response kinetics are enhanced by PIK3CA mutations in colorectal cancer cells

Cancer Prevention Research

Volumn 10, Issue 3, 2017, Pages 208-218

  Zumwalt, Timothy J ^a   Wodarz, Dominik ^b   Komarova, Natalia L ^b   Toden, Shusuke ^a   Turner, Jacob ^c   Cardenas, Jacob ^c   Burn, John ^d   Chan, Andrew T ^e   Boland, C Richard ^a   Goel, Ajay ^a  

^a BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ATM PROTEIN; BETA ACTIN; CYCLINE; K RAS PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE CATALYTIC SUBUNIT ALPHA; PROTEIN; PROTEIN KINASE B; RB1 PROTEIN; UNCLASSIFIED DRUG; CYCLOOXYGENASE 2 INHIBITOR; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PIK3CA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER PREVENTION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; COLORECTAL CANCER; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; GENE MUTATION; HUMAN; HUMAN CELL; MALE; MATHEMATICAL MODEL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; GENETICS; KINETICS; MUTATION; NUDE MOUSE; THEORETICAL MODEL; TUMOR CELL LINE;

ANIMALS; ASPIRIN; CELL LINE, TUMOR; CELL PROLIFERATION; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; COLORECTAL NEOPLASMS; CYCLOOXYGENASE 2 INHIBITORS; HUMANS; KINETICS; MALE; MICE; MICE, NUDE; MODELS, THEORETICAL; MUTATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85017361433     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-16-0175     Document Type: Article

References (54)

1. Ng K, Meyerhardt JA, Chan AT, Sato K, Chan JA, Niedzwiecki D, et al. Aspirin and COX-2 inhibitor use in patients with stage III colon cancer. J Natl Cancer Inst 2015; 107: 345.
2. Din FV, Theodoratou E, Farrington SM, Tenesa A, Barnetson RA, Cetnarskyj R, et al. Effect of aspirin and NSAIDs on risk and survival from colorectal cancer. Gut 2010; 59: 1670-9.
3. Baron JA, Cole BF, Sandler RS, Haile RW, Ahnen D, Bresalier R, et al. A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 2003; 348: 891-9.
4. Rothwell PM, Fowkes FG, Belch JF, Ogawa H, Warlow CP, Meade TW. Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet 2011; 377: 31-41.
5. Rothwell PM, Wilson M, Elwin CE, Norrving B, Algra A, Warlow CP, et al. Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials. Lancet 2010; 376: 1741-50.
6. Sandler RS, Halabi S, Baron JA, Budinger S, Paskett E, Keresztes R, et al. A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. N Engl J Med 2003; 348: 883-90.
7. Rothwell PM, Wilson M, Price JF, Belch JF, Meade TW, Mehta Z. Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet 2012; 379: 1591-601.
8. Bastiaannet E, Sampieri K, Dekkers OM, de Craen AJ, van Herk-Sukel MP, Lemmens V, et al. Use of aspirin postdiagnosis improves survival for colon cancer patients. Br J Cancer 2012; 106: 1564-70.
9. Chan AT, Ogino S, Fuchs CS. Aspirin use and survival after diagnosis of colorectal cancer. JAMA 2009; 302: 649-58.
10. Reimers MS, Bastiaannet E, van Herk-Sukel MP, Lemmens VE, van den Broek CB, van de Velde CJ, et al. Aspirin use after diagnosis improves survival in older adults with colon cancer: a retrospective cohort study. JAm Geriatr Soc 2012; 60: 2232-6.
11. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487: 330-7.
12. Burn J, Gerdes AM, Macrae F, Mecklin JP, Moeslein G, Olschwang S, 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 2011; 378: 2081-7.
13. Burn J, Bishop DT, Mecklin JP, Macrae F, Moslein G, Olschwang S, et al. Effect of aspirin or resistant starch on colorectal neoplasia in the Lynch syndrome. N Engl J Med 2008; 359: 2567-78.
14. Hadac JN, Leystra AA, Paul Olson TJ, Maher ME, Payne SN, Yueh AE, et al. Colon tumors with the simultaneous induction of driver mutations in APC, KRAS, and PIK3CA still progress through the adenoma-to-carcinoma sequence. Cancer Prev Res 2015; 8: 952-61.
15. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-67.
16. Pino MS, Chung DC. The chromosomal instability pathway in colon cancer. Gastroenterology 2010; 138: 2059-72.
17. Boland CR, Sato J, Appelman HD, Bresalier RS, Feinberg AP. Microallelotyping defines the sequence and tempo of allelic losses at tumour suppressor gene loci during colorectal cancer progression. Nat Med 1995; 1: 902-9.
18. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology 2010; 138: 2073-87 e3.
19. Goel A, Boland CR. Epigenetics of colorectal cancer. Gastroenterology 2012; 143: 1442-60 e1.
20. Liao X, Lochhead P, Nishihara R, Morikawa T, Kuchiba A, Yamauchi M, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med 2012; 367: 1596-606.
21. Gayet J, Zhou XP, Duval A, Rolland S, Hoang JM, Cottu P, et al. Extensive characterization of genetic alterations in a series of human colorectal cancer cell lines. Oncogene 2001; 20: 5025-32.
22. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483: 603-7.
23. AhmedD, Eide PW, Eilertsen IA, Danielsen SA, Eknaes M, HektoenM, et al. Epigenetic and genetic features of 24 colon cancer cell lines. Oncogenesis 2013; 2: e71.
24. Haugen AC, Goel A, Yamada K, Marra G, Nguyen TP, Nagasaka T, et al. Genetic instability caused by loss of MutS homologue 3 in human colorectal cancer. Cancer Res 2008; 68: 8465-72.
25. Poon IK, Chiu YH, Armstrong AJ, Kinchen JM, Juncadella IJ, Bayliss DA, et al. Unexpected link between an antibiotic, pannexin channels and apoptosis. Nature 2014; 507: 329-34.
26. Marshall OJ. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 2004; 20: 2471-2.
27. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The human genome browser at UCSC. Genome Res 2002; 12: 996-1006.
28. Davis S, Meltzer PS. GEOquery: a bridge between the gene expression omnibus (GEO) and BioConductor. Bioinformatics 2007; 23: 1846-7.
29. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008; 24: 1547-8.
30. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004; 304: 554.
31. Guanti G, Resta N, Simone C, Cariola F, Demma I, Fiorente P, et al. Involvement of PTEN mutations in the genetic pathways of colorectal cancerogenesis. Hum Mol Genet 2000; 9: 283-7.
32. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3, 4, 5-trisphosphate. J Biol Chem 1998; 273: 13375-8.
33. Medico E, Russo M, Picco G, Cancelliere C, Valtorta E, Corti G, et al. The molecular landscape of colorectal cancer cell lines unveils clinically actionable kinase targets. Nat Commun 2015; 6: 7002.
34. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 1999; 27: 29-34.
35. Savitsky K, Bar-Shira A, Gilad S, RotmanG, Ziv Y, Vanagaite L, et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 1995; 268: 1749-53.
36. Kiyomitsu T, Obuse C, Yanagida M. Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1. Dev Cell 2007; 13: 663-76.
37. Cato MH, Chintalapati SK, Yau IW, Omori SA, Rickert RC. Cyclin D3 is selectively required for proliferative expansion of germinal center B cells. Mol Cell Biol 2011; 31: 127-37.
38. Wu L, Timmers C, Maiti B, Saavedra HI, Sang L, Chong GT, et al. The E2F1-3 transcription factors are essential for cellular proliferation. Nature 2001; 414: 457-62.
39. Mathews MB, Bernstein RM, Franza BRJr., Garrels JI. Identity of the proliferating cell nuclear antigen and cyclin. Nature 1984; 309: 374-6.
40. Mihara K, Cao XR, Yen A, Chandler S, Driscoll B, Murphree AL, et al. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product. Science 1989; 246: 1300-3.
41. Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, et al. Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 2000; 408: 381-6.
42. Yin H, Xu H, Zhao Y, Yang W, Cheng J, Zhou Y. Cyclooxygenase-independent effects of aspirin on HT-29 human colon cancer cells, revealed by oligonucleotide microarrays. Biotechnol Lett 2006; 28: 1263-70.
43. NanH, Hutter CM, Lin Y, Jacobs EJ, Ulrich CM, White E, et al. Association of aspirin and NSAID use with risk of colorectal cancer according to genetic variants. JAMA 2015; 313: 1133-42.
44. Jehan Z, Bavi P, Sultana M, Abubaker J, Bu R, Hussain A, et al. Frequent PIK3CA gene amplification and its clinical significance in colorectal cancer. J Pathol 2009; 219: 337-46.
45. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 1998; 93: 705-16.
46. Tougeron D, Sha D, Manthravadi S, Sinicrope FA. Aspirin and colorectal cancer: back to the future. Clin Cancer Res 2014; 20: 1087-94.
47. Chan AT, Ogino S, Fuchs CS. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med 2007; 356: 2131-42.
48. Pachman LM, Olufs R, Procknal JA, Levy G. Pharmacokinetic monitoring of salicylate therapy in children with juvenile rheumatoid arthritis. Arthritis Rheum 1979; 22: 826-31.
49. Gao J, Kashfi K, Liu X, Rigas B. NO-donating aspirin induces phase II enzymes in vitro and in vivo. Carcinogenesis 2006; 27: 803-10.
50. Levy G, Tsuchiya T. Salicylate accumulation kinetics in man. N Engl J Med 1972; 287: 430-2.
51. Gao M, Kong Q, Hua H, Yin Y, Wang J, Luo T, et al. AMPK-mediated upregulation of mTORC2 and MCL-1 compromises the anti-cancer effects of aspirin. Oncotarget 2016; 7: 16349-61.
52. Jung YR, Kim EJ, Choi HJ, Park JJ, KimHS, Lee YJ, et al. Aspirin Targets SIRT1 and AMPK to induce senescence of colorectal carcinoma cells. Mol Pharmacol 2015; 88: 708-19.
53. Moon CM, Kwon JH, Kim JS, Oh SH, Jin Lee K, Park JJ, et al. Nonsteroidal anti-inflammatory drugs suppress cancer stem cells via inhibiting PTGS2 (cyclooxygenase 2) and NOTCH/HES1 and activating PPARG in colorectal cancer. Int J Cancer 2014; 134: 519-29.
54. Goel A, Chang DK, Ricciardiello L, Gasche C, Boland CR. A novel mechanismfor aspirin-mediated growth inhibition of human colon cancer cells. Clin Cancer Res 2003; 9: 383-90.