Cyclin A2 and CDK2 as novel targets of aspirin and salicylic acid: A potential role in cancer prevention

Molecular Cancer Research

Volumn 14, Issue 3, 2016, Pages 241-252

  Dachineni, Rakesh ^a   Ai, Guoqiang ^a   Kumar, D Ramesh ^a,b   Sadhu, Satya S ^a   Tummala, Hemachand ^a   Bhat, G Jayarama ^a  

^a SOUTH DAKOTA STATE UNIVERSITY   (United States)

^b ICAR CENTRAL INSTITUTE OF BRACKISHWATER AQUACULTURE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ACETYLSALICYLIC ACID; ANTIBODY; CYCLIN A2; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; CYCLIN E1; LACTACYSTIN; MESSENGER RNA; PROTEASOME; SALICYLIC ACID; UNCLASSIFIED DRUG; CCNA2 PROTEIN, HUMAN; CDK2 PROTEIN, HUMAN; PROTEIN BINDING;

AMINO ACID SUBSTITUTION; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER PREVENTION; CELL LYSATE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG ANTAGONISM; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME CONFORMATION; FEMALE; FLUORESCENCE ANALYSIS; GENE EXPRESSION; HT 29 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MALE; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; HT-29 CELL LINE; MCF-7 CELL LINE; METABOLISM; MOLECULAR MODEL; NEOPLASMS; TUMOR CELL LINE;

ASPIRIN; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN A2; CYCLIN-DEPENDENT KINASE 2; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HT29 CELLS; HUMANS; MCF-7 CELLS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; NEOPLASMS; PROTEIN BINDING; SALICYLIC ACID;

EID: 84962250051     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-15-0360     Document Type: Article

References (59)

1. Kaiser J. Will an aspirin a day keep cancer away? Science 2012;337:1471-3.
2. Thun MJ, Jacobs EJ, Patrono C. The role of aspirin in cancer prevention. Nat Rev Clin Oncol 2012;9:259-67.
3. Chan AT, Arber N, Burn J, Chia WK, Elwood P, Hull MA, et al. Aspirin in the chemoprevention of colorectal neoplasia: an overview. Cancer Prev Res 2012;5:164-78.
4. Rothwell PM, Price JF, Fowkes FGR, Zanchetti A, Roncaglioni MC, Tognoni G, et al. Short-term effects of daily aspirin on cancer incidence, mortality, and non-vascular death: analysis of the time course of risks and benefits in 51 randomised controlled trials. The Lancet 2012;379: 1602-12.
5. Sahasrabuddhe VV, Gunja MZ, Graubard BI, Trabert B, Schwartz LM, Park Y, et al. Nonsteroidal anti-inflammatory drug use, chronic liver disease, and hepatocellular carcinoma. J Natl Cancer Inst 2012;104:1808-14.
6. Gamba CA, Swetter SM, Stefanick ML, Kubo J, Desai M, Spaunhurst KM, et al. Aspirin is associated with lower melanoma risk among postmeno-pausal Caucasian women: the Women's Health Initiative. Cancer 2013; 119:1562-9.
7. Veitonmaki T, Tammela TL, Auvinen A, Murtola TJ. Use of aspirin, but not other non-steroidal anti-inflammatory drugs is associated with decreased prostate cancer risk at the population level. Eur J Cancer 2013;49:938-45.
8. Shpitz B, Klein E, Buklan G, Neufeld D, Nissan A, Freund HR, et al. Suppressive effect of aspirin on aberrant crypt foci in patients with colo-rectal cancer. Gut 2003;52:1598-601.
9. Chan AT, Ogino S, Fuchs CS, Aspirin use and survival after diagnosis of colorectal cancer. JAMA 2009;302:649-58.
10. Fraser D, Sullivan FM, Thompson AM, McCowan C. Aspirin use and survival after the diagnosis of breast cancer: a population-based cohort study. Br J Cancer 2014;111:623-7.
11. Dovizio M, Bruno A, Tacconelli S, Patrignani P. Mode of action of aspirin as a chemopreventive agent. Recent Results Cancer Res 2013;191:39-65.
12. Marimuthu S, Chivukula RS, Alfonso LF, Moridani M, Hagen FK, Bhat GJ, et al. Aspirin acetylates multiple cellular proteins in HCT-116 colon cancer cells: Identification of novel targets. Int J Oncol 2011;39: 1273-83.
13. Alfonso L, Ai G, Spitale RC, Bhat GJ. Molecular targets of aspirin and cancer prevention. Br J Cancer 2014;111:61-7.
14. Alfonso LF, Srivenugopal KS, Arumugam TV, Abbruscato TJ, Weidanz JA, Bhat GJ, et al. Aspirin inhibits camptothecin-induced p21CIP1 levels and potentiates apoptosis in human breast cancer cells. Int J Oncol 2009;34: 597-608.
15. Bateman LA, Zaro BW, Miller SM, Pratt MR. An alkyne-aspirin chemical reporter for the detection of aspirin-dependent protein modification in living cells. J Am Chem Soc 2013;135:14568-73.
16. Wang J, Zhang CJ, Zhang J, He Y, Lee YM, Chen S, et al. Mapping sites of aspirin-induced acetylations in live cells by quantitative acid-cleavable activity-based protein profiling (QA-ABPP). Sci Rep 2015;5.
17. Ai G, Dachineni R, Kumar DR, Marimuthu S, Alfonso LF, Bhat GJ, et al. Aspirin acetylates wild type and mutant p53 in colon cancer cells: identification of aspirin acetylated sites on recombinant p53. Tumor Biol 2015:1-10.
18. Kopp E, Ghosh S. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 1994;265:956-9.
19. Bos CL, Kodach LL, van den Brink GR, Diks SH, van Santen MM, Richel DJ, et al. Effectof aspirin on the Wnt/b-catenin pathway ismediated via protein phosphatase 2A. Oncogene 2006;25:6447-56.
20. Pathi S, Jutooru I, Chadalapaka G, Nair V, Lee SO, Safe S, et al. Aspirin inhibits colon cancer cell and tumor growth and downregulates specificity protein (Sp) transcription factors. PLoS One 2012;7:e48208.
21. Din FV, Valanciute A, Houde VP, Zibrova D, Green KA, Sakamoto K, et al. Aspirin inhibits mTOR signaling, activates AMP-activated protein kinase, and induces autophagy in colorectal cancer cells. Gastroenterology 2012; 142:1504-15.
22. Law BK, Waltner-Law ME, Entingh AJ, Chytil A, Aakre ME, Nørgaard P, et al. Salicylate-induced growth arrest is associated with inhibition of p70s6k and down-regulation of c-myc, cyclin D1, cyclin A, and proliferating cell nuclear antigen. J Biol Chem 2000;275:38261-7.
23. Borthwick GM, Johnson AS, Partington M, Burn J, Wilson R, Arthur HM, et al. Therapeutic levels of aspirin and salicylate directly inhibit a model of angiogenesis through a Cox-independent mechanism. FASEB J 2006;20: 2009-16.
24. Deshpande A, Sicinski P, Hinds PW. Cyclins and cdks in development and cancer: a perspective. Oncogene 2005;24:2909-15.
25. Pagano M, Pepperkok R, Verde V, Ansorge W, Draetta G, et al. Cyclin A is required at two points in the human cell cycle. EMBO J 1992;11:961.
26. Bendris N, Lemmers B, Blanchard JM, Arsic N. Cyclin A2 mutagenesis analysis: a new insight into CDK activation and cellular localization requirements. PLoS One 2011;6:e22879.
27. Gong D, Pomerening JR, Myers JW, Gustavsson C, Jones JT, et al. Cyclin A2 regulates nuclear-envelope breakdown and the nuclear accumulation of cyclin B1. Curr Biol 2007;17:85-91.
28. Peters JM. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 2006;7:644-56.
29. Bukholm IR, Bukholm G, Nesland JM, Over-expression ofcyclina is highly associated with early relapse and reduced survival in patients with primary breast carcinomas. Int J Cancer 2001;93:283-7.
30. Volm M, KoomA~ R, CyclinAisassociated withanunfavourableoutcome in patients with non-small-cell lung carcinomas. Brit J Cancer 1997;75:1774.
31. Ohashi R, Gao C, Miyazaki M, Hamazaki K, Tsuji T, Inoue Y, et al. Enhanced expression of cyclin E and cyclin A in human hepatocellular carcinomas. Anticancer Res 2000;21:657-662.
32. Malumbres M, Barbacid M. Cell cycle kinases in cancer. Curr Opin Genet Dev 2007;17:60-5.
33. Kanai M, Shiozawa T, Xin L, Nikaido T, Fujii S. Immunohistochemical detection of sex steroid receptors, cyclins, and cyclin-dependent kinases in the normal and neoplastic squamous epithelia of the uterine cervix. Cancer 1998;82:1709-19.
34. Anscombe E, Meschini E, Mora-Vidal R, Martin MP, Staunton D, Geitmann M, et al. Identification and characterization of an irreversible inhibitor of CDK2. Chem Biol 2015;22:1159-64.
35. Zalzali H, Nasr B, Harajly M, Basma H, Ghamloush F, Ghayad S, et al. CDK2 transcriptional repression is an essential effector in p53-dependent cellular senescence-implications for therapeutic intervention. Mol Cancer Res 2015;13:29-40.
36. Wang X, Chen X, Han W, Ruan A, Chen L, Wang R, et al. miR-200c targets CDK2 and suppresses tumorigenesis in renal cell carcinoma. Mol Cancer Res 2015:13:1567-77.
37. Choi KS, Eom YW, Kang Y, Ha MJ, Rhee H, Yoon J-W, et al. Cdc2 and Cdk2 kinase activated by transforming growth factor-b1 trigger apoptosis through the phosphorylation of retinoblastoma protein in FaO hepatoma cells. J Biol Chem 1999;274:31775-83.
38. Komander D, Kular GS, Schuttelkopf AW, Deak M, Prakash KR, Bain J, et al. Interactions of LY333531 and other bisindolyl maleimide inhibitors with PDK1. Structure 2004;12:215-26.
39. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ, et al. GROMACS: fast, flexible, and free. J Comput Chem 2005;26: 1701-18.
40. Martin MP, Alam R, Betzi S, Ingles DJ, Zhu JY, Schonbrunn E, et al. A novel approach to the discovery of small-molecule ligands of CDK2. Chembio-chem 2012;13:2128-36.
41. Goel A, Chang DK, Ricciardiello L, Gasche C, Boland CR. A novel mechanism for aspirin-mediated growth inhibitionofhuman colon cancer cells. Clin Cancer Res 2003;9:383-90.
42. Luciani MG, Campregher C, Gasche C. Aspirin blocks proliferation in colon cells by inducing a G1 arrest and apoptosis through activation of the checkpoint kinase ATM. Carcinogenesis 2007;28:2207-17.
43. Fenteany G, Schreiber SL. Lactacystin, proteasome function, and cell fate. J Biol Chem 1998;273:8545-8.
44. Hawley SA, Fullerton MD, Ross FA, Schertzer JD, Chevtzoff C, Walker KJ, et al. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012;336:918-22.
45. Choi HW, Tian M, Song F, Venereau E, Preti A, Park SW, et al. Aspirin's active metabolite salicylic acid targets high mobility group box 1 to modulate inflammatory responses. Mol Med 2015;21:526.
46. Betzi S, Alam R, Martin M, Lubbers DJ, Han H, Jakkaraj SR, et al. Discovery of a potential allosteric ligand binding sitein CDK2. ACS Chem Biol 2011; 6:492-501.
47. Bikadi Z, Hazai E. Application of the PM6 semi-empirical method to modeling proteins enhances docking accuracy of AutoDock. J Cheminfor-matics 2009;1:15.
48. Zeller KI, Jegga AG, Aronow BJ, O'Donnell KA, Dang CV. An integrated database of genes responsive to the Myc oncogenic transcription factor: Identification of direct genomic targets. Genome Biol 2003;4:R69.
49. Desdouets C, Matesic G, Molina CA, Foulkes NS, Sassone-Corsi P, Brechot C, et al. Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol Cell Biol 1995; 15:3301-9.
50. Ai G, Dachineni R, Muley P, Tummala H, Bhat GJ. Aspirin and salicylic acid decrease c-Myc expression in cancer cells: a potential role in chemopre-vention. Tumor Biol 2015:1-2.
51. Welburn JP, Tucker JA, Johnson T, Lindert L, Morgan M, Willis A, et al. How tyrosine 15 phosphorylation inhibits the activity of cyclin-dependent kinase 2-cyclin A. J Biol Chem 2007;282:3173-81.
52. Lees E. Cyclin dependent kinase regulation. Curr Opin Cell Biol 1995;7: 773-80.
53. Overington J, Johnson MS, Sali A, Blundell TL. Tertiary structural constraints on protein evolutionary diversity: templates, key residues and structure prediction. Proc Biol Sci 1990;241:132-45.
54. Yu X, Cojocaru V, Wade RC. Conformational diversity and ligand tunnels of mammaliancytochrome P450s. Biotechnol ApplBiochem2013;60:134-45.
55. Qiao L, Hanif R, Sphicas E, Shiff SJ, Rigas B. Effect of aspirinon induction of apoptosis in HT-29 human colon adenocarcinoma cells. Biochem Pharmacol 1998;55:53-64.
56. Shiff SJ, Koutsos MI, Qiao L, Rigas B, et al. Nonsteroidal antiinflammatory drugs inhibit the proliferation of colon adenocarcinoma cells: effects on cell cycle and apoptosis. Exp Cell Res 1996;222:179-88.
57. Davies TG, Bentley J, Arris CE, Boyle FT, Curtin NJ, Endicott JA, et al. Structure-based design of a potent purine-based cyclin-dependent kinase inhibitor. Nat Struct Biol 2002;9:745-9.
58. Deng Y, Shipps GW, Zhao L, Siddiqui MA, Popovici-Muller J, Curran PJ, et al. Modulating the interaction between CDK2 and cyclin A with a quinoline-based inhibitor. Bioorg Med Chem Lett 2014;24:199-203.
59. Alvarez ME. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. In programmed cell death in higher plants. 2000, p. 185-98. Springer Netherlands.