Boswellic acid induces epigenetic alterations by modulating DNA methylation in colorectal cancer cells

Cancer Biology and Therapy

Volumn 13, Issue 7, 2012, Pages 542-552

  Shen, Yan ^a   Takahashi, Masanobu ^a   Byun, Hyang Min ^b   Link, Alexander ^a   Sharma, Nupur ^a   Balaguer, Francesc ^a   Leung, Hon Chiu E ^c   Boland, C Richard ^a   Goel, Ajay ^a  

^a BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Acetyl keto beta boswellic acid (AKBA); Boswellic acid; Chemoprevention; Colorectal cancer; DNA methylation; Epigenetics

Indexed keywords

ACETYL KETO BETA BOSWELLIC ACID; BOSWELLIA SERRATA EXTRACT; BOSWELLIC ACID; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CHEMOPROPHYLAXIS; COLORECTAL CANCER; CONTROLLED STUDY; DNA METHYLATION; DRUG ACTIVITY; EPIGENETICS; EVIDENCE BASED PRACTICE; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; SAMD14 GENE; SMPD3 GENE; TUMOR SUPPRESSOR GENE;

ANTI-INFLAMMATORY AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL NEOPLASMS; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRITERPENES;

EID: 84861113643     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.19604     Document Type: Article

References (46)

1. Shah BA, Qazi GN, Taneja SC. Boswellic acids: a group of medicinally important compounds. Nat Prod Rep 2009; 26:72-89; PMID:19374123; http://dx.doi. org/10.1039/b809437n.
2. Moussaieff A, Mechoulam R. Boswellia resin: from religious ceremonies to medical uses; a review of in-vitro, in-vivo and clinical trials. J Pharm Pharmacol 2009; 61:1281-93; PMID:19814859.
3. Gupta I, Parihar A, Malhotra P, Singh GB, Lüdtke R, Safayhi H, et al. Effects of Boswellia serrata gum resin in patients with ulcerative colitis. Eur J Med Res 1997; 2:37-43; PMID:9049593.
4. Sharma ML, Bani S, Singh GB. Anti-arthritic activity of boswellic acids in bovine serum albumin (BSA)-induced arthritis. Int J Immunopharmacol 1989; 11:647-52; PMID:2807636; http://dx.doi. org/10.1016/0192-0561(89)90150-1.
5. Gerhardt H, Seifert F, Buvari P, Vogelsang H, Repges R. [Therapy of active Crohn disease with Boswellia serrata extract H 15]. Z Gastroenterol 2001; 39:11-7; PMID:11215357; http://dx.doi. org/10.1055/s-2001-10708.
6. Liu JJ, Nilsson A, Oredsson S, Badmaev V, Zhao WZ, Duan RD. Boswellic acids trigger apoptosis via a pathway dependent on caspase-8 activation but independent on Fas/Fas ligand interaction in colon cancer HT-29 cells. Carcinogenesis 2002; 23:2087- 93; PMID:12507932; http://dx.doi.org/10.1093/ carcin/ 23.12.2087.
7. Liu JJ, Huang B, Hooi SC. Acetyl-keto-betaboswellic acid inhibits cellular proliferation through a p21-dependent pathway in colon cancer cells. Br J Pharmacol 2006; 148:1099-107; PMID:16783403; http://dx.doi.org/10.1038/sj. bjp.0706817.
8. Lu M, Xia L, Hua H, Jing Y. Acetyl-keto-betaboswellic acid induces apoptosis through a death receptor 5-mediated pathway in prostate cancer cells. Cancer Res 2008; 68:1180-6; PMID:18281494; http://dx.doi. org/10.1158/0008-5472. CAN-07-2978.
9. Pang X, Yi Z, Zhang X, Sung B, Qu W, Lian X, et al. Acetyl-11-keto-beta- boswellic acid inhibits prostate tumor growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis. Cancer Res 2009; 69:5893-900; PMID:19567671; http://dx.doi.org/10.1158/0008-5472.CAN-09-0755.
10. Hostanska K, Daum G, Saller R. Cytostatic and apoptosis-inducing activity of boswellic acids toward malignant cell lines in vitro. Anticancer Res 2002; 22:2853-62; PMID:12530009.
11. Liu JJ, Nilsson A, Oredsson S, Badmaev V, Duan RD. Keto- and acetyl-keto-boswellic acids inhibit proliferation and induce apoptosis in Hep G2 cells via a caspase-8 dependent pathway. Int J Mol Med 2002; 10:501-5; PMID:12239601.
12. Glaser T, Winter S, Groscurth P, Safayhi H, Sailer ER, Ammon HP, et al. Boswellic acids and malignant glioma: induction of apoptosis but no modulation of drug sensitivity. Br J Cancer 1999; 80:756- 65; PMID:10360653; http://dx.doi.org/10.1038/ sj.bjc.6690419.
13. Takada Y, Ichikawa H, Badmaev V, Aggarwal BB. Acetyl-11-keto-beta- boswellic acid potentiates apoptosis, inhibits invasion and abolishes osteoclastogenesis by suppressing NFkappaB and NFkappaB-regulated gene expression. J Immunol 2006; 176:3127-40; PMID:16493072.
14. Kunnumakkara AB, Nair AS, Sung B, Pandey MK, Aggarwal BB. Boswellic acid blocks signal transducers and activators of transcription 3 signaling, proliferation and survival of multiple myeloma via the protein tyrosine phosphatase SHP-1. Mol Cancer Res 2009; 7:118-28; PMID:19147543; http://dx.doi. org/10.1158/1541-7786.MCR-08-0154.
15. Kantarjian H, Issa JP, Rosenfeld CS, Bennett JM, Albitar M, DiPersio J, et al. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer 2006; 106:1794-803; PMID:16532500; http://dx.doi. org/10.1002/cncr.21792.
16. Kantarjian H, Oki Y, Garcia-Manero G, Huang X, O'Brien S, Cortes J, et al. Results of a randomized study of 3 schedules of low-dose decitabine in higher-risk myelodysplastic syndrome and chronic myelomonocytic leukemia. Blood 2007; 109:52-7; PMID:16882708; http://dx.doi.org/10.1182/blood- 2006-05-021162.
17. Kopelovich L, Crowell JA, Fay JR. The epigenome as a target for cancer chemoprevention. J Natl Cancer Inst 2003; 95:1747-57; PMID:14652236; http://dx.doi. org/10.1093/jnci/dig109.
18. Issa JP. Cancer prevention: epigenetics steps up to the plate. Cancer Prev Res (Phila) 2008; 1:219-22; PMID:19138962; http://dx.doi.org/10.1158/1940- 6207.CAPR-08-0029.
19. Laird PW, Jackson-Grusby L, Fazeli A, Dickinson SL, Jung WE, Li E, et al. Suppression of intestinal neoplasia by DNA hypomethylation. Cell 1995; 81:197-205; PMID:7537636; http://dx.doi.org/10.1016/0092- 8674(95)90329-1.
20. Yoo CB, Chuang JC, Byun HM, Egger G, Yang AS, Dubeau L, et al. Long-term epigenetic therapy with oral zebularine has minimal side effects and prevents intestinal tumors in mice. Cancer Prev Res (Phila) 2008; 1:233-40; PMID:19138966; http://dx.doi. org/10.1158/1940-6207.CAPR-07-0008.
21. Yoo CB, Jones PA. Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov 2006; 5:37-50; PMID:16485345; http://dx.doi.org/10.1038/ nrd1930.
22. Link A, Balaguer F, Goel A. Cancer chemoprevention by dietary polyphenols: promising role for epigenetics. Biochem Pharmacol 2010; 80:1771-92; PMID:20599773; http://dx.doi.org/10.1016/j. bcp.2010.06.036.
23. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 1997; 57:808-11; PMID:9041175.
24. Sun W, Iijima T, Kano J, Kobayashi H, Li D, Morishita Y, et al. Frequent aberrant methylation of the promoter region of sterile alpha motif domain 14 in pulmonary adenocarcinoma. Cancer Sci 2008; 99:2177-84; PMID:18823374; http://dx.doi.org/10.1111/j.1349- 7006.2008.00965.x.
25. Marchesini N, Luberto C, Hannun YA. Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J Biol Chem 2003; 278:13775-83; PMID:12566438; http://dx.doi. org/10.1074/jbc.M212262200.
26. Demircan B, Dyer LM, Gerace M, Lobenhofer EK, Robertson KD, Brown KD. Comparative epigenomics of human and mouse mammary tumors. Genes Chromosomes Cancer 2009; 48:83-97; PMID:18836996; http://dx.doi.org/10.1002/ gcc.20620.
27. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999; 96:8681-6; PMID:10411935; http://dx.doi. org/10.1073/pnas.96.15.8681.
28. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 2006; 38:787-93; PMID:16804544; http://dx.doi.org/10.1038/ng1834.
29. Goel A, Nagasaka T, Arnold CN, Inoue T, Hamilton C, Niedzwiecki D, et al. The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer. Gastroenterology 2007; 132:127-38; PMID:17087942; http://dx.doi. org/10.1053/j.gastro.2006.09.018.
30. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003; 300:455; PMID:12702868; http://dx.doi.org/10.1126/science. 1083557.
31. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, et al. Induction of tumors in mice by genomic hypomethylation. Science 2003; 300:489- 92; PMID:12702876; http://dx.doi.org/10.1126/science. 1083558.
32. Cuzick J, Otto F, Baron JA, Brown PH, Burn J, Greenwald P, et al. Aspirin and non-steroidal antiinflammatory drugs for cancer prevention: an international consensus statement. Lancet Oncol 2009; 10:501-7; PMID:19410194; http://dx.doi. org/10.1016/S1470-2045(09)70035-X.
33. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, Kim K, et al.; APC Study Investigators. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 2006; 355:873-84; PMID:16943400; http://dx.doi.org/10.1056/ NEJMoa061355.
34. Bardelli A, Siena S. Molecular mechanisms of resistance to cetuximab and panitumumab in colorectal cancer. J Clin Oncol 2010; 28:1254-61; PMID:20100961; http://dx.doi.org/10.1200/JCO.2009.24.6116.
35. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology 2010; 138:2073- 87; PMID:20420947; http://dx.doi.org/10.1053/j. gastro.2009.12.064.
36. van Engeland M, Derks S, Smits KM, Meijer GA, Herman JG. Colorectal cancer epigenetics: complex simplicity. J Clin Oncol 2011; 29:1382-91; PMID:21220596; http://dx.doi.org/10.1200/ JCO.2010.28.2319.
37. Kristensen LS, Mikeska T, Krypuy M, Dobrovic A. Sensitive Melting Analysis after Real Time-Methylation Specific PCR (SMART-MSP): high-throughput and probe-free quantitative DNA methylation detection. Nucleic Acids Res 2008; 36:42; PMID:18344521; http://dx.doi.org/10.1093/nar/gkn113.
38. Arachchige Don AS, Dallapiazza RF, Bennin DA, Brake T, Cowan CE, Horne MC. Cyclin G2 is a centrosome-associated nucleocytoplasmic shuttling protein that influences microtubule stability and induces a p53-dependent cell cycle arrest. Exp Cell Res 2006; 312:4181-204; PMID:17123511; http://dx.doi. org/10.1016/j.yexcr.2006.09.023.
39. Knowles LM, Yang C, Osterman A, Smith JW. Inhibition of fatty-acid synthase induces caspase-8-mediated tumor cell apoptosis by upregulating DDIT4. J Biol Chem 2008; 283:31378-84; PMID:18796435; http://dx.doi.org/10.1074/jbc. M803384200.
40. Horak P, Crawford AR, Vadysirisack DD, Nash ZM, DeYoung MP, Sgroi D, et al. Negative feedback control of HIF-1 through REDD1-regulated ROS suppresses tumorigenesis. Proc Natl Acad Sci USA 2010; 107:4675-80; PMID:20176937; http://dx.doi. org/10.1073/pnas.0907705107.
41. Schutte B, Henfling M, Ramaekers FC. DEDD association with cytokeratin filaments correlates with sensitivity to apoptosis. Apoptosis 2006; 11:1561-72; PMID:16820959; http://dx.doi.org/10.1007/s10495- 006-9113-0.
42. Arai S, Miyake K, Voit R, Nemoto S, Wakeland EK, Grummt I, et al. Death-effector domain-containing protein DEDD is an inhibitor of mitotic Cdk1/ cyclin B1. Proc Natl Acad Sci USA 2007; 104:2289- 94; PMID:17283331; http://dx.doi.org/10.1073/ pnas.0611167104.
43. Ohta M, Inoue H, Cotticelli MG, Kastury K, Baffa R, Palazzo J, et al. The FHIT gene, spanning the chromosome 3p14.2 fragile site and renal carcinoma-associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell 1996; 84:587-97; PMID:8598045; http://dx.doi. org/10.1016/S0092-8674(00) 81034-X.
44. Behrends U, Schneider I, Rössler S, Frauenknecht H, Golbeck A, Lechner B, et al. Novel tumor antigens identified by autologous antibody screening of childhood medulloblastoma cDNA libraries. Int J Cancer 2003; 106:244-51; PMID:12800201; http://dx.doi. org/10.1002/ijc.11208.
45. Wang Z, Shen D, Parsons DW, Bardelli A, Sager J, Szabo S, et al. Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 2004; 304:1164-6; PMID:15155950; http://dx.doi. org/10.1126/science.1096096.
46. Samuels-Lev Y, O'Connor DJ, Bergamaschi D, Trigiante G, Hsieh JK, Zhong S, et al. ASPP proteins specifically stimulate the apoptotic function of p53. Mol Cell 2001; 8:781-94; PMID:11684014; http:// dx.doi.org/10.1016/S1097- 2765(01)00367-7.