Cucurbitacin B alters the expression of tumor-related genes by epigenetic modifications in NSCLC and inhibits NNK-induced lung tumorigenesis

Cancer Prevention Research

Volumn 8, Issue 6, 2015, Pages 552-562

  Shukla, Samriddhi ^a   Khan, Sajid ^a   Kumar, Sudhir ^a   Sinha, Sonam ^a   Farhan, MohD ^a   Bora, Himangsu K ^a   Maurya, Rakesh ^a,b   Meeran, Syed Musthapa ^a,b  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

Author keywords

[No Author keywords available]

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ANTINEOPLASTIC AGENT; CUCURBITACIN; CUCURBITACIN B; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 6; HISTONE H3; HISTONE H4; K RAS PROTEIN; METHYLTRANSFERASE; MYC PROTEIN; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; 4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; CARCINOGEN; HISTONE DEACETYLASE; MESSENGER RNA; NITROSAMINE; TRITERPENE;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INCIDENCE; CELL CYCLE ARREST; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA MODIFICATION; DOWN REGULATION; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; LOW DRUG DOSE; LUNG CANCER CELL LINE; LUNG CARCINOGENESIS; LUNG PARENCHYMA; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TIME-DEPENDENT INHIBITION; TRANSCRIPTION INITIATION; TUMOR SUPPRESSOR GENE; UPREGULATION; A J MOUSE; ANIMAL; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL TRANSFORMATION; CHEMICALLY INDUCED; CHEMISTRY; DNA METHYLATION; DRUG EFFECTS; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LUNG NEOPLASMS; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHWESTERN BLOTTING; TUMOR CELL CULTURE; TUMOR GENE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, SOUTHWESTERN; BLOTTING, WESTERN; CARCINOGENS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HISTONE DEACETYLASES; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MICE; MICE, INBRED A; NITROSAMINES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRITERPENES; TUMOR CELLS, CULTURED;

EID: 84941769715     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-14-0286     Document Type: Article

References (45)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Shukla S, Khan S, Tollefsbol TO, Meeran SM. Genetics and epigenetics of lung cancer: mechanisms and future perspectives. Curr Cancer Ther Rev 2013;9:97-110.
3. Meeran SM, Ahmed A, Tollefsbol TO. Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics 2010;1:101-16.
4. Fang MZ, Wang Y, Ai N, Hou Z, Sun Y, Lu H, et al. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 2003;63:7563-70.
5. Jha AK, Nikbakht M, Parashar G, Shrivastava A, Capalash N, Kaur J. Reversal of hypermethylation and reactivation of the RARbeta2 gene by natural compounds in cervical cancer cell lines. Folia Biol 2010;56:195-200.
6. Meeran SM, Patel SN, Li Y, Shukla S, Tollefsbol TO. Bioactive dietary supplements reactivate ER expression in ER-negative breast cancer cells by active chromatin modifications. PLoS One 2012;7:e37748.
7. Myzak MC, Ho E, Dashwood RH. Dietary agents as histone deacetylase inhibitors. Mol Carcinog 2006;45:443-6.
8. Li Y, Chen H, Hardy TM, Tollefsbol TO. Epigenetic regulation of multiple tumor-related genes leadsto suppression of breast tumorigenesis by dietary genistein. PLoS One 2013;8:e54369.
9. Alghasham AA. Cucurbitacins - a promising target for cancer therapy. Int J Health Sci 2013;7:77-89.
10. Chen JC, Chiu MH, Nie RL, Cordell GA, Qiu SX. Cucurbitacins and cucurbitane glycosides: structures and biological activities. Nat Prod Rep 2005;22:386-99.
11. Attard E, Brincat MP, Cuschieri A. Immunomodulatory activity of cucurbitacin E isolated from Ecballium elaterium. Fitoterapia 2005;76:439-41.
12. Chen C, Qiang S, Lou L, Zhao W. Cucurbitane-type triterpenoids from the stems of Cucumis melo. J Nat Prod 2009;72:824-9.
13. Chen W, Leiter A, Yin D, Meiring M, Louw VJ, Koeffler HP. Cucurbitacin B inhibits growth, arrests the cell cycle, and potentiates antiproliferative efficacy of cisplatin in cutaneous squamous cell carcinoma cell lines. Int J Oncol 2010;37:737-43.
14. Aribi A, Gery S, Lee DH, Thoennissen NH, Thoennissen GB, Alvarez R, et al. The triterpenoid cucurbitacin B augments the antiproliferative activity of chemotherapy in human breast cancer. Int J Cancer 2013;132:2730-7.
15. Zhang M, Sun C, Shan X, Yang X, Li-Ling J, Deng Y. Inhibition of pancreatic cancer cell growth by cucurbitacin B through modulation of signal transducer and activator of transcription 3 signaling. Pancreas 2010;39:923-9.
16. Chan KT, Meng FY, Li Q, Ho CY, Lam TS, To Y, et al. Cucurbitacin B induces apoptosis and S phase cell cycle arrest in BEL-7402 human hepatocellular carcinoma cells and is effective via oral administration. Cancer Lett 2010;294:118-24.
17. Kausar H, Munagala R, Bansal SS, Aqil F, Vadhanam MV, Gupta RC. Cucurbitacin B potently suppresses non-small-cell lung cancer growth: identification of intracellular thiols as critical targets. Cancer Lett 2013;332:35-45.
18. Thoennissen NH, Iwanski GB, Doan NB, Okamoto R, Lin P, Abbassi S, et al. Cucurbitacin B induces apoptosis by inhibition of the JAK/STAT pathway and potentiates antiproliferative effects of gemcitabine on pancreatic cancer cells. Cancer Res 2009;69:5876-84.
19. Zhang Y, Ouyang D, Xu L, Ji Y, Zha Q, Cai J, et al. Cucurbitacin B induces rapid depletion of the G-actin pool through reactive oxygen speciesdependent actin aggregation in melanoma cells. Acta Biochim Biophys Sin 2011;43:556-67.
20. Ayyad SE, Abdel-Lateff A, Basaif SA, Shier T. Cucurbitacins-type triterpene with potent activity on mouse embryonic fibroblast from Cucumis prophetarum, cucurbitaceae. Pharmacognosy Res 2011;3:189-93.
21. Meeran SM, Patel SN, Tollefsbol TO. Sulforaphane causes epigenetic repression of hTERT expression in human breast cancer cell lines. PLoS One 2010;5:e11457.
22. Meeran SM, Patel SN, Chan TH, Tollefsbol TO. A novel prodrug of epigallocatechin-3-gallate: differential epigenetic hTERT repression in human breast cancer cells. Cancer Prev Res 2011;4:1243-54.
23. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, et al. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004;64:2307-16.
24. Barta P, Van Pelt C, Men T, Dickey BF, Lotan R, Moghaddam SJ. Enhancement of lung tumorigenesis in a Gprc5a Knockout mouse by chronic extrinsic airway inflammation. Mol Cancer 2012;11:4-15.
25. Akhtar S, Meeran SM, Katiyar N, Katiyar SK. Grape seed proanthocyanidins inhibit the growth of human non-small cell lung cancer xenografts by targeting insulin-like growth factor binding protein-3, tumor cell proliferation, and angiogenic factors. Clin Cancer Res 2009;15:821-31.
26. Boisvert FM, Ahmad Y, Gierliński M, Charriere F, Lamont D, Scott M, et al. A Quantitative spatial proteomics analysis of proteome turnover in human cells. Mol Cell Proteomics 2012;11:M111.011429.
27. Reed SI. Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover. Nat Rev Mol Cell Biol 2003;4:855-64.
28. Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, Kawamoto K, et al. Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification. Cancer Res 2008;68:2736-44.
29. Shukla S, Meeran SM. Epigenetic factors in breast cancer progression. In: Ahmad A, editor. Breast cancer metastasis and drug resistance. Springer Publications; New York, 2013. p. 341-65.
30. Li Y, Yuan YY, Meeran SM, Tollefsbol TO. Synergistic epigenetic reactivation of estrogen receptor-alpha (ERalpha) by combined green tea polyphenol and histone deacetylase inhibitor in ERalpha-negative breast cancer cells. Mol Cancer 2010;9:274.
31. Guilleret I, Yan P, Grange F, Braunschweig R, Bosman FT, Benhattar J. Hypermethylation of the human telomerase catalytic subunit (hTERT) gene correlates with telomerase activity. Int J Cancer 2002;101:335-41.
32. Zhu JS, Ouyang DY, Shi ZJ, Xu LH, Zhang YT, He XH. Cucurbitacin B induces cell cycle arrest, apoptosis and autophagy associated with G actin reduction and persistent activation of cofilin in Jurkat cells. Pharmacology 2012;89:348-6.
33. Zhang T, Li Y, Park KA, Byun HS, Won M, Jeon J, et al. Cucurbitacin induces autophagy through mitochondrial ROS production which counteracts to limit caspase-dependent apoptosis. Autophagy 2012;8:559-76.
34. McCool KW, Xu X, Singer DB, Murdoch FE, Fritsch MK. The role of histone acetylation in regulating early gene expression patterns during early embryonic stem cell differentiation. J Biol Chem 2007;282:6696-706.
35. Tang Z, Chen WY, Shimada M, Nguyen UT, Kim J, Sun XJ, et al. SET1 and p300 act synergistically, through coupled histone modifications, in transcriptional activation by p53. Cell 2013;154:297-310.
36. Ducasse M, Brown MA. Epigenetic aberrations and cancer. Mol Cancer 2006;5:60.
37. Kouzarides T. Histone methylation in transcriptional control. Curr Opin Genet Dev 2002;12:198-209.
38. Huang L, Sowa Y, Sakai T, Pardee AB. Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene 2000;19:5712-9.
39. Xiao H, Hasegawa T, Isobe K. p300 collaborates with Sp1 and Sp3 in p21 (waf1/cip1) promoter activation induced by histone deacetylase inhibitor. J Biol Chem 2000;275:1371-6.
40. Gartel AL, Ye X, Goufman E, Shianov P, Hay N, Najmabadi F, et al. Myc represses the p21 (WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proc Natl Acad Sci U S A 2001;98:4510-5.
41. Lin RK, Hsieh YS, Lin P, Hsu HS, Chen CY, Tang YA, et al. The tobaccospecific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients. J Clin Invest 2010;120:521-32.
42. Tang W, Kuruvilla SA, Galitovskiy V, Pan ML, Grando SA, Mukherjee J. Targeting histone deacetylase in lung cancer for early diagnosis: (18) F-FAHAPET/CT imaging of NNK-treated A/J mice model. Am J Nucl Med Mol Imaging 2014;4:324-32.
43. Ecke I, Petry F, Rosenberger A, Tauber S, Mönkemeyer S, Hess I, et al. Antitumor effects of a combined 5-aza-2'deoxycytidine and valproic acid treatment on rhabdomyosarcoma and medulloblastoma in Ptch mutant mice. Cancer Res 2009;69(3):887-95.
44. Tellez CS, Grimes MJ, Picchi MA, Liu Y, March TH, Reed MD, etal. SGI-110 and entinostat therapy reduces lung tumor burden and reprograms the epigenome. Int J Cancer 2014;135:2223-31.
45. Belinsky SA, Swafford DS, Middleton SK, Kennedy CH, Tesfaigzi J. Deletion and differential expression of p16INK4a in mouse lung tumors. Carcinogenesis 1997;18:115-20.