Epigenetic modifications and p21-cyclin B1 nexus in anticancer effect of histone deacetylase inhibitors in combination with silibinin on non-small cell lung cancer cells

Epigenetics

Volumn 7, Issue 10, 2012, Pages 1161-1172

  Mateen, Samiha ^a   Raina, Komal ^a   Jain, Anil K ^a   Agarwal, Chapla ^a,b   Chan, Daniel ^b,c   Agarwal, Rajesh ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Cell cycle; Epigenetics; HDAC inhibitors; Lung cancer; Silibinin

Indexed keywords

ALPHA TUBULIN; CYCLIN B1; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; HISTONE H3; HISTONE H4; PROTEIN P21; PROTEIN TYROSINE PHOSPHATASE; SILIBININ; TRICHOSTATIN A; VORINOSTAT;

ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; EPIGENETICS; G2 PHASE CELL CYCLE CHECKPOINT; HISTONE ACETYLATION; IMMUNOREACTIVITY; LUNG NON SMALL CELL CANCER; MITOSIS; MITOSIS INHIBITION; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TIGHT JUNCTION; TRANSCRIPTION INITIATION; TUMOR GROWTH; XENOGRAFT;

EID: 84867164315     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.22070     Document Type: Article

References (44)

1. American Cancer Society: Cancer Facts and Figures 2012. Atlanta: American Cancer Society, 2012.
2. Risch A, Plass C. Lung cancer epigenetics and genetics. Int J Cancer 2008; 123:1-7; PMID:18425819; http://dx.doi.org/10.1002/ijc.23605.
3. Belinsky SA, Grimes MJ, Picchi MA, Mitchell HD, Stidley CA, Tesfaigzi Y, et al. Combination therapy with vidaza and entinostat suppresses tumor growth and reprograms the epigenome in an orthotopic lung cancer model. Cancer Res 2011; 71:454-62; PMID:21224363; http://dx.doi.org/10.1158/0008-5472.CAN-10-3184.
4. Hirsch FR, Lippman SM. Advances in the biology of lung cancer chemoprevention. J Clin Oncol 2005; 23:3186-97; PMID:15886305; http://dx.doi.org/10.1200/JCO.2005.14.209.
5. Song SH, Han SW, Bang YJ. Epigenetic-based therapies in cancer: progress to date. Drugs 2011; 71:2391-403; PMID:22141383; http://dx.doi.org/10.2165/11596690-000000000-00000.
6. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 2005; 102:10604-9; PMID:16009939; http://dx.doi.org/10.1073/pnas.0500398102.
7. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell 2007; 128:635-8; PMID:17320500; http://dx.doi.org/10.1016/j.cell.2007.02.006.
8. Yang IV, Schwartz DA. Epigenetic control of gene expression in the lung. Am J Respir Crit Care Med 2011; 183:1295-301; PMID:21596832; http://dx.doi.org/10.1164/rccm.201010-1579PP.
9. Chi P, Allis CD, Wang GG. Covalent histone modifications--miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 2010; 10:457-69; PMID:20574448; http://dx.doi.org/10.1038/nrc2876.
10. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997; 389:349-52; PMID:9311776; http://dx.doi.org/10.1038/38664.
11. Wade PA. Transcriptional control at regulatory checkpoints by histone deacetylases: molecular connections between cancer and chromatin. Hum Mol Genet 2001; 10:693-8; PMID:11257101; http://dx.doi.org/10.1093/hmg/10.7.693.
12. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006; 5:769-84; PMID:16955068; http://dx.doi.org/10.1038/nrd2133.
13. Bots M, Johnstone RW. Rational combinations using HDAC inhibitors. Clin Cancer Res 2009; 15:3970-7; PMID:19509171; http://dx.doi.org/10.1158/1078-0432.CCR-08-2786.
14. Wagner JM, Hackanson B, Lübbert M, Jung M. Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clin Epigenetics 2010; 1:117-36; PMID:21258646; http://dx.doi.org/10.1007/s13148-010-0012-4.
15. Lee MJ, Kim YS, Kummar S, Giaccone G, Trepel JB. Histone deacetylase inhibitors in cancer therapy. Curr Opin Oncol 2008; 20:639-49; PMID:18841045; http://dx.doi.org/10.1097/CCO.0b013e3283127095.
16. Rasheed WK, Johnstone RW, Prince HM. Histone deacetylase inhibitors in cancer therapy. Expert Opin Investig Drugs 2007; 16:659-78; PMID:17461739; http://dx.doi.org/10.1517/13543784.16.5.659.
17. Chang J, Varghese DS, Gillam MC, Peyton M, Modi B, Schiltz RL, et al. Differential response of cancer cells to HDAC inhibitors trichostatin A and depsipeptide. Br J Cancer 2012; 106:116-25; PMID:22158273; http://dx.doi.org/10.1038/bjc.2011.532.
18. Schrump DS. Cytotoxicity mediated by histone deacetylase inhibitors in cancer cells: mechanisms and potential clinical implications. Clin Cancer Res 2009; 15:3947-57; PMID:19509170; http://dx.doi.org/10.1158/1078-0432.CCR-08-2787.
19. Mateen S, Tyagi A, Agarwal C, Singh RP, Agarwal R. Silibinin inhibits human nonsmall cell lung cancer cell growth through cell-cycle arrest by modulating expression and function of key cell-cycle regulators. Mol Carcinog 2010; 49:247-58; PMID:19908243.
20. Ramasamy K, Agarwal R. Multitargeted therapy of cancer by silymarin. Cancer Lett 2008; 269:352-62; PMID:18472213; http://dx.doi.org/10.1016/j.canlet.2008.03.053.
21. Ramasamy K, Dwyer-Nield LD, Serkova NJ, Hasebroock KM, Tyagi A, Raina K, et al. Silibinin prevents lung tumorigenesis in wild-type but not in iNOS-/- mice: potential of real-time micro-CT in lung cancer chemoprevention studies. Clin Cancer Res 2011; 17:753-61; PMID:21148748; http://dx.doi.org/10.1158/1078-0432.CCR-10-2290.
22. Singh RP, Deep G, Chittezhath M, Kaur M, Dwyer- Nield LD, Malkinson AM, et al. Effect of silibinin on the growth and progression of primary lung tumors in mice. J Natl Cancer Inst 2006; 98:846-55; PMID:16788158; http://dx.doi.org/10.1093/jnci/djj231.
23. Singh RP, Mallikarjuna GU, Sharma G, Dhanalakshmi S, Tyagi AK, Chan DC, et al. Oral silibinin inhibits lung tumor growth in athymic nude mice and forms a novel chemocombination with doxorubicin targeting nuclear factor kappaB-mediated inducible chemoresistance. Clin Cancer Res 2004; 10:8641-7; PMID:15623648; http://dx.doi.org/10.1158/1078-0432.CCR-04-1435.
24. Tyagi A, Agarwal C, Dwyer-Nield LD, Singh RP, Malkinson AM, Agarwal R. Silibinin modulates TNF-α and IFN-γ mediated signaling to regulate COX2 and iNOS expression in tumorigenic mouse lung epithelial LM2 cells. Mol Carcinog 2011; In press; PMID:21882257; http://dx.doi.org/10.1002/mc.20851.
25. Chittezhath M, Deep G, Singh RP, Agarwal C, Agarwal R. Silibinin inhibits cytokine-induced signaling cascades and down-regulates inducible nitric oxide synthase in human lung carcinoma A549 cells. Mol Cancer Ther 2008; 7:1817-26; PMID:18644994; http://dx.doi.org/10.1158/1535-7163.MCT-08-0256.
26. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58:621-81; PMID:16968952; http://dx.doi.org/10.1124/pr.58.3.10.
27. Raina K, Agarwal R. Combinatorial strategies for cancer eradication by silibinin and cytotoxic agents: efficacy and mechanisms. Acta Pharmacol Sin 2007; 28:1466-75; PMID:17723180; http://dx.doi.org/10.1111/j.1745-7254.2007.00691.x.
28. Ding M, Feng Y, Vandré DD. Partial characterization of the MPM-2 phosphoepitope. Exp Cell Res 1997; 231:3-13; PMID:9056407; http://dx.doi.org/10.1006/excr.1996.3439.
29. Ishii S, Kurasawa Y, Wong J, Yu-Lee LY. Histone deacetylase 3 localizes to the mitotic spindle and is required for kinetochore-microtubule attachment. Proc Natl Acad Sci U S A 2008; 105:4179-84; PMID:18326024; http://dx.doi.org/10.1073/pnas.0710140105.
30. Zhang HY, Gu YY, Li ZG, Jia YH, Yuan L, Li SY, et al. Exposure of human lung cancer cells to 8-chloro-adenosine induces G2/M arrest and mitotic catastrophe. Neoplasia 2004; 6:802-12; PMID:15720807; http://dx.doi.org/10.1593/neo.04247.
31. Pines J, Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J Cell Biol 1991; 115:1-17; PMID:1717476; http://dx.doi.org/10.1083/jcb.115.1.1.
32. Roy S, Kaur M, Agarwal C, Tecklenburg M, Sclafani RA, Agarwal R. p21 and p27 induction by silibinin is essential for its cell cycle arrest effect in prostate carcinoma cells. Mol Cancer Ther 2007; 6:2696-707; PMID:17938263; http://dx.doi.org/10.1158/1535-7163.MCT-07-0104.
33. Dulić V, Stein GH, Far DF, Reed SI. Nuclear accumulation of p21Cip1 at the onset of mitosis: a role at the G2/M-phase transition. Mol Cell Biol 1998; 18:546-57; PMID:9418901.
34. Gillis LD, Leidal AM, Hill R, Lee PW. p21Cip1/WAF1 mediates cyclin B1 degradation in response to DNA damage. Cell Cycle 2009; 8:253-6; PMID:19158493; http://dx.doi.org/10.4161/cc.8.2.7550.
35. Kumagai T, Wakimoto N, Yin D, Gery S, Kawamata N, Takai N, et al. Histone deacetylase inhibitor, suberoylanilide hydroxamic acid (Vorinostat, SAHA) profoundly inhibits the growth of human pancreatic cancer cells. International journal of cancer 2007; 121:656-65.
36. Okamoto H, Fujioka Y, Takahashi A, Takahashi T, Taniguchi T, Ishikawa Y, et al. Trichostatin A, an inhibitor of histone deacetylase, inhibits smooth muscle cell proliferation via induction of p21(WAF1). J Atheroscler Thromb 2006; 13:183-91; PMID:16908950; http://dx.doi.org/10.5551/jat.13.183.
37. Rocchi P, Tonelli R, Camerin C, Purgato S, Fronza R, Bianucci F, et al. p21Waf1/Cip1 is a common target induced by short-chain fatty acid HDAC inhibitors (valproic acid, tributyrin and sodium butyrate) in neuroblastoma cells. Oncol Rep 2005; 13:1139-44; PMID:15870934.
38. Nian H, Delage B, Pinto JT, Dashwood RH. Allyl mercaptan, a garlic-derived organosulfur compound, inhibits histone deacetylase and enhances Sp3 binding on the P21WAF1 promoter. Carcinogenesis 2008; 29:1816-24; PMID:18628250; http://dx.doi.org/10.1093/carcin/bgn165.
39. Herceg Z, Vaissière T. Epigenetic mechanisms and cancer: an interface between the environment and the genome. Epigenetics 2011; 6:804-19; PMID:21758002; http://dx.doi.org/10.4161/epi.6.7.16262.
40. Witt O, Deubzer HE, Milde T, Oehme I. HDAC family: What are the cancer relevant targets? Cancer Lett 2009; 277:8-21; PMID:18824292; http://dx.doi.org/10.1016/j.canlet.2008.08.016.
41. Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int J Biochem Cell Biol 2007; 39:1367-74; PMID:17412634; http://dx.doi.org/10.1016/j.biocel.2007.03.001.
42. Blagosklonny MV, Robey R, Sackett DL, Du L, Traganos F, Darzynkiewicz Z, et al. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol Cancer Ther 2002; 1:937-41; PMID:12481415.
43. Witta SE, Gemmill RM, Hirsch FR, Coldren CD, Hedman K, Ravdel L, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res 2006; 66:944-50; PMID:16424029; http://dx.doi.org/10.1158/0008-5472.CAN-05-1988.
44. Singh RP, Sharma G, Dhanalakshmi S, Agarwal C, Agarwal R. Suppression of advanced human prostate tumor growth in athymic mice by silibinin feeding is associated with reduced cell proliferation, increased apoptosis, and inhibition of angiogenesis. Cancer Epidemiol Biomarkers Prev 2003; 12:933-9; PMID:14504208.