Reactivation of MASPIN in non-small cell lung carcinoma (NSCLC) cells by artificial transcription factors (ATFs)

Epigenetics

Volumn 6, Issue 2, 2011, Pages 224-235

  Beltran, Adriana S ^a   Blancafort, Pilar ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Artificial transcription factor (ATF); DNA methylation; Epigenetics; Lung cancer; MASPIN; Zinc fingers

Indexed keywords

ARTIFICIAL TRANSCRIPTION FACTOR; MASPIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; DEMETHYLATION; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; HUMAN; HUMAN CELL; LUNG SMALL CELL CANCER; MASPIN GENE; METASTASIS; MOUSE; NONHUMAN; NUDE MOUSE; PHENOTYPE; PROMOTER REGION; PROTEIN DOMAIN; TUMOR SUPPRESSOR GENE;

MUS MUSCULUS;

EID: 79951499884     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.2.13700     Document Type: Article

References (62)

1. Zardo G, Fazi F, Travaglini L, Nervi C. Dynamic and reversibility of heterochromatic gene silencing in human disease. Cell Res 2005; 15:679-90.
2. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 2006; 6:107-16.
3. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 2008; 18:350-9.
4. Collingwood TN, Urnov FD, Wolffe AP. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription. J Mol Endocrinol 1999; 23:255-75.
5. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007; 39:237-42.
6. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the reexpression of genes silenced in cancer. Nat Genet 1999; 21:103-7.
7. Oshiro MM, Watts GS, Wozniak RJ, Junk DJ, Munoz-Rodriguez JL, Domann FE, et al. Mutant p53 and aberrant cytosine methylation cooperate to silence gene expression. Oncogene 2003; 22:3624-34.
8. Zou Z, Anisowicz A, Hendrix MJ, Thor A, Neveu M, Sheng S, et al. Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 1994; 263:526-9.
9. Zou Z, Gao C, Nagaich AK, Connell T, Saito S, Moul JW, et al. p53 regulates the expression of the tumor suppressor gene maspin. J Biol Chem 2000; 275:6051-4.
10. Zhang M, Magit D, Sager R. Expression of maspin in prostate cells is regulated by a positive ets element and a negative hormonal responsive element site recognized by androgen receptor. Proc Natl Acad Sci USA 1997; 94:5673-8.
11. Khalkhali-Ellis Z, Christian AL, Kirschmann DA, Edwards EM, Rezaie-Thompson M, Vasef MA, et al. Regulating the tumor suppressor gene maspin in breast cancer cells: a potential mechanism for the anticancer properties of tamoxifen. Clin Cancer Res 2004; 10:449-54.
12. Domann FE, Rice JC, Hendrix MJ, Futscher BW. Epigenetic silencing of maspin gene expression in human breast cancers. Int J Cancer 2000; 85:805-10.
13. Futscher BW, Oshiro MM, Wozniak RJ, Holtan N, Hanigan CL, Duan H, et al. Role for DNA methylation in the control of cell type specific maspin expression. Nat Genet 2002; 31:175-9.
14. Sager R, Sheng S, Pemberton P, Hendrix MJ. Maspin. A tumor suppressing serpin. Adv Exp Med Biol 1997; 425:77-88.
15. Zhang M, Volpert O, Shi YH, Bouck N. Maspin is an angiogenesis inhibitor. Nat Med 2000; 6:196-9.
16. Seftor RE, Seftor EA, Sheng S, Pemberton PA, Sager R, Hendrix MJ. Maspin suppresses the invasive phenotype of human breast carcinoma. Cancer Res 1998; 58:5681-5.
17. Sheng S, Carey J, Seftor EA, Dias L, Hendrix MJ, Sager R. Maspin acts at cell membrane to inhibit invasion and motility of mammary and prostatic cancer cells. Proc Natl Acad Sci USA 1996; 93:11669-74.
18. Zhang M, Shi Y, Magit D, Furth PA, Sager R. Reduced mammary tumor progression in WAP-TAg/WAPmaspin bitransgenic mice. Oncogene 2000; 19:6053-8.
19. Shi HY, Liang R, Templeton NS, Zhang M. Inhibition of breast tumor progression by systemic delivery of the maspin gene in a syngeneic tumor model. Mol Ther 2002; 5:755-61.
20. Cher ML, Biliran HR, Bhagat S, Meng Y, Che M, Lockett J, et al. Maspin expression inhibits osteolysis, tumor growth and angiogenesis in a model of prostate cancer bone metastasis. Proc Natl Acad Sci USA 2003; 100:7847-52.
21. Watanabe M, Nasu Y, Kashiwakura Y, Kusumi N, Tamayose K, Nagai A, et al. Adeno-associated virus 2-mediated intratumoral prostate cancer gene therapy: long-term maspin expression efficiently suppresses tumor growth. Hum Gene Ther 2005; 16:699-710.
22. Sharma G, Mirza S, Parshad R, Srivastava A, Gupta SD, Pandya P, et al. Clinical significance of Maspin promoter methylation and loss of its protein expression in invasive ductal breast carcinoma: correlation with VEGF-A and MTA1 expression. Tumour Biol 2010.
23. Maass N, Ho Jo T, Rosel F, Ikeda T, Jonat W, Nagasaki K. Downregulation of the tumor suppressor gene maspin in breast carcinoma is associated with a higher risk of distant metastasis. Clin Biochem 2001; 34:303-7.
24. Machtens S, Serth J, Bokemeyer C, Bathke W, Minssen A, Kollmannsberger C, et al. Expression of the p53 and Maspin protein in primary prostate cancer: correlation with clinical features. Int J Cancer 2001; 95:337-42.
25. Bettstetter M, Woenckhaus M, Wild PJ, Rummele P, Blaszyk H, Hartmann A, et al. Elevated nuclear maspin expression is associated with microsatellite instability and high tumour grade in colorectal cancer. J Pathol 2005; 205:606-14.
26. Nakagawa M, Katakura H, Adachi M, Takenaka K, Yanagihara K, Otake Y, et al. Maspin expression and its clinical significance in non-small cell lung cancer. Ann Surg Oncol 2006; 13:1517-23.
27. Vereecken P, Reynaert S, Lalmand MC, Zouaoui-Boudjeltia K, Heenen M, Van Den Heule B, et al. Decreased immunoreactive maspin expression in intermediate thickness and thick primary melanoma lesions. J Int Med Res 2006; 34:52-7.
28. Katakura H, Takenaka K, Nakagawa M, Sonobe M, Adachi M, Ito S, et al. Maspin gene expression is a significant prognostic factor in resected non-small cell lung cancer (NSCLC). Maspin in NSCLC. Lung Cancer 2006; 51:323-8.
29. Takanami I, Abiko T, Koizumi S. Expression of maspin in non-small-cell lung cancer: correlation with clinical features. Clin Lung Cancer 2008; 9:361-6.
30. Kim S, Han J, Kim J, Park C. Maspin expression is transactivated by p63 and is critical for the modulation of lung cancer progression. Cancer Res 2004; 64:6900-5.
31. Yatabe Y, Mitsudomi T, Takahashi T. Maspin expression in normal lung and non-small-cell lung cancers: cellular property-associated expression under the control of promoter DNA methylation. Oncogene 2004; 23:4041-9.
32. Hurtubise A, Momparler RL. Evaluation of antineoplastic action of 5-aza-2'-deoxycytidine (Dacogen) and docetaxel (Taxotere) on human breast, lung and prostate carcinoma cell lines. Anticancer Drugs 2004; 15:161-7.
33. Beltran A, Parikh S, Liu Y, Cuevas BD, Johnson GL, Futscher BW, et al. Re-activation of a dormant tumor suppressor gene maspin by designed transcription factors. Oncogene 2007; 26:2791-8.
34. Zhang W, Shi HY, Zhang M. Maspin overexpression modulates tumor cell apoptosis through the regulation of Bcl-2 family proteins. BMC Cancer 2005; 5:50.
35. Nam E, Park C. Maspin suppresses survival of lung cancer cells through modulation of Akt pathway. Cancer Res Treat 2010; 42:42-7.
36. Chen EI, Florens L, Axelrod FT, Monosov E, Barbas CF, Yates JR, et al. Maspin alters the carcinoma proteome. FASEB J 2005; 19:1123-4.
37. Bailey CM, Hendrix MJ. IRF6 in development and disease: a mediator of quiescence and differentiation. Cell Cycle 2008; 7:1925-30.
38. Beerli RR, Segal DJ, Dreier B, Barbas CF. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc Natl Acad Sci USA 1998; 95:14628-33.
39. Beltran AS, Sun X, Lizardi PM, Blancafort P. Reprogramming epigenetic silencing: artificial transcription factors synergize with chromatin remodeling drugs to reactivate the tumor suppressor mammary serine protease inhibitor. Mol Cancer Ther 2008; 7:1080-90.
40. Bailey CM, Khalkhali-Ellis Z, Seftor EA, Hendrix MJ. Biological functions of maspin. J Cell Physiol 2006; 209:617-24.
41. Wetterwald A, van der Pluijm G, Que I, Sijmons B, Buijs J, Karperien M, et al. Optical imaging of cancer metastasis to bone marrow: a mouse model of minimal residual disease. Am J Pathol 2002; 160:1143-53.
42. Nakashima M, Ohike N, Nagasaki K, Adachi M, Morohoshi T. Prognostic significance of the maspin tumor suppressor gene in pulmonary adenocarcinoma. J Cancer Res Clin Oncol 2004; 130:475-9.
43. Hirai K, Koizumi K, Haraguchi S, Hirata T, Mikami I, Fukushima M, et al. Prognostic significance of the tumor suppressor gene maspin in non-small cell lung cancer. Ann Thorac Surg 2005; 79:248-53.
44. Bircan A, Bircan S, Kapucuoglu N, Songur N, Ozturk O, Akkaya A. Maspin, VEGF and p53 expression in small biopsies of primary advanced lung cancer and relationship with clinicopathologic parameters. Pathol Oncol Res 2010.
45. Woenckhaus M, Bubendorf L, Dalquen P, Foerster J, Blaszyk H, Mirlacher M, et al. Nuclear and cytoplasmic Maspin expression in primary non-small cell lung cancer. J Clin Pathol 2007; 60:483-6.
46. Vaissiere T, Sawan C, Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res 2008; 659:40-8.
47. Tumbar T, Sudlow G, Belmont AS. Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J Cell Biol 1999; 145:1341-54.
48. Herrera FJ, Triezenberg SJ. VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J Virol 2004; 78:9689-96.
49. Mittler G, Stuhler T, Santolin L, Uhlmann T, Kremmer E, Lottspeich F, et al. A novel docking site on Mediator is critical for activation by VP16 in mammalian cells. EMBO J 2003; 22:6494-504.
50. Yang F, DeBeaumont R, Zhou S, Naar AM. The activator-recruited co-factor/Mediator coactivator subunit ARC92 is a functionally important target of the VP16 transcriptional activator. Proc Natl Acad Sci USA 2004; 101:2339-44.
51. Wozniak RJ, Klimecki WT, Lau SS, Feinstein Y, Futscher BW. 5-Aza-2'-deoxycytidine-mediated reductions in G9A histone methyltransferase and histone H3K9 dimethylation levels are linked to tumor suppressor gene reactivation. Oncogene 2007; 26:77-90.
52. Jiang N, Meng Y, Zhang S, Mensah-Osman E, Sheng S. Maspin sensitizes breast carcinoma cells to induced apoptosis. Oncogene 2002; 21:4089-98.
53. Liu J, Yin S, Reddy N, Spencer C, Sheng S. Bax mediates the apoptosis-sensitizing effect of maspin. Cancer Res 2004; 64:1703-11.
54. Li Z, Shi HY, Zhang M. Targeted expression of maspin in tumor vasculatures induces endothelial cell apoptosis. Oncogene 2005; 24:2008-19.
55. Li X, Yin S, Meng Y, Sakr W, Sheng S. Endogenous inhibition of histone deacetylase 1 by tumor-suppressive maspin. Cancer Res 2006; 66:9323-9.
56. Kakihana M, Ohira T, Chan D, Webster RB, Kato H, Drabkin HA, et al. Induction of E-cadherin in lung cancer and interaction with growth suppression by histone deacetylase inhibition. J Thorac Oncol 2009; 4:1455-65.
57. Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 2004; 24:306-19.
58. Ben Shachar B, Feldstein O, Hacohen D, Ginsberg D. The tumor suppressor maspin mediates E2F1-induced sensitivity of cancer cells to chemotherapy. Mol Cancer Res 2010; 8:363-72.
59. Torchilin VP. Cell penetrating peptide-modified pharmaceutical nanocarriers for intracellular drug and gene delivery. Biopolymers 2008; 90:604-10.
60. Henning P, Andersson KM, Frykholm K, Ali A, Magnusson MK, Nygren PA, et al. Tumor cell targeted gene delivery by adenovirus 5 vectors carrying knobless fibers with antibody-binding domains. Gene Ther 2005; 12:211-24.
61. Harvey TJ, Burdon D, Steele L, Ingram N, Hall GD, Selby PJ, et al. Retargeted adenoviral cancer gene therapy for tumour cells overexpressing epidermal growth factor receptor or urokinase-type plasminogen activator receptor. Gene Ther 2010; 17:1000-10.
62. Klug A. Towards therapeutic applications of engineered zinc finger proteins. FEBS Lett 2005; 579:892-4.