Synergistic antineoplastic effect of DLC1 tumor suppressor protein and histone deacetylase inhibitor, suberoylanilide hydroxamic acid (SAHA), on prostate and liver cancer cells: Perspectives for therapeutics

International Journal of Oncology

Volumn 36, Issue 4, 2010, Pages 999-1005

  Zhou, Xiaoling ^a   Yang, Xu Yu ^a   Popescu, Nicholas C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Cell proliferation; DLC1; Liver cancer cells; Prostate cancer cells; SAHA; Tumor suppressor gene; Tumorigenicity

Indexed keywords

ADENOVIRUS VECTOR; DELETED IN LIVER CANCER 1 PROTEIN; DIMETHYL SULFOXIDE; HISTONE DEACETYLASE INHIBITOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VORINOSTAT;

ANCHORAGE INDEPENDENT GROWTH; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL MIGRATION; CONTROLLED STUDY; DEACETYLATION; DRUG POTENTIATION; EPIGENETICS; GENE INACTIVATION; GENE SILENCING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CANCER; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN METHYLATION;

ADENOVIRIDAE; APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; ENZYME ACTIVATION; GENE THERAPY; GENETIC VECTORS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LIVER NEOPLASMS; MALE; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; RNA, MESSENGER; TIME FACTORS; TRANSDUCTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 77749342644     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000580     Document Type: Article

References (39)

1. Yuan BZ, Miller MJ, Keck CL, Zimonjic D, Thorgeirsson SS and Popescu NC: Cloning, characterization, and chromosomal localization of a gene frequently deleted in human liver cancer (DLC-1) homologous to rat RhoGAP. Cancer Res 58: 2196-2199, 1998.
2. Xue W, Krasnitz A, Lucito R, Sordella R, Vanaelst L, Cordon-Cardo C, Singer S, Kuehnel F, Wigler M, Powers S, Zender L and Lowe SW: DLC-1 is a chromosome 8p tumor suppressor whose loss promotes hepatocellular carcinoma. Genes Dev 22: 1439-1444, 2008.
3. Durkin ME, Yuan BZ, Zhou X, Zimonjic DB, Lowy DR, Thorgeirsson SS and Popescu NC: DLC-1: a Rho GTPaseactivating protein and tumour suppressor. J Cell Mol Med 11: 1185-1207, 2007.
4. Sahai E and Marshall CJ: RHO-GTPases and cancer. Nat Rev Cancer 2: 133-142, 2002.
5. Liao YC, Shih YP and Lo SH: Mutations in the focal adhesion targeting region of deleted in liver cancer-1 attenuate their expression and function. Cancer Res 68: 7718-7722, 2008.
6. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, Calhoun ES, Kamiyama M, Walter K, Nikolskaya T, Nikolsky Y, Hartigan J, Smith DR, Hidalgo M, Leach SD, Klein AP, Jaffee EM, Goggins M, Maitra A, Iacobuzio-Donahue C, Eshleman JR, Kern SE, Hruban RH, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE and Kinzler KW: Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321: 1801-1806, 2008.
7. Pihur V, Datta S and Datta S: Finding common genes in multiple cancer types through meta-analysis of microarray experiments: a rank aggregation approach. Genomics 92: 400-403, 2008.
8. Guan M, Zhou X, Soulitzis N, Spandidos DA and Popescu NC: Aberrant methylation and deacetylation of deleted in liver cancer-1 gene in prostate cancer: potential clinical applications. Clin Cancer Res 12: 1412-1419, 2006.
9. Guan M, Tripathi V, Zhou X and Popescu NC: Adenovirus-mediated restoration of expression of the tumor suppressor gene DLC-1 inhibits the proliferation and tumorigenicity of aggressive, androgen-independent human prostate cancer cell lines: prospects for gene therapy. Cancer Gene Ther 15: 371-381, 2008.
10. Xu W, Ngo L, Perez G, Dokmanovic M and Marks PA: Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc Natl Acad Sci USA 103: 15540-15545, 2006.
11. Butler LM, Agus DB, Scher HI, Higgins B, Rose A, Cordon-Cardo C, Thaler HT, Rifkind RA, Marks PA and Richon VM: Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res 60: 5165-5170, 2000.
12. Yuan BZ, Durkin ME and Popescu NC: Promoter hypermethylation of DLC-1, a candidate tumor suppressor gene, in several common human cancers. Cancer Genet Cytogenet 140: 113-117, 2003.
13. Kim TY, Kim IS, Jong HS, Lee JW, Kim TY, Jung M and Bang YJ: Transcriptional induction of DLC-1 gene through Sp1 sites by histone deacetylase inhibitors in gastric cancer cells. Exp Mol Med 40: 639-646, 2008.
14. Zhou X, Thorgeirsson SS and Popescu NC: Restoration of DLC-1 gene expression induces apoptosis and inhibits both cell growth and tumorigenicity in human hepatocellular carcinoma cells. Oncogene 23: 1308-1313, 2004.
15. Carew JS, Giles FJ and Nawrocki ST: Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 269: 7-17, 2008.
16. Bishop JM: The molecular genetics of cancer. Science 235: 305-311, 1987.
17. Hanahan D and Weinberg RA: The hallmarks of cancer. Cell 100: 57-70, 2000.
18. Jones PA and Baylin SB: The epigenomics of cancer. Cell 128: 683-692, 2007.
19. Herman JG: Hypermethylation of tumor suppressor genes in cancer. Semin Cancer Biol 9: 359-367, 1999.
20. Palii SS and Robertson KD: Epigenetic control of tumor suppression. Crit Rev Eukaryot Gene Expr 17: 295-316, 2007.
21. Botrugno OA, Santoro F and Minucci S: Histone deacetylase inhibitors as a new weapon in the arsenal of differentiation therapies of cancer. Cancer Lett 280: 134-144, 2009.
22. Yoo CB, Cheng JC and Jones PA: Zebularine: a new drug for epigenetic therapy. Biochem Soc Trans 32: 910-912, 2004.
23. Minucci S and Pelicci PG: Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51, 2006.
24. Batty N, Malouf GG and Issa JP: Histone deacetylase inhibitors as anti-neoplastic agents. Cancer Lett 280: 192-200, 2009.
25. Richon VM, Garcia-Vargas J and Hardwick JS: Development of vorinostat: current applications and future perspectives for cancer therapy. Cancer Lett 280: 201-210, 2009.
26. Kim TY, Jong HS, Song SH, Dimtchev A, Jeong SJ, Lee JW, Kim TY, Kim NK, Jung M and Bang YJ: Transcriptional silencing of the DLC-1 tumor suppressor gene by epigenetic mechanism in gastric cancer cells. Oncogene 22: 3943-3951, 2003.
27. Song YF, Xu R, Zhang XH, Chen BB, Chen Q, Chen YM and Xie Y: High-frequency promoter hypermethylation of the deleted in liver cancer-1 gene in multiple myeloma. J Clin Pathol 59: 947-951, 2006.
28. Ullmannova-Benson V, Guan M, Zhou X, Tripathi V, Yang XY, Zimonjic DB and Popescu NC: DLC-1 tumor suppressor gene inhibits migration and invasion of multiple myeloma cells through RhoA GTPase pathway. Leukemia 23: 383-390, 2009.
29. Palmieri D, Lockman PR, Thomas FC, Hua E, Herring J, Hargrave E, Johnson M, Flores N, Qian Y, Vega-Valle E, Taskar KS, Rudraraju V, Mittapalli RK, Gaasch JA, Bohn KA, Thorsheim HR, Liewehr DJ, Davis S, Reilly JF, Walker R, Bronder JL, Feigenbaum L, Steinberg SM, Camphausen K, Meltzer PS, Richon VM, Smith QR and Steeg PS: Vorinostat inhibits brain metastatic colonization in a model of triple-negative breast cancer and induces DNA double-strand breaks. Clin Cancer Res (In press).
30. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA and Massague J: A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537-549, 2003.
31. Goodison S, Yuan J, Sloan D, Kim R, Li C, Popescu NC and Urquidi V: The RhoGAP protein DLC-1 functions as a metastasis suppressor in breast cancer cells. Cancer Res 65: 6042-6053, 2005.
32. Yuan BZ, Zhou X, Durkin ME, Zimonjic DB, Gumundsdottir K, Eyfjord JE, Thorgeirsson SS and Popescu NC: DLC-1 gene inhibits human breast cancer cell growth and in vivo tumorigenicity. Oncogene 22: 445-450, 2003.
33. Yuan B-Z, Jefferson AM, Baldwin KT, Thorgeirsson SS, Popescu NC and Reynolds SH: DLC-1 operates as a tumor suppressor gene in human and non-small cell lung carcinomas. Oncogene 23: 1405-1411, 2004.
34. Nolan L, Johnson PW, Ganesan A, Packham G and Crabb SJ: Will histone deacetylase inhibitors require combination with other agents to fulfill their therapeutic potential? Br J Cancer 99: 689-694, 2008.
35. Cheng JC, Yoo CB, Weisenberger DJ, Chuang J, Wozniak C, Liang G, Marquez VE, Greer S, Orntoft TF, Thykjaer T and Jones PA: Preferential response of cancer cells to zebularine. Cancer Cell 6: 151-158, 2004.
36. Lahoz A and Hall A: DLC1: a significant GAP in the cancer genome. Genes Dev 22: 1724-1730, 2008.
37. Cameron EE, Bachman KE, Myohanen S, Herman JG and Baylin SB: Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21: 103-107, 1999.
38. Maass N, Biallek M, Rosel F, Schem C, Ohike N, Zhang M, Jonat W and Nagasaki K: Hypermethylation and histone deacetylation lead to silencing of the maspin gene in human breast cancer. Biochem Biophys Res Commun 297: 125-128, 2002.
39. Gore SD, Baylin S, Sugar E, Carraway H, Miller CB, Carducci M, Grever M, Galm O, Dauses T, Karp JE, Rudek MA, Zhao M, Smith BD, Manning J, Jiemjit A, Dover G, Mays A, Zwiebel J, Murgo A, Weng LJ and Herman JG: Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res 66: 6361-6369, 2006.