Histone deacetylase (HDAC) 10 suppresses cervical cancer metastasis through inhibition of matrix metalloproteinase (MMP) 2 and 9 expression

Journal of Biological Chemistry

Volumn 288, Issue 39, 2013, Pages 28021-28033

  Song, Chenlin ^a   Zhu, Songcheng ^a   Wu, Chuanyue ^b   Kang, Jiuhong ^a  

^a TONGJI UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERVICAL CANCERS; CLINICAL TREATMENTS; HDAC INHIBITORS; HISTONE DEACETYLASES; MATRIX METALLOPROTEINASES; TUMOR SUPPRESSORS;

BIOCHEMISTRY; BIOLOGY;

PATHOLOGY;

GELATINASE A; GELATINASE B; HISTONE DEACETYLASE; HISTONE DEACETYLASE 10; HISTONE H3; HISTONE H4; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HELA CELL; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; METASTASIS INHIBITION; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA;

CELL INVASION; CELL MIGRATION; HISTONE DEACETYLASE; MATRIX METALLOPROTEINASE (MMP); METASTASIS;

ADULT; AGED; ANIMALS; CELL MOVEMENT; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASES; HUMANS; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; NEOPLASM METASTASIS; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; RNA INTERFERENCE; UTERINE CERVICAL NEOPLASMS;

EID: 84884784393     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498758     Document Type: Article

References (48)

1. The Merck Manual Home Health Handbook (2013) Cervical Cancer, www.merckmanuals.com/home/womens-health-issues/cancers-of-the-female- reproductive-system/cervical-cancer.html
2. Armenian Medical Network (2013) Cervical Cancer, www.health.am/ cr/cervical-cancer/
3. Boothello, R. (2011) Matrix Metalloproteinases: Its Implications in Cardiovascular Disorders, pharmaxchange.info/press/2011/11/ matrixmetalloproteinases-its-implications-in-cardiovascular-disorders/
4. Wang, X. X., Cheng, Q., Zhang, S. N., Qian, H. Y., Wu, J. X., Tian, H., Pei, D. S., and Zheng, J. N. (May 22, 2013) PAK5-Egr1-MMP2 signaling controls the migration and invasion in breast cancer cell. Tumour Biol. 10.1007/s13277-013-0824-x
5. Yu, G., Li, H., Wang, X., Wu, T., Zhu, J., Huang, S., Wan, Y., and Tang, J. (2013) MicroRNA-19a targets tissue factor to inhibit colon cancer cells migration and invasion. Mol. Cell. Biochem. 380, 239-247
6. Yang, Y., Jiao, L., Hou, J., Xu, C., Wang, L., Yu, Y., Li, Y., Yang, C., Wang, X., and Sun, Y. (2013) Dishevelled-2 silencing reduces androgen-dependent prostate tumor cell proliferation and migration and expression of Wnt-3a and matrix metalloproteinases. Mol. Biol. Rep. 40, 4241-4250
7. Bérubé, M., Deschambeault, A., Boucher, M., Germain, L., Petitclerc, E., and Guérin, S. L. (2005) MMP-2 expression in uveal melanoma: differential activation status dictated by the cellular environment. Mol. Vis. 11, 1101-1111
8. Di Nezza, L. A., Misajon, A., Zhang, J., Jobling, T., Quinn, M. A., Ostör, A. G., Nie, G., Lopata, A., and Salamonsen, L. A. (2002) Presence of active gelatinases in endometrial carcinoma and correlation of matrix metalloproteinase expression with increasing tumor grade and invasion. Cancer 94, 1466-1475
9. Sato, T., Sakai, T., Noguchi, Y., Takita, M., Hirakawa, S., and Ito, A. (2004) Tumor-stromal cell contact promotes invasion of human uterine cervical carcinoma cells by augmenting the expression and activation of stromal matrix metalloproteinases. Gynecol. Oncol. 92, 47-56
10. Roomi, M. W., Monterrey, J. C., Kalinovsky, T., Rath, M., and Niedzwiecki, A. (2010) In vitro modulation of MMP-2 and MMP-9 in human cervical and ovarian cancer cell lines by cytokines, inducers and inhibitors. Oncol. Rep. 23, 605-614
11. Boeker, K. H., Haberkorn, C. I., Michels, D., Flemming, P., Manns, M. P., and Lichtinghagen, R. (2002) Diagnostic potential of circulating TIMP-1 and MMP-2 as markers of liver fibrosis in patients with chronic hepatitis C. Clin. Chim. Acta 316, 71-81
12. Branca, M., Ciotti, M., Giorgi, C., Santini, D., Di Bonito, L., Costa, S., Benedetto, A., Bonifacio, D., Di Bonito, P., Paba, P., Accardi, L., Syrjänen, S., Favalli, C., Syrjänen, K., and HPV-PathogenISS Study Group (2006) Matrix metalloproteinase-2 (MMP-2) and its tissue inhibitor (TIMP-2) are prognostic factors in cervical cancer, related to invasive disease but not to high-risk human papillomavirus (HPV) or virus persistence after treatment of CIN. Anticancer Res. 26, 1543-1556
13. Vasala, K. (2008) Matrix metalloproteinase MMP-2 and MMP-9 and their inhibitors TIMP-1 And TIMP-2 in bladder carcinoma. Acta Univ. Oul. D 983
14. Weichert, W. (2009) HDAC expression and clinical prognosis in human malignancies. Cancer Lett. 280, 168-176
15. Sengupta, N., and Seto, E. (2004) Regulation of histone deacetylase activities. J. Cell. Biochem. 93, 57-67
16. Venkataramani, V., Rossner, C., Iffland, L., Schweyer, S., Tamboli, I. Y., Walter, J., Wirths, O., and Bayer, T. A. (2010) Histone deacetylase inhibitor valproic acid inhibits cancer cell proliferation via down-regulation of the Alzheimer amyloid precursor protein. J. Biol. Chem. 285, 10678-10689
17. Zhang, L., Wang, G., Wang, L., Song, C., Leng, Y., Wang, X., and Kang, J. (2012) VPA inhibits breast cancer cell migration by specifically targeting HDAC2 and down-regulating Survivin. Mol. Cell. Biochem. 361, 39-45
18. Ellis, L., Hammers, H., and Pili, R. (2009) Targeting tumor angiogenesis with histone deacetylase inhibitors. Cancer Lett. 280, 145-153
19. Michaelis, M., Michaelis, U. R., Fleming, I., Suhan, T., Cinatl, J., Blaheta, R. A., Hoffmann, K., Kotchetkov, R., Busse, R., Nau, H., and Cinatl, J., Jr. (2004) Valproic acid inhibits angiogenesis in vitro and in vivo. Mol. Pharmacol. 65, 520-527
20. Witt, O., Deubzer, H. E., Milde, T., and Oehme, I. (2009) HDAC family: what are the cancer relevant targets? Cancer Lett. 277, 8-21
21. Tong, J. J., Liu, J., Bertos, N. R., and Yang, X. J. (2002) Identification of HDAC10, a novel class II human histone deacetylase containing a leucinerich domain. Nucleic Acids Res. 30, 1114-1123
22. Lai, I. L., Lin, T. P., Yao, Y. L., Lin, C. Y., Hsieh, M. J., and Yang, W. M. (2010) Histone deacetylase 10 relieves repression on the melanogenic program by maintaining the deacetylation status of repressors. J. Biol. Chem. 285, 7187-7196
23. Lee, J. H., Jeong, E. G., Choi, M. C., Kim, S. H., Park, J. H., Song, S. H., Park, J., Bang, Y. J., and Kim, T. Y. (2010) Inhibition of histone deacetylase 10 induces thioredoxin-interacting protein and causes accumulation of reactive oxygen species in SNU-620 human gastric cancer cells. Mol. Cells 30, 107-112
24. Kotian, S., Liyanarachchi, S., Zelent, A., and Parvin, J. D. (2011) Histone deacetylases 9 and 10 are required for homologous recombination. J. Biol. Chem. 286, 7722-7726
25. Im, H., Grass, J. A., Johnson, K. D., Boyer, M. E., Wu, J., and Bresnick, E. H. (2004) Measurement of protein-DNA interactions in vivo by chromatin immunoprecipitation. Methods Mol. Biol. 284, 129-146
26. Kato, Y., Yamashita, T., and Ishikawa, M. (2002) Relationship between expression of matrix metalloproteinase-2 and matrix metalloproteinase-9 and invasion ability of cervical cancer cells. Oncol. Rep. 9, 565-569
27. Chernov, A. V., Sounni, N. E., Remacle, A. G., and Strongin, A. Y. (2009) Epigenetic control of the invasion-promoting MT1-MMP/MMP-2/ TIMP-2 axis in cancer cells. J. Biol. Chem. 284, 12727-12734
28. Kim, Y., and Jeoung, D. (2009) The cancer/testis antigen CAGE induces MMP-2 through the activation of NF-κB and AP-1. BMB Rep. 42, 758-763
29. Lee, C. W., Lin, C. C., Lin, W. N., Liang, K. C., Luo, S. F., Wu, C. B., Wang, S. W., and Yang, C. M. (2007) TNF-α induces MMP-9 expression via activation of Src/EGFR, PDGFR/PI3K/Akt cascade and promotion of NF-κB/p300 binding in human tracheal smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L799-L812
30. Lin, L. F., Chuang, C. H., Li, C. F., Liao, C. C., Cheng, C. P., Cheng, T. L., Shen, M. R., Tseng, J. T., Chang, W. C., and Lee, W. H. (2010) ZBRK1 acts as a metastatic suppressor by directly regulatingMMP9in cervical cancer. Cancer Res. 70, 192-201
31. Satpathy, M., Shao, M., Emerson, R., Donner, D. B., and Matei, D. (2009) Tissue transglutaminase regulates matrix metalloproteinase-2 in ovarian cancer by modulating cAMP-response element-binding protein activity. J. Biol. Chem. 284, 15390-15399
32. Song, H., Ki, S. H., Kim, S. G., and Moon, A. (2006) Activating transcription factor 2 mediates matrix metalloproteinase-2 transcriptional activation induced by p38 in breast epithelial cells. Cancer Res. 66, 10487-10496
33. Takahra, T., Smart, D. E., Oakley, F., and Mann, D. A. (2004) Induction of myofibroblast MMP-9 transcription in three-dimensional collagen I gel cultures: regulation by NF-κB, AP-1 and Sp1. Int. J. Biochem. Cell Biol. 36, 353-363
34. Yoshizaki, T., Sato, H., Furukawa, M., and Pagano, J. S. (1998) The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein. Proc. Natl. Acad. Sci. U.S.A. 95, 3621-3626
35. Reichert, N., Choukrallah, M. A., and Matthias, P. (2012) Multiple roles of class I HDACs in proliferation, differentiation, and development. Cell. Mol. Life Sci. 69, 2173-2187
36. Hellebrekers, D. M., Griffioen, A. W., and van Engeland, M. (2007) Dual targeting of epigenetic therapy in cancer. Biochim. Biophys. Acta 1775, 76-91
37. Glaser, K. B., Li, J., Staver, M. J., Wei, R. Q., Albert, D. H., and Davidsen, S. K. (2003) Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem. Biophys. Res. Commun. 310, 529-536
38. Valenzuela-FernAndez, A., Cabrero, J. R., Serrador, J. M., and SAnchez-Madrid, F. (2008) HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol. 18, 291-297
39. Zhang, X., Yuan, Z., Zhang, Y., Yong, S., Salas-Burgos, A., Koomen, J., Olashaw, N., Parsons, J. T., Yang, X. J., Dent, S. R., Yao, T. P., Lane, W. S., and Seto, E. (2007) HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol. Cell 27, 197-213
40. Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X. F., and Yao, T. P. (2002) HDAC6 is a microtubuleassociated deacetylase. Nature 417, 455-458
41. Osada, H., Tatematsu, Y., Saito, H., Yatabe, Y., Mitsudomi, T., and Takahashi, T. (2004) Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int. J. Cancer 112, 26-32
42. Kristensen, L. S., Nielsen, H. M., and Hansen, L. L. (2009) Epigenetics and cancer treatment. Eur. J. Pharmacol. 625, 131-142
43. Cress, W. D., and Seto, E. (2000) Histone deacetylases, transcriptional control, and cancer. J. Cell. Physiol. 184, 1-16
44. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260
45. Armstrong, E. P. (2010) Prophylaxis of cervical cancer and related cervical disease: a review of the cost-effectiveness of vaccination against oncogenic HPV types. J. Manag. Care Pharm. 16, 217-230
46. Asha Nair, S., Karunagaran, D., Nair, M. B., and Sudhakaran, P. R. (2003) Changes in matrix metalloproteinases and their endogenous inhibitors during tumor progression in the uterine cervix. J. Cancer Res. Clin. Oncol. 129, 123-131
47. Zhou, C. Y, Yao, J. F., and Chen, X. D. (2002) Expression of matrix metalloproteinase-2, 9 and their inhibitor-TIMP 1, 2 in human squamous cell carcinoma of uterine cervix. Ai Zheng 21, 735-739
48. Xu, P., Cai, H., and Wang, D. (2009) The significance of matrix metalloproteinase-2 (MMP-2) and matrix metalloproteinase-9 (MMP-9) in the course of development of cervical carcinoma. Med. J. West China 21, 2040-2042