Human family with sequence similarity 60 member A (FAM60A) protein: A new subunit of the Sin3 deacetylase complex

Molecular and Cellular Proteomics

Volumn 11, Issue 12, 2012, Pages 1815-1828

  Smith, Karen T ^a   Sardiu, Mihaela E ^a   Martin Brown, Skylar A ^a   Seidel, Chris ^a   Mushegian, Arcady ^a   Egidy, Rhonda ^a   Florens, Laurence ^a   Washburn, Michael P ^a,b   Workman, Jerry L ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b MISSOURI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE; PROTEIN A; PROTEIN FAMILY WITH SEQUENCE SIMILARITY 60 MEMBER A; UNCLASSIFIED DRUG;

ADHESION; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; CHROMOSOME 12P; CONTROLLED STUDY; ENZYME SUBUNIT; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETIC CODE; HUMAN; HUMAN CELL; MIGRATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

CELL LINE; CELL MOVEMENT; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELLS; HEP G2 CELLS; HISTONE DEACETYLASE INHIBITORS; HOMEODOMAIN PROTEINS; HUMANS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, PROTEIN; SIN3 HISTONE DEACETYLASE AND COREPRESSOR COMPLEX; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS;

EID: 84870707603     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.020255     Document Type: Article

References (68)

1. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
2. Witt, O., Deubzer, H. E., Milde, T., and Oehme, I. (2009) HDAC family: What are the cancer relevant targets? Cancer Letts. 277, 8-21
3. Yang, X. J., and Seto, E. (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206-218
4. Gregoretti, I. V., Lee, Y. M., and Goodson, H. V. (2004) Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338, 17-31 (Pubitemid 38429783)
5. David, G., Grandinetti, K. B., Finnerty, P. M., Simpson, N., Chu, G. C., and Depinho, R. A. (2008) Specific requirement of the chromatin modifier mSin3B in cell cycle exit and cellular differentiation. Proc. Natl. Acad. Sci. U. S. A. 105, 4168-4172 (Pubitemid 351754352)
6. Pile, L. A., Schlag, E. M., and Wassarman, D. A. (2002) The SIN3/RPD3 deacetylase complex is essential for G(2) phase cell cycle progression and regulation of SMRTER corepressor levels. Mol. Cell. Biol. 22, 4965-4976 (Pubitemid 34700689)
7. Suryadinata, R., Sadowski, M., Steel, R., and Sarcevic, B. (2011) Cyclin-dependent kinase-mediated phosphorylation of RBP1 and pRb promotes their dissociation to mediate release of the SAP30.mSin3.HDAC transcriptional repressor complex. J. Biol. Chem. 286, 5108-5118
8. Lai, A., Kennedy, B. K., Barbie, D. A., Bertos, N. R., Yang, X. J., Theberge, M. C., Tsai, S. C., Seto, E., Zhang, Y., Kuzmichev, A., Lane, W. S., Reinberg, D., Harlow, E., and Branton, P. E. (2001) RBP1 recruits the mSIN3-histone deacetylase complex to the pocket of retinoblastoma tumor suppressor family proteins found in limited discrete regions of the nucleus at growth arrest. Mol. Cell. Biol. 21, 2918-2932 (Pubitemid 32244934)
9. Alland, L., David, G., Shen-Li, H., Potes, J., Muhle, R., Lee, H. C., Hou, H., Jr., Chen, K., and DePinho, R. A. (2002) Identification of mammalian Sds3 as an integral component of the Sin3/histone deacetylase corepressor complex. Mol. Cell. Biol. 22, 2743-2750 (Pubitemid 34262994)
10. Lechner, T., Carrozza, M. J., Yu, Y., Grant, P. A., Eberharter, A., Vannier, D., Brosch, G., Stillman, D. J., Shore, D., and Workman, J. L. (2000) Sds3 (suppressor of defective silencing 3) is an integral component of the yeast Sin3[middle dot]Rpd3 histone deacetylase complex and is required for histone deacetylase activity. J. Biol. Chem. 275, 40961-40966 (Pubitemid 32054920)
11. Ludwig, S., Klitzsch, A., and Baniahmad, A. (2011) The ING tumor suppressors in cellular senescence and chromatin. Cell Biosci. 1, 25
12. Ayer, D. E., Lawrence, Q. A., and Eisenman, R. N. (1995) Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 80, 767-776
13. Sommer, A., Hilfenhaus, S., Menkel, A., Kremmer, E., Seiser, C., Loidl, P., and Lüscher, B. (1997) Cell growth inhibition by the Mad/Max complex through recruitment of histone deacetylase activity. Curr. Biol. 7, 357-365 (Pubitemid 27274789)
14. Wotton, D., Knoepfler, P. S., Laherty, C. D., Eisenman, R. N., and Massagué, J. (2001) The Smad transcriptional corepressor TGIF recruits mSin3. Cell Growth Differ. 12, 457-463 (Pubitemid 32906090)
15. Smith, K. T., Martin-Brown, S. A., Florens, L., Washburn, M. P., and Workman, J. L. (2010) Deacetylase inhibitors dissociate the histone-targeting ING2 subunit from the Sin3 complex. Chem. Biol. 17, 65-74
16. Dickinson, M., Johnstone, R. W., and Prince, H. M. (2010) Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect. Invest. New Drugs 28, S3-20
17. Bantscheff, M., Hopf, C., Savitski, M. M., Dittmann, A., Grandi, P., Michon, A. M., Schlegl, J., Abraham, Y., Becher, I., Bergamini, G., Boesche, M., Delling, M., Dümpelfeld, B., Eberhard, D., Huthmacher, C., Mathieson, T., Poeckel, D., Reader, V., Strunk, K., Sweetman, G., Kruse, U., Neubauer, G., Ramsden, N. G., and Drewes, G. (2011) Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat. Biotechnol. 29, 255-265
18. Seraj, M. J., Samant, R. S., Verderame, M. F., and Welch, D. R. (2000) Functional evidence for a novel human breast carcinoma metastasis suppressor, BRMS1, encoded at chromosome 11q13. Cancer Res. 60, 2764-2769 (Pubitemid 30395788)
19. Wu, M. Y., Eldin, K. W., and Beaudet, A. L. (2008) Identification of chromatin remodeling genes Arid4a and Arid4b as leukemia suppressor genes. J. Natl. Cancer Inst. 100, 1247-1259
20. Ythier, D., Larrieu, D., Brambilla, C., Brambilla, E., and Pedeux, R. (2008) The new tumor suppressor genes ING: genomic structure and status in cancer. Int. J. Cancer 123, 1483-1490
21. Unoki, M., Kumamoto, K., Takenoshita, S., and Harris, C. C. (2009) Reviewing the current classification of inhibitor of growth family proteins. Cancer Sci. 100, 1173-1179
22. Unoki, M., Kumamoto, K., and Harris, C. C. (2009) ING proteins as potential anticancer drug targets. Current Drug Targets 10, 442-454
23. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
24. Washburn, M. P., Wolters, D., and Yates, J. R., 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247 (Pubitemid 32220565)
25. Wolters, D. A., Washburn, M. P., and Yates, J. R., 3rd (2001) An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 73, 5683-5690 (Pubitemid 33126725)
26. McDonald, W. H., Ohi, R., Miyamoto, D. T., Mitchison, T. J., and Yates, J. R. (2002) Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LCMS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int. J. Mass Spectrom. 219, 245-251
27. Florens, L., and Washburn, M. P. (2006) Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328, 159-175
28. Eng, J., McCormack, A. L., and Yates, J. R., III (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Mass Spectrom. 5, 976-989
29. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
30. Zybailov, B., Mosley, A. L., Sardiu, M. E., Coleman, M. K., Florens, L., and Washburn, M. P. (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339-2347 (Pubitemid 44330827)
31. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (Pubitemid 37428274)
32. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
33. Smyth, G. K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3
34. Benjamini, Y., and Hochber, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B 57, 289-300
35. Söding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-248 (Pubitemid 44529917)
36. Mosley, A. L., Florens, L., Wen, Z., and Washburn, M. P. (2009) A label free quantitative proteomic analysis of the Saccharomyces cerevisiae nucleus. J. Proteomics 72, 110-120
37. Zhang, Y., Wen, Z., Washburn, M. P., and Florens, L. (2010) Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82, 2272-2281
38. Mosley, A. L., Sardiu, M. E., Pattenden, S. G., Workman, J. L., Florens, L., and Washburn, M. P. (2011) Highly reproducible label free quantitative proteomic analysis of RNA polymerase complexes. Mol. Cell. Proteomics 10, M110.000687
39. Shiio, Y., Rose, D. W., Aur, R., Donohoe, S., Aebersold, R., and Eisenman, R. N. (2006) Identification and characterization of SAP25, a novel component of the mSin3 corepressor complex. Mol. Cell. Biol. 26, 1386-1397 (Pubitemid 43202564)
40. Katz, E., Dubois-Marshall, S., Sims, A. H., Gautier, P., Caldwell, H., Meehan, R. R., and Harrison, D. J. (2011) An in vitro model that recapitulates the epithelial to mesenchymal transition (EMT) in human breast cancer. PLoS One 6, e17083
41. Shi, X., Hong, T., Walter, K. L., Ewalt, M., Michishita, E., Hung, T., Carney, D., Pena, P., Lan, F., Kaadige, M. R., Lacoste, N., Cayrou, C., Davrazou, F., Saha, A., Cairns, B. R., Ayer, D. E., Kutateladze, T. G., Shi, Y., Côté, J., Chua, K. F., and Gozani, O. (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442, 96-99 (Pubitemid 44064216)
42. Egeblad, M., Rasch, M. G., and Weaver, V. M. (2010) Dynamic interplay between the collagen scaffold and tumor evolution. Current Opinion Cell Biol. 22, 697-706
43. Zhang, Y., Handley, D., Kaplan, T., Yu, H., Bais, A. S., Richards, T., Pandit, K. V., Zeng, Q., Benos, P. V., Friedman, N., Eickelberg, O., and Kaminski, N. (2011) High throughput determination of TGFbeta1/SMAD3 targets in A549 lung epithelial cells. PLoS One 6, e20319
44. Kiemer, A. K., Takeuchi, K., and Quinlan, M. P. (2001) Identification of genes involved in epithelial-mesenchymal transition and tumor progression. Oncogene 20, 6679-6688 (Pubitemid 33020596)
45. Lee, E. K., Han, G. Y., Park, H. W., Song, Y. J., and Kim, C. W. (2010) Transgelin promotes migration and invasion of cancer stem cells. J. Proteome Res. 9, 5108-5117
46. Yu, H., Königshoff, M., Jayachandran, A., Handley, D., Seeger, W., Kaminski, N., and Eickelberg, O. (2008) Transgelin is a direct target of TGF-beta/Smad3-dependent epithelial cell migration in lung fibrosis. FASEB J. 22, 1778-1789 (Pubitemid 351811455)
47. Micalizzi, D. S., Farabaugh, S. M., and Ford, H. L. (2010) Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia 15, 117-134
48. Halder, S. K., Beauchamp, R. D., and Datta, P. K. (2005) A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7, 509-521 (Pubitemid 40791869)
49. Keshamouni, V. G., Michailidis, G., Grasso, C. S., Anthwal, S., Strahler, J. R., Walker, A., Arenberg, D. A., Reddy, R. C., Akulapalli, S., Thannickal, V. J., Standiford, T. J., Andrews, P. C., and Omenn, G. S. (2006) Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J. Proteome Res. 5, 1143-1154 (Pubitemid 43727792)
50. Hjelmeland, M. D., Hjelmeland, A. B., Sathornsumetee, S., Reese, E. D., Herbstreith, M. H., Laping, N. J., Friedman, H. S., Bigner, D. D., Wang, X. F., and Rich, J. N. (2004) SB-431542, a small molecule transforming growth factor-beta-receptor antagonist, inhibits human glioma cell line proliferation and motility. Mol. Cancer Ther. 3, 737-745 (Pubitemid 39193755)
51. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Fan, R. S., Zborowska, E., Kinzler, K. W., Vogelstein, B., et al. (1995) Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 268, 1336-1338
52. Miyafuji, Y., Zhong, X., Uchida, I., Koi, M., and Hemmi, H. (2001) Growth inhibition due to complementation of transforming growth factor-beta receptor type II-defect by human chromosome 3 transfer in human colorectal carcinoma cells. J. Cell. Physiol. 187, 356-364 (Pubitemid 32378360)
53. Munoz, I. M., Macartney, T., Sanchez-Pulido, L., Ponting, C. P., Rocha, S., and Rouse, J. (2012) FAM60A (Family with sequence similarity 60A) is a cell cycle-fluctuating regulator of the SIN3-HDAC1 histone deacetylase complex. J. Biol. Chem. 287, 32346-32353
54. McDonel, P., Demmers, J., Tan, D. W., Watt, F., and Hendrich, B. D. (2012) Sin3a is essential for the genome integrity and viability of pluripotent cells. Dev. Biol. 363, 62-73
55. Meulmeester, E., and Ten Dijke, P. (2011) The dynamic roles of TGF-beta in cancer. J. Pathol. 223, 205-218
56. Margadant, C., and Sonnenberg, A. (2010) Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep. 11, 97-105
57. Hurst, D. R., and Welch, D. R. (2011) Metastasis suppressor genes at the interface between the environment and tumor cell growth. Int. Rev. CellMol. Biol. 286, 107-180
58. Yoshikawa, M., Hishikawa, K., Marumo, T., and Fujita, T. (2007) Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells. J. Am. Soc. Nephrol. 18, 58-65 (Pubitemid 46053422)
59. Srivastava, R. K., Kurzrock, R., and Shankar, S. (2010) MS-275 sensitizes TRAIL-resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses epithelial-mesenchymal transition in vivo. Mol. Cancer Ther. 9, 3254-3266
60. Lei, W., Zhang, K., Pan, X., Hu, Y., Wang, D., Yuan, X., Shu, G., and Song, J. (2010) Histone deacetylase 1 is required for transforming growth factor-beta1-induced epithelial-mesenchymal transition. Int. J. Biochem. Cell Biol. 42, 1489-1497
61. Bruzzese, F., Leone, A., Rocco, M., Carbone, C., Piro, G., Caraglia, M., Di Gennaro, E., and Budillon, A. (2011) HDAC inhibitor vorinostat enhances the antitumor effect of gefitinib in squamous cell carcinoma of head and neck by modulating ErbB receptor expression and reverting EMT. J. Cell. Physiol. 226, 2378-2390
62. Kumamoto, K., Fujita, K., Kurotani, R., Saito, M., Unoki, M., Hagiwara, N., Shiga, H., Bowman, E. D., Yanaihara, N., Okamura, S., Nagashima, M., Miyamoto, K., Takenoshita, S., Yokota, J., and Harris, C. C. (2009) ING2 is upregulated in colon cancer and increases invasion by enhanced MMP13 expression. Int. J. Cancer 125, 1306-1315
63. Lai, A. Y., and Wade, P. A. (2011) Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11, 588-596
64. Yu, Y., Zeng, P., Xiong, J., Liu, Z., Berger, S. L., and Merlino, G. (2010) Epigenetic drugs can stimulate metastasis through enhanced expression of the pro-metastatic Ezrin gene. PLoS One 5, e12710
65. Fujita, N., Jaye, D. L., Kajita, M., Geigerman, C., Moreno, C. S., and Wade, P. A. (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113, 207-219 (Pubitemid 36514972)
66. Salisbury, C. M., and Cravatt, B. F. (2007) Activity-based probes for proteomic profiling of histone deacetylase complexes. Proc. Natl. Acad. Sci. U. S. A. 104, 1171-1176 (Pubitemid 46183977)
67. Mahrour, N., Redwine, W. B., Florens, L., Swanson, S. K., Martin-Brown, S., Bradford, W. D., Staehling-Hampton, K., Washburn, M. P., Conaway, R. C., and Conaway, J. W. (2008) Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J. Biol. Chem. 283, 8005-8013.
68. Petroziello, J., Yamane, A., Westendorf, L., Thompson, M., McDonagh, C., Cerveny, C., Law, C. L., Wahl, A., and Carter, P. (2004). Suppression subtractive hybridization and expression profiling identifies a unique set of genes overexpressed in non-small-cell lung cancer. Oncogene. 23, 7734-7745 (Pubitemid 39424932)