PATZ1 is a DNA damage-responsive transcription factor that inhibits p53 function

Molecular and Cellular Biology

Volumn 35, Issue 10, 2015, Pages 1741-1753

  Keskin, Nazli ^a   Deniz, Emre ^a   Eryilmaz, Jitka ^a,e   Un, Manolya ^a   Batur, Tugce ^a   Ersahin, Tulin ^b,c   Atalay, Rengul Cetin ^b,c   Sakaguchi, Shinya ^d   Ellmeier, Wilfried ^d   Erman, Batu ^a  

^a SABANCI UNIVERSITY   (Turkey)

^b BILKENT UNIVERSITY   (Turkey)

^c MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e SANKO Textile   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; HETERODIMER; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PATZ1; UNCLASSIFIED DRUG; KRUPPEL LIKE FACTOR; PATZ1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TP53 PROTEIN, HUMAN; TUMOR PROTEIN; ZFP278 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL GROWTH; DNA DAMAGE; DOWN REGULATION; EMBRYO; GENE ONTOLOGY; HUMAN; HUMAN CELL; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA SEQUENCE; TRANSCRIPTION INITIATION; 3T3 CELL LINE; ANIMAL; CELL LINE; CELL PROLIFERATION; DNA REPAIR; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; SEQUENCE ANALYSIS;

ANIMALS; CELL ADHESION; CELL LINE; CELL PROLIFERATION; DNA REPAIR; DOXORUBICIN; GENE EXPRESSION PROFILING; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; NIH 3T3 CELLS; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84929171690     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01475-14     Document Type: Article

References (45)

1. Vousden KH, Prives C. 2009. Blinded by the light: the growing complexity of p53. Cell 137:413-431. http://dx.doi.org/10.1016/j.cell.2009.04.037.
2. Levine AJ, Oren M. 2009. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 9:749-758. http://dx.doi.org/10.1038/nrc2723.
3. Marine J-C, Francoz S, Maetens M, Wahl G, Toledo F, Lozano G. 2006. Keeping p53 in check: essential and synergistic functions of Mdm2 and Mdm4. Cell Death Differ 13:927-934. http://dx.doi.org/10.1038/sj.cdd.4401912.
4. El-Deiry W, Kern S, Pietenpol J, Kinzler K, Vogelstein B. 1992. Definition of a consensus binding site for p53. Nat Genet 1:45-49. http://dx.doi.org/10.1038/ng0492-45.
5. Riley T, Sontag E, Chen P, Levine A. 2008. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9:402-412. http://dx.doi.org/10.1038/nrm2395.
6. Wei C-L, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, Shahab A, Yong HC, Fu Y, Weng Z, Liu J, Zhao XD, Chew J-L, Lee YL, Kuznetsov VA, Sung W-K, Miller LD, Lim B, Liu ET, Yu Q, Ng H-H, Ruan Y. 2006. A global map of p53 transcription-factor binding sites in the human genome. Cell 124:207-219. http://dx.doi.org/10.1016/j.cell.2005.10.043.
7. Li M, He Y, Dubois W, Wu X, Shi J, Huang J. 2012. Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol Cell 46:30-42. http://dx.doi.org/10.1016/j.molcel.2012.01.020.
8. Kenzelmann Broz D, Spano Mello S, Bieging KT, Jiang D, Dusek RL, Brady CA, Sidow A, Attardi LD. 2013. Global genomic profiling reveals an extensive p53-regulated autophagy program contributing to key p53 responses. Genes Dev 27:1016-1031. http://dx.doi.org/10.1101/gad.212282.112.
9. Fedele M, Benvenuto G, Pero R, Majello B, Battista S, Lembo F, Vollono E, Day PM, Santoro M, Lania L, Bruni CB, Fusco A, Chiariotti L. 2000. A novel member of the BTB/POZ family, PATZ, associates with the RNF4 RING finger protein and acts as a transcriptional repressor. J Biol Chem 275:7894-7901. http://dx.doi.org/10.1074/jbc.275.11.7894.
10. Costoya JA. 2007. Functional analysis of the role of POK transcriptional repressors. Brief Funct Genomic Proteomic 6:8-18. http://dx.doi.org/10.1093/bfgp/elm002.
11. Siggs O, Beutler B. 2012. The BTB-ZF transcription factors. Cell Cycle 11:3358-3369. http://dx.doi.org/10.4161/cc.21277.
12. Ow JR, Ma H, Jean A, Goh Z, Lee YH, Chong YM, Soong R, Fu X-Y, Yang H, Wu Q. 2014. Patz1 regulates embryonic stem cell identity. Stem Cells Dev 23:1062-1073. http://dx.doi.org/10.1089/scd.2013.0430.
13. Pero R, Palmieri D, Angrisano T, Valentino T, Federico A, Franco R, Lembo F, Klein-Szanto AJ, Del Vecchio L, Montanaro D, Keller S, Arra C, Papadopoulou V, Wagner SD, Croce CM, Fusco A, Chiariotti L, Fedele M. 2012. POZ-, AT-hook-, and zinc finger-containing protein (PATZ) interacts with human oncogene B cell lymphoma 6 (BCL6) and is required for its negative autoregulation. J Biol Chem 287:18308-18317. http://dx.doi.org/10.1074/jbc. M112.346270.
14. Bilic I, Koesters C, Unger B, Sekimata M, Hertweck A, Maschek R, Wilson CB, Ellmeier W. 2006. Negative regulation of CD8 expression via Cd8 enhancer-mediated recruitment of the zinc finger protein MAZR. Nat Immunol 7:392-400. http://dx.doi.org/10.1038/ni1311.
15. Abramova A, Sakaguchi S, Schebesta A, Hassan H, Boucheron N, Valent P, Roers A, Ellmeier W. 2013. The transcription factor MAZR preferentially acts as a transcriptional repressor in mast cells and plays a minor role in the regulation of effector functions in response to FceRI stimulation. PLoS One 8:e77677. http://dx.doi.org/10.1371/journal.pone.0077677.
16. Sakaguchi S, Hombauer M, Bilic I, Naoe Y, Schebesta A, Taniuchi I, Ellmeier W. 2010. The zinc-finger protein MAZR is part of the transcription factor network that controls the CD4 versus CD8 lineage fate of double- positive thymocytes. Nat Immunol 11:442-448. http://dx.doi.org/10.1038/ni.1860.
17. Valentino T, Palmieri D, Vitiello M, Pierantoni GM, Fusco A, Fedele M. PATZ1 interacts with p53 and regulates expression of p53-target genes enhancing apoptosis or cell survival based on the cellular context. Cell Death Dis 4:e963. http://dx.doi.org/10.1038/cddis.2013.500.
18. Yang W, Ravatn R, Kudoh K. 2010. Interaction of the regulatory subunit of the cAMP-dependent protein kinase with PATZ1 (ZNF278). Biochem Biophys Res Commun 391:1318-1323. http://dx.doi.org/10.1016/j.bbrc.2009.12.026.
19. Kobayashi A, Yamagiwa H, Hoshino H, Muto A, Sato K, Morita M, Hayashi N, Yamamoto M, Igarashi K. 2000. A combinatorial code for gene expression generated by transcription factor Bach2 and MAZR (MAZ-related factor) through the BTB/POZ domain. Mol Cell Biol 20: 1733-1746. http://dx.doi.org/10.1128/MCB.20.5.1733-1746.2000.
20. Mastrangelo T, Modena P, Tornielli S, Bullrich F, Testi MA, Mezzelani A, Radice P, Azzarelli A, Pilotti S, Croce CM, Pierotti MA, Sozzi G. 2000. A novel zinc finger gene is fused to EWS in small round cell tumor. Oncogene 19:3799-3804. http://dx.doi.org/10.1038/sj.onc.1203762.
21. Cho JH, Kim MJ, Kim KJ, Kim J-R. 2012. POZ/BTB and AT-hookcontaining zinc finger protein 1 (PATZ1) inhibits endothelial cell senescence through a p53 dependent pathway. Cell Death Differ 19:703-712. http://dx.doi.org/10.1038/cdd.2011.142.
22. Silverstone A, Sun L, Witte ON, Baltimore D. 1980. Biosynthesis of murine terminal deoxynucleotidyltransferase. J Biol Chem 255:791-796.
23. Groves T, Katis P, Madden Z, Manickam K, Ramsden D, Wu G, Guidos CJ. 1995. In vitro maturation of clonal CD4+CD8+ cell lines in response to TCR engagement. J Immunol 154:5011-5022.
24. Naviaux RK, Costanzi E, Haas M, Verma IM. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J Virol 70:5701-5705.
25. Morgenstern JP, Land H. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18: 3587-3596. http://dx.doi.org/10.1093/nar/18.12.3587.
26. El-Deiry W. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825. http://dx.doi.org/10.1016/0092-8674(93)90500-P.
27. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. 2001. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7:673-682. http://dx.doi.org/10.1016/S1097-2765(01)00213-1.
28. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343-345. http://dx.doi.org/10.1038/nmeth.1318.
29. Ayed A, Mulder FAA, Yi GS, Lu Y, Kay LE, Arrowsmith CH. 2001. Latent and active p53 are identical in conformation. Nat Struct Biol 8:756-760. http://dx.doi.org/10.1038/nsb0901-756.
30. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. http://dx.doi.org/10.1038/nmeth.2089.
31. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. 2006. Gene- Pattern 2.0. Nat Genet 38:500-501. http://dx.doi.org/10.1038/ng0506-500.
32. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
33. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
34. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11:R106. http://dx.doi.org/10.1186/gb-2010-11-10-r106.
35. Valentino T, Palmieri D, Vitiello M, Simeone A, Palma G, Arra C, Chieffi P, Chiariotti L, Fusco A, Fedele M. 2013. Embryonic defects and growth alteration in mice with homozygous disruption of the Patz1 gene. J Cell Physiol 228:646-653. http://dx.doi.org/10.1002/jcp.24174.
36. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, Kinzler KW, Vogelstein B. 1997. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1:3-11. http://dx.doi.org/10.1016/S1097-2765(00)80002-7.
37. Stogios PJ, Downs GS, Jauhal JJS, Nandra SK, Privé GG. 2005. Sequence and structural analysis of BTB domain proteins. Genome Biol 6:R82. http://dx.doi.org/10.1186/gb-2005-6-10-r82.
38. Lai JS, Herr W. 1992. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc Natl Acad SciUSA 89:6958-6962. http://dx.doi.org/10.1073/pnas.89.15.6958.
39. Khoury MP, Bourdon J-C. 2010. The isoforms of the p53 protein. Cold Spring Harb Perspect Biol 2:a000927. http://dx.doi.org/10.1101/cshperspect.a000927.
40. Bilic I, Ellmeier W. 2007. The role of BTB domain-containing zinc finger proteins in T cell development and function. Immunol Lett 108:1-9. http://dx.doi.org/10.1016/j.imlet.2006.09.007.
41. Pero R, Lembo F, Palmieri EA, Vitiello C, Fedele M, Fusco A, Bruni CB, Chiariotti L. 2002. PATZ attenuates the RNF4-mediated enhancement of androgen receptor-dependent transcription. J Biol Chem 277:3280-3285. http://dx.doi.org/10.1074/jbc. M109491200.
42. Shi X, Kachirskaia I, Yamaguchi H, West LE, Wen H, Wang EW, Dutta S, Appella E, Gozani O. 2007. Modulation of p53 function by SET8-mediated methylation at lysine 382. Mol Cell 27:636-646. http://dx.doi.org/10.1016/j.molcel.2007.07.012.
43. Kachirskaia I, Shi X, Yamaguchi H, Tanoue K, Wen H, Wang EW, Appella E, Gozani O. 2008. Role for 53BP1 Tudor domain recognition of p53 dimethylated at lysine 382 in DNA damage signaling. J Biol Chem 283:34660-34666. http://dx.doi.org/10.1074/jbc. M806020200.
44. Botuyan MV, Lee J, Ward IM, Kim J-E, Thompson JR, Chen J, Mer G. 2006. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127:1361-1373. http://dx.doi.org/10.1016/j.cell.2006.10.043.
45. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. http://dx.doi.org/10.1038/nprot.2008.211.