Reptin and pontin oligomerization and activity are modulated through histone H3 N-terminal tail interaction

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 33999-34012

  Queval, Richard ^a,b   Papin, Christophe ^c   Dalvai, Mathieu ^a,b,d   Bystricky, Kerstin ^a,b   Humbert, Odile ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; ALKYLATION; GENES; OLIGOMERS; TRANSCRIPTION;

ATP-ASE ACTIVITY; CELLULAR PROCESS; CHROMATIN REMODELING COMPLEX; DIFFERENTIAL ACTIVITY; ENZYMATIC ACTIVITIES; NUCLEOSOME CORE PARTICLES; PROGESTERONE RECEPTOR; REGULATORY FACTORS;

PROTEINS;

HISTONE H3; MEMBRANE PROTEIN; PONTIN; REPTIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA; DNA HELICASE; HISTONE; NUCLEOSOME; PROTEIN BINDING; RECOMBINANT PROTEIN; RUVBL1 PROTEIN, HUMAN; RUVBL2 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CODON; CONTROLLED STUDY; DNA METABOLISM; ENZYME ACTIVITY; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; HYDROLYSIS; MOLECULAR DYNAMICS; OLIGOMERIZATION; PROMOTER REGION; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; AMINO ACID SEQUENCE; BINDING SITE; CELL FREE SYSTEM; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOSOME; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CELL-FREE SYSTEM; DNA; DNA HELICASES; ESCHERICHIA COLI; GENE EXPRESSION; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 84917707282     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.576785     Document Type: Article

References (49)

1. Rosenbaum, J., Baek, S. H., Dutta, A., Houry, W. A., Huber, O., Hupp, T. R., and Matias, P. M. (2013) The emergence of the conserved AAA+ ATPases Pontin and Reptin on the signaling landscape. Sci. Signal. 6, mr1
2. Kanemaki, M., Makino, Y., Yoshida, T., Kishimoto, T., Koga, A., Yamamoto, K., Yamamoto, M., Moncollin, V., Egly, J. M., Muramatsu, M., and Tamura, T. (1997) Molecular cloning of a rat 49-kDa TBP-interacting protein (TIP49) that is highly homologous to the bacterial RuvB. Biochem. Biophys. Res. Commun. 235, 64-68
3. Gallant, P. (2007) Control of transcription by Pontin and Reptin. Trends Cell Biol. 17, 187-192
4. Jha, S., Shibata, E., and Dutta, A. (2008) Human Rvb1/Tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol. Cell. Biol. 28, 2690-2700
5. Ikura, T., Ogryzko, V. V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J., and Nakatani, Y. (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102, 463-473
6. Jin, J., Cai, Y., Yao, T., Gottschalk, A. J., Florens, L., Swanson, S. K., Gutiérrez, J. L., Coleman, M. K., Workman, J. L., Mushegian, A., Washburn, M. P., Conaway, R. C., and Conaway, J. W. (2005) A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J. Biol. Chem. 280, 41207-41212
7. Jónsson, Z. O., Jha, S., Wohlschlegel, J. A., and Dutta, A. (2004) Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol. Cell 16, 465-477
8. Shen, X., Mizuguchi, G., Hamiche, A., and Wu, C. (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406, 541-544
9. Wu, W. H., Alami, S., Luk, E., Wu, C. H., Sen, S., Mizuguchi, G., Wei, D., and Wu, C. (2005) Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12, 1064-1071
10. Mizuguchi, G., Shen, X., Landry, J., Wu, W. H., Sen, S., and Wu, C. (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343-348
11. Qiu, X. B., Lin, Y. L., Thome, K. C., Pian, P., Schlegel, B. P., Weremowicz, S., Parvin, J. D., and Dutta, A. (1998) A eukaryotic RuvB-like protein (RUVBL1) essential for growth. J. Biol. Chem. 273, 27786-27793
12. Bauer, A., Chauvet, S., Huber, O., Usseglio, F., Rothbächer, U., Aragnol, D., Kemler, R., and Pradel, J. (2000) Pontin52 and Reptin52 function as antagonistic regulators of β-catenin signalling activity. EMBO J. 19, 6121-6130
13. Matias, P. M., Gorynia, S., Donner, P., and Carrondo, M. A. (2006) Crystal structure of the human AAA+ protein RuvBL1. J. Biol. Chem. 281, 38918-38929
14. Diop, S. B., Bertaux, K., Vasanthi, D., Sarkeshik, A., Goirand, B., Aragnol, D., Tolwinski, N. S., Cole, M. D., Pradel, J., Yates, J. R., 3rd, Mishra, R. K., Graba, Y., and Saurin, A. J. (2008) Reptin and Pontin function antagonistically with PcG and TrxG complexes to mediate Hox gene control.EMBO Rep. 9, 260-266
15. Bochkarev, A., Pfuetzner, R. A., Edwards, A. M., and Frappier, L. (1997) Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature 385, 176-181
16. Petukhov, M., Dagkessamanskaja, A., Bommer, M., Barrett, T., Tsaneva, I., Yakimov, A., Quéval, R., Shvetsov, A., Khodorkovskiy, M., Käs, E., and Grigoriev, M. (2012) Large-scale conformational flexibility determines the properties of AAA+ TIP49 ATPases. Structure 20, 1321-1331
17. Gribun, A., Cheung, K. L., Huen, J., Ortega, J., and Houry, W. A. (2008) Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. J. Mol. Biol. 376, 1320-1333
18. Cheung, K. L., Huen, J., Kakihara, Y., Houry, W. A., and Ortega, J. (2010) Alternative oligomeric states of the yeast Rvb1/Rvb2 complex induced by histidine tags. J. Mol. Biol. 404, 478-492
19. López-Perrote, A., Muñoz-Hernández, H., Gil, D., and Llorca, O. (2012) Conformational transitions regulate the exposure of a DNA-binding domain in the RuvBL1-RuvBL2 complex. Nucleic Acids Res. 40, 11086-11099
20. Puri, T., Wendler, P., Sigala, B., Saibil, H., and Tsaneva, I. R. (2007) Dodecameric structure and ATPase activity of the human TIP48/TIP49 complex. J. Mol. Biol. 366, 179-192
21. Torreira, E., Jha, S., López-Blanco, J. R., Arias-Palomo, E., Chacón, P., Cañas, C., Ayora, S., Dutta, A., and Llorca, O. (2008) Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes. Structure 16, 1511-1520
22. Papin, C., Humbert, O., Kalashnikova, A., Eckert, K., Morera, S., Käs, E., and Grigoriev, M. (2010) 3′- to 5′ DNA unwinding by TIP49b proteins. FEBS J. 277, 2705-2714
23. Jha, S., Gupta, A., Dar, A., and Dutta, A. (2013) RVBs are required for assembling a functional TIP60 complex. Mol. Cell. Biol. 33, 1164-1174
24. Grigoletto, A., Lestienne, P., and Rosenbaum, J. (2011) The multifaceted proteins Reptin and Pontin as major players in cancer. Biochim. Biophys. Acta 1815, 147-157
25. Huen, J., Kakihara, Y., Ugwu, F., Cheung, K. L., Ortega, J., and Houry, W. A. (2010) Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem. Cell Biol. 88, 29-40
26. Luger, K., Rechsteiner, T. J., and Richmond, T. J. (1999) Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304, 3-19
27. Grigoriev, M., and Hsieh, P. (1997) A histone octamer blocks branch migration of a Holliday junction. Mol. Cell. Biol. 17, 7139-7150
28. Hamiche, A., and Xiao, H. (2004) Methods for analysis of nucleosome sliding by Drosophila NURF. Methods Enzymol. 377, 353-363
29. Iacovoni, J. S., Caron, P., Lassadi, I., Nicolas, E., Massip, L., Trouche, D., and Legube, G. (2010) High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29, 1446-1457
30. Dalvai, M., Fleury, L., Bellucci, L., Kocanova, S., and Bystricky, K. (2013) TIP48/Reptin and H2A.Z requirement for initiating chromatin remodeling in estrogen-activated transcription. PLoS Genet. 9, e1003387
31. Choi, J., Heo, K., and An, W. (2009) Cooperative action of TIP48 and TIP49 in H2A.Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res. 37, 5993-6007
32. Pinnola, A., Naumova, N., Shah, M., and Tulin, A. V. (2007) Nucleosomal core histones mediate dynamic regulation of poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J. Biol. Chem. 282, 32511-32519
33. Clark, N. J., Kramer, M., Muthurajan, U. M., and Luger, K. (2012) Alternative modes of binding of poly(ADP-ribose) polymerase 1 to free DNA and nucleosomes. J. Biol. Chem. 287, 32430-32439
34. Zheng, C., and Hayes, J. J. (2003) Structures and interactions of the core histone tail domains. Biopolymers 68, 539-546
35. 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
36. Elkaim, J., Castroviejo, M., Bennani, D., Taouji, S., Allain, N., Laguerre, M., Rosenbaum, J., Dessolin, J., and Lestienne, P. (2012) First identification of small-molecule inhibitors of Pontin by combining virtual screening and enzymatic assay. Biochem. J. 443, 549-559
37. Haurie, V., Ménard, L., Nicou, A., Touriol, C., Metzler, P., Fernandez, J., Taras, D., Lestienne, P., Balabaud, C., Bioulac-Sage, P., Prats, H., Zucman- Rossi, J., and Rosenbaum, J. (2009) Adenosine triphosphatase pontin is overexpressed in hepatocellular carcinoma and coregulated with reptin through a new posttranslational mechanism. Hepatology 50, 1871-1883
38. Cheung, K. L., Huen, J., Houry, W. A., and Ortega, J. (2010) Comparison of the multiple oligomeric structures observed for the Rvb1 and Rvb2 proteins. Biochem. Cell Biol. 88, 77-88
39. Niewiarowski, A., Bradley, A. S., Gor, J., McKay, A. R., Perkins, S. J., and Tsaneva, I. R. (2010) Oligomeric assembly and interactions within the human RuvB-like RuvBL1 and RuvBL2 complexes. Biochem. J. 429, 113-125
40. Udugama, M., Sabri, A., and Bartholomew, B. (2011) The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 31, 662-673
41. Tosi, A., Haas, C., Herzog, F., Gilmozzi, A., Berninghausen, O., Ungewickell, C., Gerhold, C. B., Lakomek, K., Aebersold, R., Beckmann, R., and Hopfner, K. P. (2013) Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 154, 1207-1219
42. Ettig, R., Kepper, N., Stehr, R., Wedemann, G., and Rippe, K. (2011) Dissecting DNA-histone interactions in the nucleosome by molecular dynamics simulations of DNA unwrapping. Biophys. J. 101, 1999-2008
43. Sun, Y., Jiang, X., Xu, Y., Ayrapetov, M. K., Moreau, L. A., Whetstine, J. R., and Price, B. D. (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11, 1376-1382
44. Yen, K., Vinayachandran, V., and Pugh, B. F. (2013) SWR-C and INO80 chromatin remodelers recognize nucleosome-free regions near +1 nucleosomes. Cell 154, 1246-1256
45. Nguyen, V. Q., Ranjan, A., Stengel, F., Wei, D., Aebersold, R., Wu, C., and Leschziner, A. E. (2013) Molecular architecture of the ATP-dependent chromatin-remodeling complex SWR1. Cell 154, 1220-1231
46. Papamichos-Chronakis, M., Watanabe, S., Rando, O. J., and Peterson, C. L. (2011) Global regulation of H2A.Z localization by the INO80 chromatinremodeling enzyme is essential for genome integrity. Cell 144, 200-213
47. Weiske, J., and Huber, O. (2005) The histidine triad protein Hint1 interacts with Pontin and Reptin and inhibits TCF- β-catenin-mediated transcription. J. Cell Sci. 118, 3117-3129
48. Wood, M. A., McMahon, S. B., and Cole, M. D. (2000)AnATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc. Mol. Cell 5, 321-330
49. Fleury, L., Gerus, M., Lavigne, A. C., Richard-Foy, H., and Bystricky, K. (2008) Eliminating epigenetic barriers induces transient hormone-regulated gene expression in estrogen receptor negative breast cancer cells. Oncogene 27, 4075-4085