Human CHD2 is a chromatin assembly ATPase regulated by its chromo- And DNA-binding domains

Journal of Biological Chemistry

Volumn 290, Issue 1, 2015, Pages 25-34

  Liu, Jessica C ^a,b   Ferreira, Catarina G ^a   Yusufzai, Timur ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

C-TERMINAL REGIONS; CELLULAR ACTIVITIES; CHROMATIN ASSEMBLY; CHROMATIN REMODELING; DNA BINDING DOMAIN; DNA-BINDING PROTEIN; DOUBLE STRANDED DNA; EPILEPTIC DISORDERS;

CHROMOSOMES;

ADENOSINE TRIPHOSPHATASE; CHROMODOMAIN HELICASE DNA BINDING PROTEIN 2; DOUBLE STRANDED DNA; UNCLASSIFIED DRUG; CHD2 PROTEIN, HUMAN; CHROMATIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HISTONE; PROTEIN BINDING; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BASE PAIRING; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMODOMAIN; CONTROLLED STUDY; DNA BINDING DOMAIN; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME REGULATION; ENZYME SPECIFICITY; HYDROLYSIS; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; AMINO ACID SEQUENCE; ANIMAL; BACULOVIRIDAE; BINDING SITE; CHEMISTRY; CHROMATIN; DROSOPHILA MELANOGASTER; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; SF9 CELL LINE; SPODOPTERA;

MUS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; BACULOVIRIDAE; BINDING SITES; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SF9 CELLS; SPODOPTERA;

EID: 84920522426     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.609156     Document Type: Article

References (43)

1. Gorbalenya, A. E., and Koonin, E. V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3, 419-429
2. Eisen, J. A., Sweder, K. S., and Hanawalt, P. C. (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 23, 2715-2723
3. Flaus, A., Martin, D. M., Barton, G. J., and Owen-Hughes, T. (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34, 2887-2905
4. Clapier, C. R., and Cairns, B. R. (2009) The Biology of Chromatin Remodeling Complexes. Annu. Rev. Biochem. 78, 273-304
5. Woodage, T., Basrai, M. A., Baxevanis, A. D., Hieter, P., and Collins, F. S. (1997) Characterization of the CHD family of proteins. Proc. Natl. Acad. Sci. U.S.A. 94, 11472-11477
6. Marfella, C. G. A., Ohkawa, Y., Coles, A. H., Garlick, D. S., Jones, S. N., and Imbalzano, A. N. (2006) Mutation of the SNF2 Family Member Chd2 Affects Mouse Development and Survival. J. Cell. Physiol. 209, 162-171
7. Kulkarni, S., Nagarajan, P., Wall, J., Donovan, D. J., Donell, R. L., Ligon, A. H., Venkatachalam, S, and Quade, B. J. (2008) Disruption of Chromodomain Helicase DNA Binding Protein 2 (CHD2) Causes Scoliosis. Am. J. Med. Genet. 146, 1117-1127
8. Carvill, G. L., Heavin, S. B., Yendle, S. C., McMahon, J. M., O'Roak, B. J., Cook, J., Khan, A., Dorschner, M. O., Weaver, M., and Calvert, S., Malone, S., Wallace, G., Stanley, T., Bye, A. M., Bleasel, A., Howell, K. B., Kivity, S., Mackay, M. T., Rodriguez-Casero, V., Webster, R., Korczyn, A., Afawi, Z., Zelnick, N., Lerman-Sagie, T., Lev, D., Møller, R. S., Gill, D., Andrade, D. M., Freeman, J. L., Sadleir, L. G., Shendure, J., Berkovic, S. F., Scheffer, I. E., and Mefford, H. C. (2013) Targeted resequencing in epileptic encephalopathis identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet. 45, 825-830
9. Lund, C., Brodtkorb, E., Øye, A.-M., Røsby, O., and Selmer, K. K. (2014) CHD2 mutations in Lennox-Gastaut Syndrome. Epilepsy Behav. 33, 18-21
10. Courage, C., Houge, G., Gallati, S., Schjelderup, J., and Rieubland, C. (2014) 15q26.1 microdeletion encompassing only CHD2 and RGMA in two adults with moderate intellectual disability, epilepsy and truncal obesity. Eur. J. Med. Genet. 10.1016/j.ejmg. 2014.06.003
11. Chénier, S., Yoon, G., Argiropoulos, B., Lauzon, J., Laframboise, R., Ahn, J. W., Ogilvie, C. M., Lionel, A. C., Marshall, C. R., and Vaags A. K., et al. (2014) CHD2 haploinsufficiency is associated with developmental delay, intellectual disability, epilepsy an neurobehavioural problems. J. Neurodev. Disord. 10.1186/1866-1955-6-9
12. Suls, A., Jaehn, J. A., Kecskés, A., Weber, Y., Weckhuysen, S., Craiu, D. C., Siekierska, A., Djémié, T., Afrikanova, T., Gormley, P., von Spiczak S, Kluger, G., Iliescu, C. M., Talvik, T., Talvik, I., Meral, C., Caglayan, H. S., Giraldez, B. G., Serratosa, J., Lemke, J. R., Hoffman-Zacharska, D., Szczepanik, E., Barisic, N., Komarek, V., Hjalgrim, H., Møller, R. S., Linnankivi, T., Dimova, P., Striano, P., Zara, F., Marini, C., Guerrini, R., Depienne, C., Baulac, S., Kuhlenbäumer, G., Crawford, A. D., Lehesjoki, A. E., de Witte, P. A., Palotie, A., Lerche, H., Esguerra, C. V., De Jonghe, P., Helbig, I., EuroEPINOMICS RES Consortium (2013) De Novo Loss-of-Function Mutations in CHD2 Cause a Fever-Sensitive Myoclonic Epileptic Encephalopathy Sharing Features with Dravet Syndrome. Am. J. Hum. Genet. 93, 967-975
13. Harada, A., Okada, S., Konno, D., Odawara, J., Yoshimi, T., Yoshimura, S., Kumamaru, H., Saiwai, H., Tsubota, T, Kurumizaka, H., Akashi, K., Tachibana, T., Imbalzano, A. N., and Ohkawa, Y. (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. EMBO J. 31, 2994-3007
14. Yusufzai, T., and Kadonaga, J. T. (2008) HARP is an ATP-driven annealing helicase. Science 322, 748-750
15. Fyodorov, D. V., and Kadonaga, J. T. (2003) Chromatin Assembly In Vitro with Purified Recombinant ACF and NAP-1. Methods Enzymol. 371, 499-515
16. Alexiadis, V., and Kadonaga, J. T. (2002) Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev. 16, 2767-2771
17. Brehm, A., Tufteland, K. R., Aasland, R., and Becker, P. B. (2004) The many colours of chromodomains. Bioessays. 26, 133-140
18. Quan, J., and Yusufzai, T. (2014) The Tumor Suppressor Chromodomain Helicase DNA-binding Protein 5 (CHD5) Remodels Nucleosomes by Unwrapping. J. Biol. Chem. 289, 20717-20726
19. Ito, T., Bulger, M., Pazin, M. J., Kobayashi, R., and Kadonaga, J. T. (1997) ACF, an ISWI-Containing and ATP-Utilizing Chromatin Assembly and Remodeling Factor. Cell 90, 145-155
20. Robinson, K. M., and Schultz, M. C. (2003) Replication-Independent Assembly of Nucleosome Arrays in a Novel Yeast Chromatin Reconstitution System Involves Antisilencing Factor Asf1p and Chromodomain Protein Chd1p. Mol. Cell Biol. 23, 7937-7946
21. Lusser, A., Urwin, D. L., and Kadonaga, J. T. (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 12, 160-166
22. Torigoe, S. E., Urwin, D. L., Ishii, H., Smith, D. E., and Kadonaga, J. T. (2011) Identification of a Rapidly Formed Nonnucleosomal Histone-DNA Intermediate that Is Converted into Chromatin by ACF. Mol. Cell 43, 638-648
23. Nakagawa, T., Bulger, M., Muramatsu, M., and Ito, T. (2001) Multistep Chromatin Assembly on Supercoiled Plasmid DNA by Nucleosome Assembly Protein-1 and ATP-utilizing Chromatin Assembly and Remodeling Factor. J. Biol. Chem. 276, 27384-27391
24. Alexiadis, V., Lusser, A., and Kadonaga, J. T. (2004) A Conserved N-terminal Motif in Rad54 Is Important for Chromatin Remodeling and Homologous Strand Pairing. J. Biol. Chem. 279, 27824-27829
25. Lake, R. J., Geyko, A., Hemashettar, G., Zhao, Y., and Fan, H-Y. (2010) UV-Induced Association of the CSB Remodeling Protein with Chromatin Requires ATP-Dependent Relief of N-Terminal Autorepression. Mol. Cell 37, 235-246
26. Hauk, G., McKnight, J. N., Nodelman, I. M., and Bowman, G. D. (2010) The Chromodomains of theChd1 Chromatin Remodeler Regulate DNA Access to the ATPase Motor. Mol. Cell 39, 711-723
27. Clapier, C. R., and Cairns, B. R. (2012) Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492, 280-284
28. Mueller-Planitz, F., Klinker, H., Ludwigsen, J., and Becker, P. B. (2013) The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat. Struct. Mol. Biol. 20, 82-89
29. Henikoff, S. (1993) Transcriptional activator components and poxvirus DNA-dependent ATPases comprise a single family. Trends Biochem. Sci. 18, 291-292
30. Torigoe, S. E., Patel, A., Khuong, M. T., Bowman, G. D., and Kadonaga, J. T. (2013) ATP-dependent chromatin assembly is functionally distinct from chromatin remodeling. Elife. 0.7554/eLife. 00863
31. Almer, A., Rudolph, H., Hinnen, A., and Hörz, W. (1986) Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5, 2689-2696
32. Varga-Weisz, P. D., Wilm, M., Bonte, E., Dumas, K., Mann, M., and Becker, P. B. (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598-602
33. 2 Tetramer in Nucleosome Remodeling by the SWI-SNF Complex. J. Biol. Chem. 275, 11545-11552
34. Fan, H. Y., He, X., Kingston, R. E., and Narlikar, G. J. (2003) Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11, 1311-1322
35. Stopka, T., and Skoultchi, A. I. (2003) The ISWI ATPase Snf2h is required for early mouse development. Proc. Natl. Acad. Sci. U.S.A. 100, 14097-14102
36. Gaspar-Maia, A., Alajem, A., Polesso, F., Sridharan, R., Mason, M. J., Heidersbach, A., Ramalho-Santos, J., McManus, M. T., Plath, K., Meshorer, E., and Ramalho-Santos, M. (2009) Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863-868
37. Stockdale, C., Flaus, A., Ferreira, H., and Owen-Hughes, T. (2006) Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 281, 16279-26288
38. Yang, J. G., Madrid, T. S., Sevastopoulos, E., and Narlikar, G. J. (2006) The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 13, 1078-1083
39. Gangaraju, V. K., and Bartholomew, B. (2007) Mechanisms of ATP dependent chromatin remodeling. Mutat. Res. 618, 3-17
40. Ryan, D. P., Sundaramoorthy, R., Martin, D., Singh, V., and Owen-Hughes, T. (2011) The DNA-binding domain of the Chd1 chromatin-remodelling enzyme contains SANT and SLIDE domains. EMBO J. 30, 2596-2609
41. Racki, L. R., Yang, J. G., Naber, N., Partensky, P. D., Acevedo, A., Purcell, T. J., Cooke, R., Cheng, Y., and Narlikar, G. J. (2009) The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462, 1016-1021
42. Widom, J. (1992) A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells. Proc. Natl. Acad. Sci. U.S.A. 89, 1095-1099
43. Gaffney, D. J., McVicker, G., Pai, A. A., Fondufe-Mittendorf, Y. N., Lewellen, N., Michelini, K., Widom, J., Gilad, Y., and Pritchard, J. K. (2012) Controls of nucleosome positioning in the human genome. PLoS Genet. 10.1371/journal.pgen.1003036