Browse > Article
http://dx.doi.org/10.14348/molcells.2021.2242

Single-Molecule Imaging Reveals the Mechanism Underlying Histone Loading of Schizosaccharomyces pombe AAA+ ATPase Abo1  

Kang, Yujin (Department of Biological Sciences, Ulsan National Institute of Science and Technology (UNIST))
Cho, Carol (Department of Biological Sciences and KI for the BioCentury, Korea Advanced Institute of Science and Technology (KAIST))
Lee, Kyung Suk (Department of Physics Education, Kongju National University)
Song, Ji-Joon (Department of Biological Sciences and KI for the BioCentury, Korea Advanced Institute of Science and Technology (KAIST))
Lee, Ja Yil (Department of Biological Sciences, Ulsan National Institute of Science and Technology (UNIST))
Abstract
Chromatin dynamics is essential for maintaining genomic integrity and regulating gene expression. Conserved bromodomain-containing AAA+ ATPases play important roles in nucleosome organization as histone chaperones. Recently, the high-resolution cryo-electron microscopy structures of Schizosaccharomyces pombe Abo1 revealed that it forms a hexameric ring and undergoes a conformational change upon ATP hydrolysis. In addition, single-molecule imaging demonstrated that Abo1 loads H3-H4 histones onto DNA in an ATP hydrolysis-dependent manner. However, the molecular mechanism by which Abo1 loads histones remains unknown. Here, we investigated the details concerning Abo1-mediated histone loading onto DNA and the Abo1-DNA interaction using single-molecule imaging techniques and biochemical assays. We show that Abo1 does not load H2A-H2B histones. Interestingly, Abo1 deposits multiple copies of H3-H4 histones as the DNA length increases and requires at least 80 bp DNA. Unexpectedly, Abo1 weakly binds DNA regardless of ATP, and neither histone nor DNA stimulates the ATP hydrolysis activity of Abo1. Based on our results, we propose an allosteric communication model in which the ATP hydrolysis of Abo1 changes the configuration of histones to facilitate their deposition onto DNA.
Keywords
bromodomain-containing AAA+ ATPase; DNA curtain; histone loading; single-molecule photobleaching;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Cho, C., Jang, J., Kang, Y., Watanabe, H., Uchihashi, T., Kim, S.J., Kato, K., Lee, J.Y., and Song, J.J. (2019). Structural basis of nucleosome assembly by the Abo1 AAA+ ATPase histone chaperone. Nat. Commun. 10, 5764.   DOI
2 Dong, W., Oya, E., Zahedi, Y., Prasad, P., Svensson, J.P., Lennartsson, A., Ekwall, K., and Durand-Dubief, M. (2020). Abo1 is required for the H3K9me2 to h3K9me3 transition in heterochromatin. Sci. Rep. 10, 6055.   DOI
3 Dyer, P.N., Edayathumangalam, R.S., White, C.L., Bao, Y., Chakravarthy, S., Muthurajan, U.M., and Luger, K. (2004). Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44.
4 Fierz, B. and Poirier, M.G. (2019). Biophysics of chromatin dynamics. Annu. Rev. Biophys. 48, 321-345.   DOI
5 Gal, C., Murton, H.E., Subramanian, L., Whale, A.J., Moore, K.M., Paszkiewicz, K., Codlin, S., Bähler, J., Creamer, K.M., Partridge, J.F., et al. (2016). Abo1, a conserved bromodomain AAA-ATPase, maintains global nucleosome occupancy and organisation. EMBO Rep. 17, 79-93.   DOI
6 Gradolatto, A., Rogers, R.S., Lavender, H., Taverna, S.D., Allis, C.D., Aitchison, J.D., and Tackett, A.J. (2008). Saccharomyces cerevisiae Yta7 regulates histone gene expression. Genetics 179, 291-304.   DOI
7 Grover, P., Asa, J.S., and Campos, E.I. (2018). H3-H4 histone chaperone pathways. Annu. Rev. Genet. 52, 109-130.   DOI
8 Gurard-Levin, Z.A., Quivy, J.P., and Almouzni, G. (2014). Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83, 487-517.   DOI
9 Lombardi, L.M., Davis, M.D., and Rine, J. (2015). Maintenance of nucleosomal balance in cis by conserved AAA-ATPase Yta7. Genetics 199, 105-116.   DOI
10 Lloyd, J.T., Poplawaski, A., Lubula, M.Y., Carlson, S., Gay, J., and Glass, K.C. (2017). Biological function and histone recognition of family IV bromodomaincontaining proteins. FASEB J. 31 Suppl 1, 755.7.
11 Lowe, J., Ellonen, A., Allen, M.D., Atkinson, C., Sherratt, D.J., and Grainge, I. (2008). Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell 31, 498-509.   DOI
12 Sauer, P.V., Gu, Y., Liu, W.H., Mattiroli, F., Panne, D., Luger, K., and Churchill, M.E. (2018). Mechanistic insights into histone deposition and nucleosome assembly by the chromatin assembly factor-1. Nucleic Acids Res. 46, 9907-9917.   DOI
13 Luger, K., Rechsteiner, T.J., and Richmond, T.J. (1999). Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1-16.
14 Morozumi, Y., Boussouar, F., Tan, M., Chaikuad, A., Jamshidikia, M., Colak, G., He, H., Nie, L., Petosa, C., de Dieuleveult, M., et al. (2016). Atad2 is a generalist facilitator of chromatin dynamics in embryonic stem cells. J. Mol. Cell Biol. 8, 349-362.   DOI
15 Peterson, C.L. and Almouzni, G. (2013). Nucleosome dynamics as modular systems that integrate DNA damage and repair. Cold Spring Harb. Perspect. Biol. 5, a012658.   DOI
16 Shahnejat-Bushehri, S. and Ehrenhofer-Murray, A.E. (2020). The ATAD2/ANCCA homolog Yta7 cooperates with Scm3(HJURP) to deposit Cse4(CENP-A) at the centromere in yeast. Proc. Natl. Acad. Sci. U. S. A. 117, 5386-5393.   DOI
17 Visnapuu, M.L., Fazio, T., Wind, S., and Greene, E.C. (2008). Parallel arrays of geometric nanowells for assembling curtains of DNA with controlled lateral dispersion. Langmuir 24, 11293-11299.   DOI
18 Zou, J.X., Revenko, A.S., Li, L.B., Gemo, A.T., and Chen, H.W. (2007). ANCCA, an estrogen-regulated AAA+ ATPase coactivator for ER alpha, is required for coregulator occupancy and chromatin modification. Proc. Natl. Acad. Sci. U. S. A. 104, 18067-18072.   DOI
19 Zhang, K., Gao, Y., Li, J., Burgess, R., Han, J., Liang, H., Zhang, Z., and Liu, Y. (2016). A DNA binding winged helix domain in CAF-1 functions with PCNA to stabilize CAF-1 at replication forks. Nucleic Acids Res. 44, 5083-5094.   DOI
20 Zhang, M.J., Zhang, C., Du, W., Yang, X., and Chen, Z. (2016). ATAD2 is overexpressed in gastric cancer and serves as an independent poor prognostic biomarker. Clin. Transl. Oncol. 18, 776-781.   DOI
21 Liu, Y., Zhou, K., Zhang, N., Wei, H., Tan, Y.Z., Zhang, Z., Carragher, B., Potter, C.S., D'Arcy, S., and Luger, K. (2020). FACT caught in the act of manipulating the nucleosome. Nature 577, 426-431.   DOI
22 Cheon, N.Y., Kim, H.S., Yeo, J.E., Scharer, O.D., and Lee, J.Y. (2019). Singlemolecule visualization reveals the damage search mechanism for the human NER protein XPC-RAD23B. Nucleic Acids Res. 47, 8337-8347.   DOI
23 Kim, D., Setiaputra, D., Jung, T., Chung, J., Leitner, A., Yoon, J., Aebersold, R., Hebert, H., Yip, C.K., and Song, J.J. (2016). Molecular architecture of yeast chromatin assembly factor 1. Sci. Rep. 6, 26702.   DOI
24 Kim, K., Eom, J., and Jung, I. (2019). Characterization of structural variations in the context of 3D chromatin structure. Mol. Cells 42, 512-522.   DOI
25 Koo, S.J., Fernandez-Montalvan, A.E., Badock, V., Ott, C.J., Holton, S.J., von Ahsen, O., Toedling, J., Vittori, S., Bradner, J.E., and Gorjanacz, M. (2016). ATAD2 is an epigenetic reader of newly synthesized histone marks during DNA replication. Oncotarget 7, 70323-70335.   DOI
26 Lee, J.Y., Finkelstein, I.J., Crozat, E., Sherratt, D.J., and Greene, E.C. (2012). Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK. Proc. Natl. Acad. Sci. U. S. A. 109, 6531-6536.   DOI