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The Actin-Related Protein BAF53 Is Essential for Chromosomal Subdomain Integrity

  • Lee, Kiwon (Department of Bioscience and Biotechnology and Protein Research Center for Bio-Industry, Hankuk University of Foreign Studies) ;
  • Kim, Ji Hye (Department of Bioscience and Biotechnology and Protein Research Center for Bio-Industry, Hankuk University of Foreign Studies) ;
  • Kwon, Hyockman (Department of Bioscience and Biotechnology and Protein Research Center for Bio-Industry, Hankuk University of Foreign Studies)
  • Received : 2015.04.24
  • Accepted : 2015.05.28
  • Published : 2015.09.30

Abstract

A chromosome territory is composed of chromosomal subdomains. The internal structure of chromosomal subdomains provides a structural framework for many genomic activities such as replication and DNA repair, and thus is key to determining the basis of their mechanisms. However, the internal structure and regulating proteins of a chromosomal subdomain remains elusive. Previously, we showed that the chromosome territory expanded after BAF53 knockdown. Because the integrity of chromosomal subdomains is a deciding factor of the volume of a chromosome territory, we examined here the effect of BAF53 knockdown on chromosomal subdomains. We found that BAF53 knockdown led to the disintegration of histone H2B-GFP-visualized chromosomal subdomains and BrdU-labeled replication foci. In addition, the size of DNA loops measured by the maximum fluorescent halo technique increased and became irregular after BAF53 knockdown, indicating DNA loops were released from the residual nuclear structure. These data can be accounted for by the model that BAF53 is prerequisite for maintaining the structural integrity of chromosomal subdomains.

Acknowledgement

Supported by : National Research Foundation of Korea

References

  1. Albiez, H., Cremer, M., Tiberi, C., Vecchio, L., Schermelleh, L., Dittrich, S., Kupper, K., Joffe, B., Thormeyer, T., von Hase, J., et al. (2006). Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Chromosome Res. 14, 707-733. https://doi.org/10.1007/s10577-006-1086-x
  2. Andersson, K., Bjorkroth, B., and Daneholt, B. (1980). The in situ structure of the active 75 S RNA genes in Balbiani rings of Chironomus tentans. Exp. Cell Res. 130, 313-326. https://doi.org/10.1016/0014-4827(80)90008-7
  3. Belmont, A.S., and Bruce, K. (1994). Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure. J. Cell Biol. 127, 287-302. https://doi.org/10.1083/jcb.127.2.287
  4. Buongiorno-Nardelli, M., Micheli, G., Carri, M.T., and Marilley, M. (1982). A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298, 100-102. https://doi.org/10.1038/298100a0
  5. Cayrou, C., Coulombe, P., and Mechali, M. (2010). Programming DNA replication origins and chromosome organization. Chromosome Res. 18, 137-145. https://doi.org/10.1007/s10577-009-9105-3
  6. Cremer, T., and Cremer, M. (2010). Chromosome territories. Cold Spring Harb. Perspect. Biol. 2, a003889.
  7. Cremer, T., Kreth, G., Koester, H., Fink, R.H., Heintzmann, R., Cremer, M., Solovei, I., Zink, D., and Cremer, C. (2000). Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture. Crit. Rev. Eukaryot. Gene Expr. 10, 179-212.
  8. Dixon, J.R., Selvaraj. S., Yue. F., Kim. A., Li. Y., Shen. Y., Hu. M., Liu. J.S., and Ren, B. (2012), Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380. https://doi.org/10.1038/nature11082
  9. Jackson, D.A., and Pombo, A. (1998). Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140, 1285-1295. https://doi.org/10.1083/jcb.140.6.1285
  10. Ji, L., Xu, R., Lu, L., Zhang, J., Yang, G., Huang, J., Wu, C., and Zheng, C. (2013). TM6, a novel nuclear matrix attachment region, enhances its flanking gene expression through influencing their chromatin structure. Mol. Cells 36,127-137. https://doi.org/10.1007/s10059-013-0092-z
  11. Kanda, T., Sullivan, K.F., and Wahl, G.M. (1998). Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385. https://doi.org/10.1016/S0960-9822(98)70156-3
  12. Kennedy, B.K., Barbie, D.A., Classon, M., Dyson, N., and Harlow, E. (2000). Nuclear organization of DNA replication in primary mammalian cells. Genes Dev. 14, 2855-2868. https://doi.org/10.1101/gad.842600
  13. Kwon, S.J., and Kwon, H. (2012). Actin-related protein BAF53 is essential for the formation of replication foci. Anim. Cells Syst. 16, 183-189. https://doi.org/10.1080/19768354.2011.642085
  14. Lark, C.G., Consigli, R., and Toliver, A. (1971). DNA replication in Chinese hamster cells: evidence for a single replication fork per replicon. J. Mol. Biol. 58, 873-875. https://doi.org/10.1016/0022-2836(71)90046-5
  15. Lee, J.H., Chang, S.H., Shim, J.H., Lee, J.Y., Yoshida, M., and Kwon, H. (2003). Cytoplasmic localization and nucleocytoplasmic shuttling of BAF53, a component of chromatinmodifying complexes. Mol. Cells 16, 78-83.
  16. Lee, K., Kang, M.J., Kwon, S.J., Kwon, Y.K., Kim, K.W., Lim, J.H., and Kwon, H. (2007). Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol. Biol. Cell 18, 4013-4023. https://doi.org/10.1091/mbc.E07-05-0437
  17. Leonhardt, H., Rahn, H.P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D., and Cardoso, M.C. (2000). Dynamics of DNA replication factories in living cells. J. Cell Biol. 149, 271-280. https://doi.org/10.1083/jcb.149.2.271
  18. Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O., et al. (2009). Comprehensive mapping of longrange interactions reveals folding principles of the human genome. Science 326, 289-293. https://doi.org/10.1126/science.1181369
  19. Michalet, X., Ekong, R., Fougerousse, F., Rousseaux, S., Schurra, C., Hornigold, N., van Slegtenhorst, M., Wolfe, J., Povey, S., Beckmann, J.S., Bensimon, A., et al. (1997). Dynamic molecular combing: stretching the whole human genome for highresolution studies. Science 277, 1518-1523. https://doi.org/10.1126/science.277.5331.1518
  20. Mirny, L.A. (2011). The fractal globule as a model of chromatin architecture in the cell. Chromosome Res. 19, 37-51.
  21. Muck, J., and Zink, D. (2009). Nuclear organization and dynamics of DNA replication in eukaryotes. Front. Biosci. 14, 5361-5371. https://doi.org/10.2741/3600
  22. Muller, W.G., Walker, D., Hager, G.L., and McNally, J.G. (2001). Large-scale chromatin decondensation and recondensation regulated by transcription from a natural promoter. J. Cell Biol. 154, 33-48. https://doi.org/10.1083/jcb.200011069
  23. Muller, W.G., Rieder, D., Kreth, G., Cremer, C., Trajanoski, Z., and McNally, J.G. (2004). Generic features of tertiary chromatin structure as detected in natural chromosomes. Mol. Cell Biol. 24, 9359-9370. https://doi.org/10.1128/MCB.24.21.9359-9370.2004
  24. Munkel, C., Eils, R., Dietzel, S., Zink, D., Mehring, C., Wedemann, G., Cremer, T., and Langowski, J. (1999). Compartmentalization of interphase chromosomes observed in simulation and experiment. J. Mol. Biol. 285, 1053-1065. https://doi.org/10.1006/jmbi.1998.2361
  25. O'Keefe, R.T., Henderson, S.C., and Spector, D.L. (1992). Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J. Cell Biol. 116, 1095-1110. https://doi.org/10.1083/jcb.116.5.1095
  26. Rao, S.S., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., and Aiden, E.L. (2014). A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680. https://doi.org/10.1016/j.cell.2014.11.021
  27. Rando, O.J., Zhao, K., Janmey, P., and Crabtree, G.R. (2002). Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl. Acad. Sci. USA 99, 2824-2829. https://doi.org/10.1073/pnas.032662899
  28. Spring, H., and Franke, W.W. (1981). Transcriptionally active chromatin in loops of lampbrush chromosomes at physiological salt concentrations as revealed by electron microscopy of sections. Eur. J. Cell Biol. 24, 298-308.
  29. Sung, Y.H., Choi, E.Y., and Kwon, H. (2001). Identification of a nuclear protein ArpN as a component of human SWI/SNF complex and its selective association with a subset of active genes. Mol. Cells 11, 75-81.
  30. Tumbar, T., Sudlow, G., and Belmont, A.S. (1999). Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J. Cell Biol. 145, 1341-1354. https://doi.org/10.1083/jcb.145.7.1341
  31. Vogelstein, B., Pardoll, D.M., and Coffey, D.S. (1980). Supercoiled loops and eucaryotic DNA replicaton. Cell 22, 79-85. https://doi.org/10.1016/0092-8674(80)90156-7
  32. Zhao, K., Wang, W., Rando, O.J., Xue, Y., Swiderek, K., Kuo, A., and Crabtree, G.R. (1998). Rapid and phosphoinositoldependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95, 625-636. https://doi.org/10.1016/S0092-8674(00)81633-5
  33. Zink, D., Bornfleth, H., Visser, A., Cremer, C., and Cremer, T. (1999). Organization of early and late replicating DNA in human chromosome territories. Exp. Cell Res. 247, 176-188. https://doi.org/10.1006/excr.1998.4311