Alba shapes the archaeal genome using a delicate balance of bridging and stiffening the DNA

Nature Communications

Volumn 3, Issue , 2012, Pages

  Laurens, Niels ^a   Driessen, Rosalie P C ^b   Heller, Iddo ^a   Vorselen, Daan ^a   Noom, Maarten C ^a   Hol, Felix J H ^a   White, Malcolm F ^c   Dame, Remus T ^a,b   Wuite, Gijs J L ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALBA1 PROTEIN; ALBA2 PROTEIN; ARCHAEAL PROTEIN; BACTERIAL DNA; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

GENE EXPRESSION; GENOME; MITOCHONDRIAL DNA; PROKARYOTE; PROTEIN;

ARCHAEAL GENOME; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENETIC MANIPULATION; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR MODEL; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FOLDING; PROTEIN FUNCTION;

ARCHAEA;

EID: 84871815721     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2330     Document Type: Article

References (44)

1. Odijk, T. Osmotic compaction of supercoiled DNA into a bacterial nucleoid. Biophys. Chem. 73, 23-29 (1998). (Pubitemid 28325691)
2. Luijsterburg, M. S., White, M. F., van Driel, R. & Dame, R. T. The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit. Rev. Biochem. Mol. Biol. 43, 393-418 (2008).
3. van Noort, J., Verbrugge, S., Goosen, N., Dekker, C. & Dame, R. T. Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc. Natl Acad. Sci. USA 101, 6969-6974 (2004). (Pubitemid 38596427)
4. Dame, R. T., Noom, M. C. & Wuite, G. J. Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444, 387-390 (2006). (Pubitemid 44764116)
5. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 (1997). (Pubitemid 27406632)
6. Misteli, T. Higher-order genome organization in human disease. Cold Spring Harb. Perspect. Biol. 2, a000794 (2010).
7. Tark-Dame, M., van Driel, R. & Heermann, D. W. Chromatin folding - from biology to polymer models and back. J. Cell Sci. 124, 839-845 (2011).
8. Dorsett, D. Cohesin: genomic insights into controlling gene transcription and development. Curr. Opin. Genet. Dev. 21, 199-206 (2011).
9. Zlatanova, J. & Caiafa, P. CCCTC-binding factor: to loop or to bridge. Cell Mol. Life Sci. 66, 1647-1660 (2009).
10. Kucej, M. & Butow, R. A. Evolutionary tinkering with mitochondrial nucleoids. Trends Cell Biol. 17, 586-592 (2007). (Pubitemid 350138432)
11. Farge, G. et al. Protein sliding and DNA denaturation are essential for DNA organization by human mitochondrial transcription factor A. Nat. Commun. 3, 1013 (2012).
12. Bell, S. D. & White, M. F. in Bacterial Chromatin. (eds Dame, R. T. & Dorman, C. J.) Ch. 10 205-217 (Springer, 2010).
13. White, M. F. & Bell, S. D. Holding it together: chromatin in the archaea. Trends Genet. 18, 621-626 (2002). (Pubitemid 35346685)
14. Kelman, Z. & White, M. F. Archaeal DNA replication and repair. Curr. Opin. Microbiol. 8, 669-676 (2005). (Pubitemid 41643035)
15. Sandman, K., Krzycki, J. A., Dobrinski, B., Lurz, R. & Reeve, J. N. HMf, a DNAbinding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc. Natl Acad. Sci. USA 87, 5788-5791 (1990).
16. Driessen, R. P. C. & Dame, R. T. Nucleoid-associated proteins in Crenarchaea. Biochem. Soc. Trans. 39, 116-121 (2011).
17. Lurz, R., Grote, M., Dijk, J., Reinhardt, R. & Dobrinski, B. Electron microscopic study of DNA complexes with proteins from the archaebacterium Sulfolobus acidocaldarius. EMBO J. 5, 3715-3721 (1986).
18. Forterre, P., Confalonieri, F. & Knapp, S. Identification of the gene encoding archeal-specific DNA-binding proteins of the Sac10b family. Mol. Microbiol. 32, 669-670 (1999). (Pubitemid 29233909)
19. Xue, H., Guo, R., Wen, Y., Liu, D. & Huang, L. An abundant DNA binding protein from the hyperthermophilic archaeon Sulfolobus shibatae affects DNA supercoiling in a temperature-dependent fashion. J. Bacteriol. 182, 3929-3933 (2000). (Pubitemid 30436552)
20. Grote, M., Dijk, J. & Reinhardt, R. Ribosomal and DNA binding proteins of the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biochim. Biophys. Acta. 873, 405-413 (1986). (Pubitemid 16002294)
21. Jelinska, C. et al. Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging. Structure 13, 963-971 (2005). (Pubitemid 40943328)
22. Wardleworth, B. N., Russell, R. J., Bell, S. D., Taylor, G. L. & White, M. F. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J. 21, 4654-4662 (2002). (Pubitemid 34984352)
23. Tanaka, T., Padavattan, S. & Kumarevel, T. Crystal structure of archaeal chromatin protein Alba2-double-stranded DNA complex from Aeropyrum pernix K1. J. Biol. Chem. 287, 10394-10402 (2012).
24. Jelinska, C., Petrovic-Stojanovska, B., Ingledew, W. J. & White, M. F. Dimerdimer stacking interactions are important for nucleic acid binding by the archaeal chromatin protein Alba. Biochem. J. 427, 49-55 (2010).
25. Wurtzel, O. et al. A single-base resolution map of an archaeal transcriptome. Genome Res. 20, 133-141 (2010).
26. Chou, C. C., Lin, T. W., Chen, C. Y. & Wang, A. H. Crystal structure of the hyperthermophilic archaeal DNA-binding protein Sso10b2 at a resolution of 1.85 Angstroms. J. Bacteriol. 185, 4066-4073 (2003). (Pubitemid 36835245)
27. Dame, R. T. Single-molecule micromanipulation studies of DNA and architectural proteins. Biochem. Soc. Trans. 36, 732-737 (2008).
28. Chaurasiya, K. R., Paramanathan, T., Mccauley, M. J. & Williams, M. C. Biophysical characterization of DNA binding from single molecule force measurements. Phys. Life Rev. 1-43 (2010).
29. Gross, P. et al. Quantifying how DNA stretches, melts and changes twist under tension. Nat. Phys. 7, 731-736 (2011).
30. Bell, S. D., Botting, C. H.,Wardleworth, B. N., Jackson, S. P. &White, M. F. The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science 296, 148-151 (2002). (Pubitemid 34280075)
31. Lim, C. J., Whang, Y. R., Kenney, L. J. & Yan, J. Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res. 40, 3316-3328 (2012).
32. Winardhi, R. S. et al. Higher order oligomerization is required for H-NS family member MvaT to form gene-silencing nucleoprotein filament. Nucleic Acids Res. 40, 8942-8952 (2012).
33. Dame, R. T., Kalmykowa, O. J. & Grainger, D. C. Chromosomal macrodomains and associated proteins: implications for DNA organization and replication in gram negative bacteria. PLoS Genet. 7, e1002123 (2011).
34. Postow, L., Hardy, C. D., Arsuaga, J. & Cozzarelli, N. R. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 18, 1766-1779 (2004). (Pubitemid 38938191)
35. Higgins, N. P., Yang, X., Fu, Q. & Roth, J. R. Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium. J. Bacteriol. 178, 2825-2835 (1996). (Pubitemid 26144039)
36. Noom, M. C., Navarre, W. W., Oshima, T., Wuite, G. J. & Dame, R. T. H-NS promotes looped domain formation in the bacterial chromosome. Curr. Biol. 17, R913-R914 (2007). (Pubitemid 350016916)
37. Wiggins, P. A., Dame, R. T., Noom, M. C. & Wuite, G. J. Protein-mediated molecular bridging: a key mechanism in biopolymer organization. Biophys. J. 97, 1997-2003 (2009).
38. Liu, Y., Chen, H., Kenney, L. J. & Yan, J. A divalent switch drives H-NS/DNAbinding conformations between stiffening and bridging modes. Genes Dev. 24, 339-344 (2010).
39. Lim,C. J., Lee, S. Y.,Kenney, L. J. & Yan, J.Nucleoprotein filament formation is the structural basis for bacterial protein H-NS gene silencing. Sci. Rep. 2, 509 (2012).
40. Dorman, C. J. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2, 391-400 (2004).
41. Noom, M. C., van den Broek, B., van Mameren, J.v. & Wuite, G. J. L. Visualizing single DNA-bound proteins using DNA as a scanning probe. Nat. Methods 4, 1031-1036 (2007). (Pubitemid 350201775)
42. Mangeol, P. & Bockelmann, U. Interference and crosstalk in double optical tweezers using a single laser source. Rev. Sci. Instrum. 79, 083103 (2008).
43. Odijk, T. Stiff chains and filaments under tension. Macromolecules 28, 7016-7018 (1995).
44. McGhee, J. D. & von Hippel, P. H. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J. Mol. Biol. 86, 469-489 (1974).