HU multimerization shift controls nucleoid compaction

Hammel, Michal; Amlanjyoti, Dhar; Reyes, Francis E.; Chen, Jian-Hua; Parpana, Rochelle; Tang, Henry Y.  H.; Larabell, Carolyn A.; Tainer, John A.; Adhya, Sankar

doi:10.1126/sciadv.1600650

Title: HU multimerization shift controls nucleoid compaction

Journal Article · Fri Jul 01 00:00:00 EDT 2016 · Science Advances

DOI:https://doi.org/10.1126/sciadv.1600650· OSTI ID:1625960

Hammel, Michal ^[1]; Amlanjyoti, Dhar ^[2]; Reyes, Francis E. ^[1]; Chen, Jian-Hua ^[3]; Parpana, Rochelle ^[1]; Tang, Henry Y. H. ^[1]; Larabell, Carolyn A. ^[4]; Tainer, John A. ^[5];

^[2]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
National Inst. of Health (NIH), Bethesda, MD (United States)
Univ. of California, San Francisco, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, San Francisco, CA (United States)
Univ. of Texas, Houston, TX (United States). MD Anderson Cancer Center; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Molecular mechanisms controlling functional bacterial chromosome (nucleoid) compaction and organization are surprisingly enigmatic but partly depend on conserved, histone-like proteins HUαα and HUαβ and their interactions that span the nanoscale and mesoscale from protein-DNA complexes to the bacterial chromosome and nucleoid structure. We determined the crystal structures of these chromosome-associated proteins in complex with native duplex DNA. Distinct DNA binding modes of HUαα and HUαβ elucidate fundamental features of bacterial chromosome packing that regulate gene transcription. By combining crystal structures with solution x-ray scattering results, we determined architectures of HU-DNA nucleoproteins in solution under near-physiological conditions. These macromolecular conformations and interactions result in contraction at the cellular level based on in vivo imaging of native unlabeled nucleoid by soft x-ray tomography upon HUβ and ectopic HUα38 expression. Structural characterization of charge-altered HUαα-DNA complexes reveals an HU molecular switch that is suitable for condensing nucleoid and reprogramming noninvasiveEscherichia coliinto an invasive form. Collective findings suggest that shifts between networking and cooperative and noncooperative DNA-dependent HU multimerization control DNA compaction and supercoiling independently of cellular topoisomerase activity. By integrating x-ray crystal structures, x-ray scattering, mutational tests, and x-ray imaging that span from protein-DNA complexes to the bacterial chromosome and nucleoid structure, we show that defined dynamic HU interaction networks can promote nucleoid reorganization and transcriptional regulation as efficient general microbial mechanisms to help synchronize genetic responses to cell cycle, changing environments, and pathogenesis.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health, Structural Cell Biology of DNA Repair Machines; National Institutes of Health, Macromolecular Insights on Nucleic Acids Optimized by Scattering (MINOS); National Institutes of Health, National Institute of General Medical Sciences; National Institutes of Health, Intramural Research Program; National Cancer Institute, Center for Cancer Research

Grant/Contract Number:: AC02-05CH11231; P01 CA92584; GM105404; P41GM103445

OSTI ID:: 1625960

Journal Information:: Science Advances, Vol. 2, Issue 7; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 62 works

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References (66)

Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival Claret, Laurent; Rouviere-Yaniv, Josette Journal of Molecular Biology, Vol. 273, Issue 1 https://doi.org/10.1006/jmbi.1997.1310	journal	October 1997
Spiral structure of Escherichia coli HU provides foundation for DNA supercoiling Guo, F.; Adhya, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 11 https://doi.org/10.1073/pnas.0611686104	journal	March 2007
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
Major Nucleoid Proteins in the Structure and Function of theEscherichia coliChromosome Johnson, Reid C.; Johnson, Lianna M.; Schmidt, John W. The Bacterial Chromosome https://doi.org/10.1128/9781555817640.ch5	book	April 2014
Nucleoid remodeling by an altered HU protein: Reorganization of the transcription program Kar, S.; Edgar, R.; Adhya, S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 45 https://doi.org/10.1073/pnas.0508032102	journal	October 2005
Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Dorman, Charles J. Nature Reviews Microbiology, Vol. 11, Issue 5 https://doi.org/10.1038/nrmicro3007	journal	April 2013
Effect of Varying the Supercoiling of DNA on Transcription and Its Regulation Lim, Heon M.; Lewis, Dale E. A.; Lee, Hee Jung Biochemistry, Vol. 42, Issue 36 https://doi.org/10.1021/bi030110t	journal	September 2003
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Nonspecific DNA Binding and Bending by HUαβ: Interfaces of the Three Binding Modes Characterized by Salt-Dependent Thermodynamics Koh, Junseock; Shkel, Irina; Saecker, Ruth M. Journal of Molecular Biology, Vol. 410, Issue 2 https://doi.org/10.1016/j.jmb.2011.04.001	journal	July 2011
Small-Angle X-Ray Scattering on Biological Macromolecules and Nanocomposites in Solution Blanchet, Clement E.; Svergun, Dmitri I. Annual Review of Physical Chemistry, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-physchem-040412-110132	journal	April 2013
Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12 Prieto, Ana I.; Kahramanoglou, Christina; Ali, Ruhi M. Nucleic Acids Research, Vol. 40, Issue 8 https://doi.org/10.1093/nar/gkr1236	journal	December 2011
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
IHF and HU: flexible architects of bent DNA Swinger, Kerren K.; Rice, Phoebe A. Current Opinion in Structural Biology, Vol. 14, Issue 1 https://doi.org/10.1016/j.sbi.2003.12.003	journal	February 2004
Proteins in dynamic equilibrium Bernadó, Pau; Blackledge, Martin Nature, Vol. 468, Issue 7327 https://doi.org/10.1038/4681046a	journal	December 2010
Soft X-ray tomography and cryogenic light microscopy: the cool combination in cellular imaging McDermott, Gerry; Le Gros, Mark A.; Knoechel, Christian G. Trends in Cell Biology, Vol. 19, Issue 11 https://doi.org/10.1016/j.tcb.2009.08.005	journal	November 2009
Repressor induced site-specific binding of HU for transcriptional regulation Aki, T. The EMBO Journal, Vol. 16, Issue 12 https://doi.org/10.1093/emboj/16.12.3666	journal	June 1997
HU Binding to a DNA Four-Way Junction Probed by Förster Resonance Energy Transfer Vitoc, Codruta Iulia; Mukerji, Ishita Biochemistry, Vol. 50, Issue 9 https://doi.org/10.1021/bi1007589	journal	March 2011
Dual architectural roles of HU: Formation of flexible hinges and rigid filaments van Noort, J.; Verbrugge, S.; Goosen, N. Proceedings of the National Academy of Sciences, Vol. 101, Issue 18 https://doi.org/10.1073/pnas.0308230101	journal	April 2004
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Putnam, Christopher D.; Hammel, Michal; Hura, Greg L. Quarterly Reviews of Biophysics, Vol. 40, Issue 3 https://doi.org/10.1017/S0033583507004635	journal	August 2007
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Flexible DNA bending in HU-DNA cocrystal structures Swinger, K. K. The EMBO Journal, Vol. 22, Issue 14 https://doi.org/10.1093/emboj/cdg351	journal	July 2003
Conversion of Commensal Escherichia coli K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein Koli, Preeti; Sudan, Sudhanshu; Fitzgerald, David mBio, Vol. 2, Issue 6 https://doi.org/10.1128/mbio.00263-11	journal	December 2011
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
The histone-like protein HU binds specifically to DNA recombination and repair intermediates Kamashev, D. The EMBO Journal, Vol. 19, Issue 23 https://doi.org/10.1093/emboj/19.23.6527	journal	December 2000
Understanding Apparent DNA Flexibility Enhancement by HU and HMGB Architectural Proteins Czapla, Luke; Peters, Justin P.; Rueter, Emily M. Journal of Molecular Biology, Vol. 409, Issue 2 https://doi.org/10.1016/j.jmb.2011.03.050	journal	June 2011
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
Computational studies of polyurethanases from Pseudomonas do Canto, Vanessa Petry; Thompson, Claudia Elizabeth; Netz, Paulo Augusto Journal of Molecular Modeling, Vol. 27, Issue 2 https://doi.org/10.1007/s00894-021-04671-x	journal	January 2021
Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS) Hammel, Michal European Biophysics Journal, Vol. 41, Issue 10 https://doi.org/10.1007/s00249-012-0820-x	journal	May 2012
Shaping the Borrelia burgdorferi genome: crystal structure and binding properties of the DNA-bending protein Hbb Mouw, Kent W.; Rice, Phoebe A. Molecular Microbiology, Vol. 63, Issue 5 https://doi.org/10.1111/j.1365-2958.2007.05586.x	journal	March 2007
Twelve Species of the Nucleoid-associated Protein from Escherichia coli: SEQUENCE RECOGNITION SPECIFICITY AND DNA BINDING AFFINITY Azam, Talukder Ali; Ishihama, Akira Journal of Biological Chemistry, Vol. 274, Issue 46 https://doi.org/10.1074/jbc.274.46.33105	journal	November 1999
Implementation and performance of SIBYLS: a dual endstation small-angle X-ray scattering and macromolecular crystallography beamline at the Advanced Light Source Classen, Scott; Hura, Greg L.; Holton, James M. Journal of Applied Crystallography, Vol. 46, Issue 1 https://doi.org/10.1107/S0021889812048698	journal	January 2013
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach Dyer, Kevin N.; Hammel, Michal; Rambo, Robert P. Structural Genomics https://doi.org/10.1007/978-1-62703-691-7_18	book	October 2013
Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Prieto, Ana I.; Kahramanoglou, Christina; Ali, Raghib Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.26768	text	January 2012
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
X-ray tomography of whole cells Le Gros, Mark A.; McDermott, Gerry; Larabell, Carolyn A. Current Opinion in Structural Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.sbi.2005.08.008	journal	October 2005
Die Röntgenkleinwinkelstreuung von dichtgepackten kolloiden Systemen Porod, G. Kolloid-Zeitschrift, Vol. 133, Issue 1 https://doi.org/10.1007/bf01513908	journal	October 1953
Organization and segregation of bacterial chromosomes Wang, Xindan; Llopis, Paula Montero; Rudner, David Z. Nature Reviews Genetics, Vol. 14, Issue 3 https://doi.org/10.1038/nrg3375	journal	February 2013
Chromosome Organization by a Nucleoid-Associated Protein in Live Bacteria Wang, W.; Li, G. -W.; Chen, C. Science, Vol. 333, Issue 6048 https://doi.org/10.1126/science.1204697	journal	September 2011
Right-handed DNA Supercoiling by an Octameric Form of Histone-like Protein HU: MODULATION OF CELLULAR TRANSCRIPTION Kar, Sudeshna; Choi, Eugene J.; Guo, Fusheng Journal of Biological Chemistry, Vol. 281, Issue 52 https://doi.org/10.1074/jbc.M605576200	journal	October 2006
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Die Röntgenkleinwinkelstreuung von dichtgepackten kolloiden Systemen: I. Teil Porod, G. Kolloid-Zeitschrift, Vol. 124, Issue 2 https://doi.org/10.1007/BF01512792	journal	November 1951
The DNA-Binding Protein HU has a Regulatory Role in the Acid Stress Response Mechanism in Helicobacter pylori Almarza, Oscar; Núñez, Daniel; Toledo, Hector Helicobacter, Vol. 20, Issue 1 https://doi.org/10.1111/hel.12171	journal	September 2014
Crystal Structure of an IHF-DNA Complex: A Protein-Induced DNA U-Turn Rice, Phoebe A.; Yang, Shu-wei; Mizuuchi, Kiyoshi Cell, Vol. 87, Issue 7, p. 1295-1306 https://doi.org/10.1016/S0092-8674(00)81824-3	journal	December 1996
Structure and Function of Bacterial Sigma Factors Helmann, John D.; Chamberlin, Michael J. Annual Review of Biochemistry, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.bi.57.070188.004203	journal	June 1988
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
E. coli DNA binding protein HU forms nucleosome-like structure with circular double-stranded DNA Rouvière-Yaniv, Josette; Yaniv, Moshe; Germond, Jacques-Edouard Cell, Vol. 17, Issue 2 https://doi.org/10.1016/0092-8674(79)90152-1	journal	June 1979
DNA Binding Mode Transitions of Escherichia coli HUαβ: Evidence for Formation of a Bent DNA — Protein Complex on Intact, Linear Duplex DNA Koh, Junseock; Saecker, Ruth M.; Record, M. Thomas Journal of Molecular Biology, Vol. 383, Issue 2 https://doi.org/10.1016/j.jmb.2008.07.024	journal	November 2008
Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law Rambo, Robert P.; Tainer, John A. Biopolymers, Vol. 95, Issue 8 https://doi.org/10.1002/bip.21638	journal	April 2011
Modulation of HU–DNA interactions by salt concentration and applied force Xiao, Botao; Johnson, Reid C.; Marko, John F. Nucleic Acids Research, Vol. 38, Issue 18 https://doi.org/10.1093/nar/gkq435	journal	May 2010
Data processing and analysis with the autoPROC toolbox Vonrhein, Clemens; Flensburg, Claus; Keller, Peter Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007773	journal	March 2011
Structure and flexibility within proteins as identified through small angle X-ray scattering Pelikan, M.; Hura, G.; Hammel, M. General Physiology and Biophysics, Vol. 28, Issue 2 https://doi.org/10.4149/gpb_2009_02_174	journal	January 2009
Bacterial nucleoid-associated proteins, nucleoid structure and gene expression Dillon, Shane C.; Dorman, Charles J. Nature Reviews Microbiology, Vol. 8, Issue 3 https://doi.org/10.1038/nrmicro2261	journal	February 2010
Promoter selectivity of prokaryotic RNA polymerases Ishihama, Akira Trends in Genetics, Vol. 4, Issue 10 https://doi.org/10.1016/0168-9525(88)90170-9	journal	October 1988
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
Recruitment of HU by piggyback: a special role of GalR in repressosome assembly Kar, S. Genes & Development, Vol. 15, Issue 17 https://doi.org/10.1101/gad.920301	journal	September 2001
Chromosome Organization by a Nucleoid-Associated Protein in Live Bacteria Chen, Chongyi; Wang, Wenqin; Li, Gene-Wei Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.11.2628	journal	January 2012
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER Smart, Oliver S.; Womack, Thomas O.; Flensburg, Claus Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444911056058	journal	March 2012
Die Röntgenkleinwinkelstreuung von dichtgepackten kolloiden Systemen: II. Teil Porod, G. Kolloid-Zeitschrift, Vol. 125, Issue 1 https://doi.org/10.1007/bf01519615	journal	January 1952
DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Dorman, C. J. Infection and Immunity, Vol. 59, Issue 3 https://doi.org/10.1128/iai.59.3.745-749.1991	journal	January 1991
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Structure and dynamics of the DNA binding protein HU from Bacillus stearothermophilus by NMR spectroscopy Boelens, Rolf; Vis, Hans; Vorgias, Constantin E. Biopolymers, Vol. 40, Issue 5 https://doi.org/10.1002/(sici)1097-0282(1996)40:5<553::aid-bip13>3.0.co;2-i	journal	January 1996
Evidence of a Thermal Unfolding Dimeric Intermediate for the Escherichia coli Histone-like HU Proteins: Thermodynamics and Structure Ramstein, Jean; Hervouet, Nadège; Coste, Franck Journal of Molecular Biology, Vol. 331, Issue 1 https://doi.org/10.1016/s0022-2836(03)00725-3	journal	August 2003
Growth Phase-Dependent Variation in Protein Composition of the Escherichia coli Nucleoid Ali Azam, Talukder; Iwata, Akira; Nishimura, Akiko Journal of Bacteriology, Vol. 181, Issue 20 https://doi.org/10.1128/jb.181.20.6361-6370.1999	journal	October 1999
Conversion of Commensal Escherichia coli K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein Koli, Preeti; Sudan, Sudhanshu; Fitzgerald, David mBio, Vol. 2, Issue 5 https://doi.org/10.1128/mbio.00182-11	journal	September 2011

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