Ionic switch controls the DNA state in phage λ

Li, Dong; Liu, Ting; Zuo, Xiaobing; Li, Tao; Qiu, Xiangyun; Evilevitch, Alex

doi:10.1093/nar/gkv611

Ionic switch controls the DNA state in phage λ

Journal Article · Fri Jun 19 00:00:00 EDT 2015 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkv611· OSTI ID:1221840

Li, Dong ^[1]; Liu, Ting ^[1]; Zuo, Xiaobing ^[2]; Li, Tao ^[2]; Qiu, Xiangyun ^[3]; Evilevitch, Alex ^[4]

Carnegie Mellon Univ., Pittsburgh, PA (United States). Physics Dept.
Argonne National Lab., Argonne, IL (United States). Advanced Photon Source, X-ray Science Div.
George Washington Univ., Washington, DC (United States). Dept. of Physics.
Carnegie Mellon Univ., Pittsburgh, PA (United States). Physics Dept.; Lund Univ., Lund (Sweden). Dept. of Biochemistry and Structural Biology.

We have recently found that DNA packaged in phage λ undergoes a disordering transition triggered by temperature, which results in increased genome mobility. This solid-to-fluid like DNA transition markedly increases the number of infectious λ particles facilitating infection. However, the structural transition strongly depends on temperature and ionic conditions in the surrounding medium. Using titration microcalorimetry combined with solution X-ray scattering, we mapped both energetic and structural changes associated with transition of the encapsidated λ-DNA. Packaged DNA needs to reach a critical stress level in order for transition to occur. We varied the stress on DNA in the capsid by changing the temperature, packaged DNA length and ionic conditions. We found striking evidence that the intracapsid DNA transition is ‘switched on’ at the ionic conditions mimicking those in vivo and also at the physiologic temperature of infection at 37°C. This ion regulated on-off switch of packaged DNA mobility in turn affects viral replication. The results suggest a remarkable adaptation of phage λ to the environment of its host bacteria in the human gut. The metastable DNA state in the capsid provides a new paradigm for the physical evolution of viruses.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1221840

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 13 Vol. 43; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (96)

Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. Lepault, J.; Dubochet, J.; Baschong, W. The EMBO Journal, Vol. 6, Issue 5 https://doi.org/10.1002/j.1460-2075.1987.tb02393.x	journal	May 1987
Polyamines: Mysterious Modulators of Cellular Functions Igarashi, Kazuei; Kashiwagi, Keiko Biochemical and Biophysical Research Communications, Vol. 271, Issue 3 https://doi.org/10.1006/bbrc.2000.2601	journal	May 2000
DNA packaging by the double-stranded DNA bacteriophages Earnshaw, William C.; Casjens, Sherwood R. Cell, Vol. 21, Issue 2 https://doi.org/10.1016/0092-8674(80)90468-7	journal	September 1980
DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry Jeembaeva, Meerim; Jönsson, Bengt; Castelnovo, Martin Biophysical Journal, Vol. 96, Issue 3 https://doi.org/10.1016/j.bpj.2008.12.1856	journal	February 2009
Influence of Internal Capsid Pressure on Viral Infection by Phage λ Köster, Sarah; Evilevitch, Alex; Jeembaeva, Meerim Biophysical Journal, Vol. 97, Issue 6 https://doi.org/10.1016/j.bpj.2009.07.007	journal	September 2009
Temperature Dependence of DNA Persistence Length Geggier, Stephanie; Kotlyar, Alexander; Vologodskii, Alexander Biophysical Journal, Vol. 100, Issue 3 https://doi.org/10.1016/j.bpj.2010.12.621	journal	February 2011
Building a Virus from Scratch: Assembly of an Infectious Virus Using Purified Components in a Rigorously Defined Biochemical Assay System Gaussier, Hélène; Yang, Qin; Catalano, Carlos Enrique Journal of Molecular Biology, Vol. 357, Issue 4 https://doi.org/10.1016/j.jmb.2006.01.013	journal	April 2006
Forces Controlling the Rate of DNA Ejection from Phage λ Löf, David; Schillén, Karin; Jönsson, Bengt Journal of Molecular Biology, Vol. 368, Issue 1 https://doi.org/10.1016/j.jmb.2007.01.076	journal	April 2007
Forces and Pressures in DNA Packaging and Release from Viral Capsids Tzlil, Shelly; Kindt, James T.; Gelbart, William M. Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/s0006-3495(03)74971-6	journal	March 2003
Condensed phases of DNA: Structures and phase transitions Livolant, Françoise; Leforestier, Amélie Progress in Polymer Science, Vol. 21, Issue 6 https://doi.org/10.1016/s0079-6700(96)00016-0	journal	January 1996
Encapsidated Conformation of Bacteriophage T7 DNA Cerritelli, Mario E.; Cheng, Naiqian; Rosenberg, Alan H. Cell, Vol. 91, Issue 2 https://doi.org/10.1016/s0092-8674(00)80409-2	journal	October 1997
DNA-DNA interactions Strey, Helmut H.; Podgornik, Rudi; Rau, Donald C. Current Opinion in Structural Biology, Vol. 8, Issue 3 https://doi.org/10.1016/s0959-440x(98)80063-8	journal	June 1998
Spontaneous Sharp Bending of Double-Stranded DNA Cloutier, Timothy E.; Widom, Jonathan Molecular Cell, Vol. 14, Issue 3 https://doi.org/10.1016/s1097-2765(04)00210-2	journal	May 2004
Herpes Virus Genome, The Pressure Is On Bauer, David W.; Huffman, Jamie B.; Homa, Fred L. Journal of the American Chemical Society, Vol. 135, Issue 30 https://doi.org/10.1021/ja404008r	journal	July 2013
Binding of Intercalating and Groove-Binding Cyanine Dyes to Bacteriophage T5 Eriksson, Maja; Härdelin, Maria; Larsson, Anette The Journal of Physical Chemistry B, Vol. 111, Issue 5 https://doi.org/10.1021/jp064322m	journal	February 2007
Mechanistic Insight into the Structure and Dynamics of Entangled and Hydrated λ-Phage DNA Chakraborty, Sandipan; Uematsu, Takashi; Svanberg, Christer The Journal of Physical Chemistry A, Vol. 116, Issue 17 https://doi.org/10.1021/jp2108363	journal	April 2012
Molecular biology: DNA bending and kinking Widom, Jonathan Nature, Vol. 309, Issue 5966 https://doi.org/10.1038/309312a0	journal	May 1984
The exchange properties of magnesium in Escherichia coli ribosomes Rodgers, A. Biochemical Journal, Vol. 90, Issue 3 https://doi.org/10.1042/bj0900548	journal	March 1964
Microbial magnesium transport: unusual transporters searching for identity Smith, Ronald L.; Maguire, Michael E. Molecular Microbiology, Vol. 28, Issue 2 https://doi.org/10.1046/j.1365-2958.1998.00810.x	journal	April 1998
Real-time observations of single bacteriophage DNA ejections in vitro Grayson, P.; Han, L.; Winther, T. Proceedings of the National Academy of Sciences, Vol. 104, Issue 37 https://doi.org/10.1073/pnas.0703274104	journal	September 2007
Osmotic pressure inhibition of DNA ejection from phage Evilevitch, A.; Lavelle, L.; Knobler, C. M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 16 https://doi.org/10.1073/pnas.1233721100	journal	July 2003
Solid-to-fluid-like DNA transition in viruses facilitates infection Liu, T.; Sae-Ueng, U.; Li, D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1321637111	journal	September 2014
DNA packaging and ejection forces in bacteriophage Kindt, J.; Tzlil, S.; Ben-Shaul, A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 24 https://doi.org/10.1073/pnas.241486298	journal	November 2001
Compartmentalization of Spermine and Spermidine in the Herpes Simplex Virion Gibson, W.; Roizman, B. Proceedings of the National Academy of Sciences, Vol. 68, Issue 11 https://doi.org/10.1073/pnas.68.11.2818	journal	November 1971
The design of an agent to bend DNA. Akiyama, T.; Hogan, M. E. Proceedings of the National Academy of Sciences, Vol. 93, Issue 22 https://doi.org/10.1073/pnas.93.22.12122	journal	October 1996
Strained DNA is kinked by low concentrations of Zn2+ Han, W.; Dlakic, M.; Zhu, Y. J. Proceedings of the National Academy of Sciences, Vol. 94, Issue 20 https://doi.org/10.1073/pnas.94.20.10565	journal	September 1997
Kinking the double helix by bending deformation Du, Quan; Kotlyar, Alexander; Vologodskii, Alexander Nucleic Acids Research, Vol. 36, Issue 4 https://doi.org/10.1093/nar/gkm1125	journal	December 2007
DNA bending-induced phase transition of encapsidated genome in phage Lander, G. C.; Johnson, J. E.; Rau, D. C. Nucleic Acids Research, Vol. 41, Issue 8 https://doi.org/10.1093/nar/gkt137	journal	February 2013
Why genes overlap in viruses Chirico, Nicola; Vianelli, Alberto; Belshaw, Robert Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1701 https://doi.org/10.1098/rspb.2010.1052	journal	June 2010
Exact theory of kinkable elastic polymers Wiggins, Paul A.; Phillips, Rob; Nelson, Philip C. Physical Review E, Vol. 71, Issue 2 https://doi.org/10.1103/physreve.71.021909	journal	February 2005
Localized Single-Stranded Bubble Mechanism for Cyclization of Short Double Helix DNA Yan, Jie; Marko, John F. Physical Review Letters, Vol. 93, Issue 10 https://doi.org/10.1103/physrevlett.93.108108	journal	September 2004
Repulsion of Superinfecting Virions: A Mechanism for Rapid Virus Spread Doceul, V.; Hollinshead, M.; van der Linden, L. Science, Vol. 327, Issue 5967 https://doi.org/10.1126/science.1183173	journal	January 2010
Effect of Salt Shock on Stability of λimm434 Lysogens Shkilnyj, Paul; Koudelka, Gerald B. Journal of Bacteriology, Vol. 189, Issue 8 https://doi.org/10.1128/jb.01857-06	journal	February 2007
Defect in the Formation of 70S Ribosomes Caused by Lack of Ribosomal Protein L34 Can Be Suppressed by Magnesium Akanuma, Genki; Kobayashi, Ako; Suzuki, Shota Journal of Bacteriology, Vol. 196, Issue 22 https://doi.org/10.1128/jb.01896-14	journal	November 2014
Metal ion content of Escherichia coli versus cell age. Kung, F. C.; Raymond, J.; Glaser, D. A. Journal of Bacteriology, Vol. 126, Issue 3 https://doi.org/10.1128/jb.126.3.1089-1095.1976	journal	January 1976
Live-Cell Analysis of a Green Fluorescent Protein-Tagged Herpes Simplex Virus Infection Elliott, Gillian; O’Hare, Peter Journal of Virology, Vol. 73, Issue 5 https://doi.org/10.1128/jvi.73.5.4110-4119.1999	journal	May 1999
Herpes Simplex Virus Type 1 Entry into Host Cells: Reconstitution of Capsid Binding and Uncoating at the Nuclear Pore Complex In Vitro Ojala, Päivi M.; Sodeik, Beate; Ebersold, Melanie W. Molecular and Cellular Biology, Vol. 20, Issue 13 https://doi.org/10.1128/mcb.20.13.4922-4931.2000	journal	July 2000
Sequestered end products and enzyme regulation: the case of ornithine decarboxylase Davis, R. H.; Morris, D. R.; Coffino, P. Microbiological Reviews, Vol. 56, Issue 2 https://doi.org/10.1128/mr.56.2.280-290.1992	journal	June 1992
Hydration Forces Leikin, S.; Parsegian, V. A.; Rau, D. C. Annual Review of Physical Chemistry, Vol. 44, Issue 1 https://doi.org/10.1146/annurev.pc.44.100193.002101	journal	October 1993
Correction: Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages Taddei, François; De Paepe, Marianne PLoS Biology, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pbio.0040273	journal	August 2006
Heat Induced Capsid Disassembly and DNA Release of Bacteriophage λ Qiu, Xiangyun PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0039793	journal	July 2012
Effects of Salt Concentrations and Bending Energy on the Extent of Ejection of Phage Genomes Evilevitch, Alex; Fang, Li Tai; Yoffe, Aron M. Biophysical Journal, Vol. 94, Issue 3 https://doi.org/10.1529/biophysj.107.115345	journal	February 2008
Bending of short DNA helices Vologodskii, Alexander; Du, Quan; Frank-Kamenetskii, Maxim D. Artificial DNA: PNA & XNA, Vol. 4, Issue 1 https://doi.org/10.4161/adna.23892	journal	January 2013
Hydration Forces Todd, Brian A.; Sidorova, Nina Y.; Rau, Donald C. Wiley Encyclopedia of Chemical Biology https://doi.org/10.1002/9780470048672.wecb230	book	May 2008
The effects of magnesium starvation on the ribosome content of Escherichia coli McCarthy, B. J. Biochimica et Biophysica Acta, Vol. 55, Issue 6 https://doi.org/10.1016/0006-3002(62)90901-0	journal	June 1962
The effects of magnesium starvation on the ribosome content of Escherichia coli McCarthy, B. J. Biochimica et Biophysica Acta (BBA) - Specialized Section on Nucleic Acids and Related Subjects, Vol. 55, Issue 6 https://doi.org/10.1016/0926-6550(62)90345-6	journal	June 1962
Forces and Pressures in DNA Packaging and Release from Viral Capsids Tzlil, Shelly; Kindt, James T.; Gelbart, William M. Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/S0006-3495(03)74971-6	journal	March 2003
Direct measurement of temperature-dependent solvation forces between DNA double helices Rau, D. C.; Parsegian, V. A. Biophysical Journal, Vol. 61, Issue 1 https://doi.org/10.1016/S0006-3495(92)81832-5	journal	January 1992
Topological Defects and the Optimum Size of DNA Condensates Park, Stella Y.; Harries, Daniel; Gelbart, William M. Biophysical Journal, Vol. 75, Issue 2 https://doi.org/10.1016/S0006-3495(98)77561-7	journal	August 1998
Cro regulatory protein specified by bacteriophage lambda. Structure, DNA-binding, and repression of RNA synthesis. Takeda, Y.; Folkmanis, A.; Echols, H. Journal of Biological Chemistry, Vol. 252, Issue 17 https://doi.org/10.1016/S0021-9258(17)40047-0	journal	September 1977
Magnesium Transport in Escherichia coli Nelson, David L.; Kennedy, Eugene P. Journal of Biological Chemistry, Vol. 246, Issue 9 https://doi.org/10.1016/S0021-9258(18)62288-4	journal	May 1971
Magnesium and the Growth of Escherichia coli Lusk, J. E.; Williams, R. J. P.; Kennedy, E. P. Journal of Biological Chemistry, Vol. 243, Issue 10 https://doi.org/10.1016/S0021-9258(18)93417-4	journal	May 1968
The Intracellular Concentration of Bound and Unbound Magnesium Ions in Escherichia coli Hurwitz, Charles; Rosano, Carmen L. Journal of Biological Chemistry, Vol. 242, Issue 16 https://doi.org/10.1016/S0021-9258(18)95867-9	journal	August 1967
Condensed phases of DNA: Structures and phase transitions Livolant, Françoise; Leforestier, Amélie Progress in Polymer Science, Vol. 21, Issue 6 https://doi.org/10.1016/S0079-6700(96)00016-0	journal	January 1996
Encapsidated Conformation of Bacteriophage T7 DNA Cerritelli, Mario E.; Cheng, Naiqian; Rosenberg, Alan H. Cell, Vol. 91, Issue 2 https://doi.org/10.1016/S0092-8674(00)80409-2	journal	October 1997
DNA-DNA interactions Strey, Helmut H.; Podgornik, Rudi; Rau, Donald C. Current Opinion in Structural Biology, Vol. 8, Issue 3 https://doi.org/10.1016/S0959-440X(98)80063-8	journal	June 1998
Spontaneous Sharp Bending of Double-Stranded DNA Cloutier, Timothy E.; Widom, Jonathan Molecular Cell, Vol. 14, Issue 3 https://doi.org/10.1016/S1097-2765(04)00210-2	journal	May 2004
Is the In Vitro Ejection of Bacteriophage DNA Quasistatic? A Bulk to Single Virus Study Chiaruttini, N.; de Frutos, M.; Augarde, E. Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.04.048	journal	July 2010
Challenging Packaging Limits and Infectivity of Phage Nurmemmedov, Elmar; Castelnovo, Martin; Medina, Elizabeth Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.11.3500	journal	January 2012
Solid-To-Fluid DNA Transition Inside HSV-1 Capsid Close to the Temperature of Infection Evilevitch, Alex; Sae-Ueng, Udom; Li, Dong Biophysical Journal, Vol. 108, Issue 2 https://doi.org/10.1016/j.bpj.2014.11.1924	journal	January 2015
The Bacteriophage Genome Undergoes a Succession of Intracapsid Phase Transitions upon DNA Ejection Leforestier, Amélie; Livolant, Françoise Journal of Molecular Biology, Vol. 396, Issue 2 https://doi.org/10.1016/j.jmb.2009.11.047	journal	February 2010
DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry Jeembaeva, Meerim; Jönsson, Bengt; Castelnovo, Martin Journal of Molecular Biology, Vol. 395, Issue 5 https://doi.org/10.1016/j.jmb.2009.11.069	journal	February 2010
Challenging Packaging Limits and Infectivity of Phage λ Nurmemmedov, Elmar; Castelnovo, Martin; Medina, Elizabeth Journal of Molecular Biology, Vol. 415, Issue 2 https://doi.org/10.1016/j.jmb.2011.11.015	journal	January 2012
Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22 Tang, Jinghua; Lander, Gabriel C.; Olia, Adam Structure, Vol. 19, Issue 4 https://doi.org/10.1016/j.str.2011.02.010	journal	April 2011
Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22 Tang, Jinghua; Lander, Gabriel C.; Olia, Adam S. Structure, Vol. 19, Issue 5 https://doi.org/10.1016/j.str.2011.05.001	journal	May 2011
The effect of genome length on ejection forces in bacteriophage lambda Grayson, Paul; Evilevitch, Alex; Inamdar, Mandar M. Virology, Vol. 348, Issue 2 https://doi.org/10.1016/j.virol.2006.01.003	journal	May 2006
Secondary structure and interactions of the packaged dsDNA genome of bacteriophage P22 investigated by Raman difference spectroscopy Aubrey, K. L.; Casjens, S. R.; Thomas, G. J. Biochemistry, Vol. 31, Issue 47 https://doi.org/10.1021/bi00162a023	journal	December 1992
DNA arrangement in isometric phage heads Earnshaw, W. C.; Harrison, S. C. Nature, Vol. 268, Issue 5621 https://doi.org/10.1038/268598a0	journal	August 1977
Solid-to-fluid DNA transition inside HSV-1 capsid close to the temperature of infection Sae-Ueng, Udom; Li, Dong; Zuo, Xiaobing Nature Chemical Biology, Vol. 10, Issue 10 https://doi.org/10.1038/nchembio.1628	journal	September 2014
Internal DNA pressure modifies stability of WT phage Ivanovska, I.; Wuite, G.; Jonsson, B. Proceedings of the National Academy of Sciences, Vol. 104, Issue 23 https://doi.org/10.1073/pnas.0703166104	journal	May 2007
Nonequilibrium dynamics and ultraslow relaxation of confined DNA during viral packaging Berndsen, Z. T.; Keller, N.; Grimes, S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 23 https://doi.org/10.1073/pnas.1405109111	journal	May 2014
Dynamics of Double Stranded DNA Reptation From Bacteriophage Gabashvili, Irene S.; Grosberg, Alexander Yu. Journal of Biomolecular Structure and Dynamics, Vol. 9, Issue 5 https://doi.org/10.1080/07391102.1992.10507966	journal	April 1992
Temperature dependence of DNA persistence length Geggier, Stephanie; Kotlyar, Alexander; Vologodskii, Alexander Nucleic Acids Research, Vol. 39, Issue 4 https://doi.org/10.1093/nar/gkq932	journal	October 2010
Statics and dynamics of condensed DNA within phages and globules Odijk, Theo Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, Vol. 362, Issue 1820 https://doi.org/10.1098/rsta.2004.1385	journal	July 2004
Conditions for the Infection of Escherichia coli with Lambda Phage and for the Establishment of Lysogeny Fry, B. A. Journal of General Microbiology, Vol. 21, Issue 3 https://doi.org/10.1099/00221287-21-3-676	journal	December 1959
Exact theory of kinkable elastic polymers Wiggins, Paul A.; Phillips, Rob; Nelson, Philip C. Physical Review E, Vol. 71, Issue 2 https://doi.org/10.1103/PhysRevE.71.021909	journal	February 2005
Salt-Dependent DNA-DNA Spacings in Intact Bacteriophage λ Reflect Relative Importance of DNA Self-Repulsion and Bending Energies Qiu, Xiangyun; Rau, Donald C.; Parsegian, V. Adrian Physical Review Letters, Vol. 106, Issue 2 https://doi.org/10.1103/PhysRevLett.106.028102	journal	January 2011
Localized Single-Stranded Bubble Mechanism for Cyclization of Short Double Helix DNA Yan, Jie; Marko, John F. Physical Review Letters, Vol. 93, Issue 10 https://doi.org/10.1103/PhysRevLett.93.108108	journal	September 2004
Structure and interactions of biological helices Kornyshev, Alexei A.; Lee, Dominic J.; Leikin, Sergey Reviews of Modern Physics, Vol. 79, Issue 3 https://doi.org/10.1103/RevModPhys.79.943	journal	August 2007
Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization Vafabakhsh, R.; Ha, T. Science, Vol. 337, Issue 6098 https://doi.org/10.1126/science.1224139	journal	August 2012
Effect of Salt Shock on Stability of λimm434 Lysogens Shkilnyj, Paul; Koudelka, Gerald B. Journal of Bacteriology, Vol. 189, Issue 8 https://doi.org/10.1128/JB.01857-06	journal	February 2007
Mg2+, K+, and the Ribosome Nierhaus, K. H. Journal of Bacteriology, Vol. 196, Issue 22 https://doi.org/10.1128/JB.02297-14	journal	September 2014
Metal ion content of Escherichia coli versus cell age. Kung, F. C.; Raymond, J.; Glaser, D. A. Journal of Bacteriology, Vol. 126, Issue 3 https://doi.org/10.1128/JB.126.3.1089-1095.1976	journal	January 1976
Electron Microscopy of Magnesium-Depleted Bacteria Morgan, Councilman; Rosenkranz, Herbert S.; Chan, Betty Journal of Bacteriology, Vol. 91, Issue 2 https://doi.org/10.1128/JB.91.2.891-895.1966	journal	January 1966
Live-Cell Analysis of a Green Fluorescent Protein-Tagged Herpes Simplex Virus Infection Elliott, Gillian; O’Hare, Peter Journal of Virology, Vol. 73, Issue 5 https://doi.org/10.1128/JVI.73.5.4110-4119.1999	journal	May 1999
Herpes Simplex Virus Type 1 Entry into Host Cells: Reconstitution of Capsid Binding and Uncoating at the Nuclear Pore Complex In Vitro Ojala, Päivi M.; Sodeik, Beate; Ebersold, Melanie W. Molecular and Cellular Biology, Vol. 20, Issue 13 https://doi.org/10.1128/MCB.20.13.4922-4931.2000	journal	July 2000
Sequestered end products and enzyme regulation: the case of ornithine decarboxylase. Davis, R. H.; Morris, D. R.; Coffino, P. Microbiological Reviews, Vol. 56, Issue 2 https://doi.org/10.1128/MMBR.56.2.280-290.1992	journal	January 1992
DNA bending-induced phase transition of encapsidated genome in phage λ. Lander, Gabriel C.; Johnson, John E.; Rau, Donald C. Carnegie Mellon University https://doi.org/10.1184/r1/6506645	text	January 2013
DNA bending-induced phase transition of encapsidated genome in phage λ. Lander, Gabriel C.; Johnson, John E.; Rau, Donald C. Carnegie Mellon University https://doi.org/10.1184/r1/6506645.v1	text	January 2013
Herpes virus genome, the pressure is on. Bauer, David W.; Huffman, Jamie B.; Homa, Fred L. Carnegie Mellon University https://doi.org/10.1184/r1/6506921	text	January 2013
Herpes virus genome, the pressure is on. Bauer, David W.; Huffman, Jamie B.; Homa, Fred L. Carnegie Mellon University https://doi.org/10.1184/r1/6506921.v1	text	January 2013
Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages De Paepe, Marianne; Taddei, François PLoS Biology, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pbio.0040193	journal	June 2006
Incomplete Ion Dissociation Underlies the Weakened Attraction between DNA Helices at High Spermidine Concentrations Yang, Jie; Rau, Donald C. Biophysical Journal, Vol. 89, Issue 3 https://doi.org/10.1529/biophysj.105.065060	journal	September 2005
Statics and Dynamics of Condensed DNA within Phages and Globules Odijk, Theo arXiv https://doi.org/10.48550/arxiv.cond-mat/0305354	preprint	January 2003
Exact theory of kinkable elastic polymers Wiggins, Paul A.; Phillips, Rob; Nelson, Philip C. arXiv https://doi.org/10.48550/arxiv.cond-mat/0409003	text	January 2004
Encyclopedia of dietary supplements Coates, Paul M. Choice Reviews Online, Vol. 43, Issue 01, p. 43-0034-43-0034 https://doi.org/10.5860/choice.43-0034	journal	September 2005

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