A Promiscuous DNA Packaging Machine from Bacteriophage T4
Publication Date
February 15, 2011
Journal
PLOS Biology
Authors
Zhihong Zhang, Vishal I. Kottadiel, Reza Vafabakhsh, Li Dai, et al
Volume
9
Issue
2
Pages
e1000592
DOI
http://doi.org/10.1371/journal.pbio.1000592
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.1000592
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21358801
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3039672
Europe PMC
http://europepmc.org/abstract/MED/21358801
Web of Science
000287653800007
Scopus
79952264222
Mendeley
http://www.mendeley.com/research/promiscuous-dna-packaging-machine-bacteriophage-t4
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Mendeley | Further Information

{"title"=>"A promiscuous DNA packaging machine from bacteriophage T4", "type"=>"journal", "authors"=>[{"first_name"=>"Zhihong", "last_name"=>"Zhang", "scopus_author_id"=>"55644003973"}, {"first_name"=>"Vishal I.", "last_name"=>"Kottadiel", "scopus_author_id"=>"23028087100"}, {"first_name"=>"Reza", "last_name"=>"Vafabakhsh", "scopus_author_id"=>"41662471400"}, {"first_name"=>"Li", "last_name"=>"Dai", "scopus_author_id"=>"41661240700"}, {"first_name"=>"Yann R.", "last_name"=>"Chemla", "scopus_author_id"=>"6603236123"}, {"first_name"=>"Taekjip", "last_name"=>"Ha", "scopus_author_id"=>"7203014287"}, {"first_name"=>"Venigalla B.", "last_name"=>"Rao", "scopus_author_id"=>"7402899348"}], "year"=>2011, "source"=>"PLoS Biology", "identifiers"=>{"pui"=>"361373952", "scopus"=>"2-s2.0-79952264222", "doi"=>"10.1371/journal.pbio.1000592", "isbn"=>"1545-7885 (Electronic)\\n1544-9173 (Linking)", "sgr"=>"79952264222", "issn"=>"15449173", "pmid"=>"21358801"}, "id"=>"736d15b8-2911-3c09-8423-163229e30253", "abstract"=>"Complex viruses are assembled from simple protein subunits by sequential and irreversible assembly. During genome packaging in bacteriophages, a powerful molecular motor assembles at the special portal vertex of an empty prohead to initiate packaging. The capsid expands after about 10%-25% of the genome is packaged. When the head is full, the motor cuts the concatemeric DNA and dissociates from the head. Conformational changes, particularly in the portal, are thought to drive these sequential transitions. We found that the phage T4 packaging machine is highly promiscuous, translocating DNA into finished phage heads as well as into proheads. Optical tweezers experiments show that single motors can force exogenous DNA into phage heads at the same rate as into proheads. Single molecule fluorescence measurements demonstrate that phage heads undergo repeated initiations, packaging multiple DNA molecules into the same head. These results suggest that the phage DNA packaging machine has unusual conformational plasticity, powering DNA into an apparently passive capsid receptacle, including the highly stable virus shell, until it is full. These features probably led to the evolution of viral genomes that fit capsid volume, a strikingly common phenomenon in double-stranded DNA viruses, and will potentially allow design of a novel class of nanocapsid delivery vehicles.", "link"=>"http://www.mendeley.com/research/promiscuous-dna-packaging-machine-bacteriophage-t4", "reader_count"=>55, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>4, "Student > Bachelor"=>2, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>14, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>4, "Student > Bachelor"=>2, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Agricultural and Biological Sciences"=>35, "Philosophy"=>1, "Chemistry"=>5, "Computer Science"=>1, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Materials Science"=>1, "Medicine and Dentistry"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>3, "Social Sciences"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>5}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>35}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Republic of Singapore"=>1, "Iran"=>1, "United States"=>4, "Japan"=>1, "China"=>1, "Israel"=>1, "Nigeria"=>1, "Paraguay"=>1}, "group_count"=>1}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/798248"], "description"=>"<p>(A) Partial heads (lanes 3–6), full heads (lanes 7–10), or proheads (lane 12) were treated with DNAse I (37°C, 30 min) and/or proteinase K (65°C, 30 min), as shown by “+” or “−” rows under the figure, and subjected to agarose gel (0.8% w/v) electrophoresis and stained with cyber green. The molecular size markers λ HindIII (lane 1), λ DNA (lane 2), and T4 DNA (lane 11) were used to determine the size of the DNA present in the heads. Partial head lanes 3–6: lane 3, without any treatment; lane 4, treated with DNAse I; lane 5, treated with proteinase K; lane 6, treated first with DNAse I and then with proteinase K. Arrow shows the position of the heads stained with cyber green because they were associated with a ∼8-kb DNA (lane 3). The 8-kb DNA was inside the heads because it was resistant to DNAse I treatment (lane 4) but released by treatment with proteinase K (lanes 5 and 6). Full head lanes 7–10: lane 7, without any treatment; lane 8, treated with DNAse I; lane 9, treated with proteinase K; lane 10, treated first with DNAse I and then with proteinase K. Note that the untreated full heads showed, in addition to the head band (arrow), an intensely stained band in the well plus a smear (lane 7), both of which were removed by digestion with DNAse I (lane 8). This was because some of the full heads extruded the packaged DNA during storage, which remained complexed with the head and retained in the well. This was confirmed by treatment with proteinase K, which released this DNA as well as that packaged inside, producing a single band (lane 9). Treatment first with DNAse I resulted in the digestion of the outside DNA, and subsequent addition of proteinase K digested the capsids and released the DNA packaged inside (lane 10). The DNA in lanes 9 and 10 is slightly shorter than that isolated from phage (lane 11), presumably because a segment of packaged DNA near the portal was accessible to DNAse I digestion <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592-Rao2\" target=\"_blank\">[11]</a>,<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592-Bode1\" target=\"_blank\">[13]</a>,<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592-Lhuillier1\" target=\"_blank\">[14]</a>. Arrow shows the position of the heads stained with cyber green because they were associated with DNA inside the head (lane 7). The control <i>17am18amrII</i> proheads are empty and showed no staining with cyber green (lane 12). (B and C) Packaging of short DNA fragments (B) (50–766 bp), or λ DNA (C) (48.5 kb) under various reaction conditions, as shown under the figure. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#s4\" target=\"_blank\">Materials and Methods</a> for additional details.</p>", "links"=>[], "tags"=>["t4", "packaging", "repackages", "dna", "phage"], "article_id"=>468610, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g003", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_T4_packaging_machine_repackages_DNA_into_phage_heads_/468610", "title"=>"The T4 packaging machine repackages DNA into phage heads.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:23:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/798532"], "description"=>"<p>Quantification of packaging by single molecule fluorescence assay. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#s4\" target=\"_blank\">Materials and Methods</a> for details. (A and C) Fluorescence images of immobilized T4 heads packaged with Cy3 (83-bp) and Cy5 (39-bp) DNAs, respectively. One-fourth of the 70 µm ×35 µm imaging area is shown in each case (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592.s001\" target=\"_blank\">Figures S1</a> and <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592.s002\" target=\"_blank\">S2</a> for full-size fluorescent images). (B and D) Histograms showing the number of heads packaged with Cy3 or Cy5 DNAs. The number of heads showing fluorescence in more than 30 images was averaged in each case.</p>", "links"=>[], "tags"=>["fluorescence", "refilled"], "article_id"=>468901, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g006", "stats"=>{"downloads"=>3, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Single_molecule_fluorescence_measurements_of_refilled_heads_/468901", "title"=>"Single molecule fluorescence measurements of refilled heads.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:28:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/798135"], "description"=>"<p>(A) The <i>10am13am</i> heads were isolated by differential centrifugation followed by CsCl gradient centrifugation (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#s4\" target=\"_blank\">Materials and Methods</a> for details). The two closely spaced bands at the top of the gradient contained partial heads that had ejected most of their packaged DNA, save an ∼8-kb piece. The band at the bottom of the gradient contained full heads in which the packaged T4 genome was stabilized (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio-1000592-g003\" target=\"_blank\">Figure 3</a> legend for additional details). (B) Purification of partial heads by DEAE-Sepharose column chromatography. The two closely spaced head bands at the top of the CsCl gradient were pooled, dialyzed against 10 mM Tris-HCl (pH 7.5), 50 mM NaCl, and 5 mM MgCl<sub>2</sub>, and purified by ion-exchange chromatography (AKTA Prime, GE Healthcare). The column was pre-equilibrated with 50 mM Tris-HCl (pH 7.5) and 5 mM MgCl<sub>2</sub>, and a linear gradient of 0–300 mM NaCl was applied to elute the bound heads. The peak fractions were pooled, concentrated by filtration, and stored at 4°C. (C) The partial and full heads are fully expanded. The purified proheads, partial heads, and full heads were mixed with SDS gel loading buffer and kept at room temperature (“−”) or boiling temperature (“+”) for 5 min. The samples were then separated by 10% SDS-PAGE, stained with Coomassie blue R, and destained. Note that the major capsid protein, gp23* (position marked with arrow), was not seen in the room temperature samples because the expanded heads could not be dissociated into gp23* subunits. (D) Partial and full heads reassemble with the exogenous gp17. About 5×10<sup>11</sup> proheads, partial heads, or full heads were incubated with purified gp17-K577 (0.3 µM; 50:1 ratio of gp17 molecules to gp20 subunits) in a buffer containing 50 mM Tris-HCl (pH 7.5), 100 mM NaCl, and 5 mM MgCl<sub>2</sub>, at room temperature for 30 min. The head-gp17 complexes were sedimented by centrifugation at 18,000 rpm for 45 min, and the pellet was washed several times to remove any unbound gp17. The proteins were transferred to PVDF membrane, and Western blotting was performed using polyclonal gp17 antibodies. The results were confirmed by doing the same experiment with full-length gp17 and a GFP-gp17 fusion protein. Only the gp17-K577 (C-terminal 33 amino acids of gp17 were deleted) data are shown because gp17-K577 is protease resistant and migrates as a single band as opposed to three bands with the full-length gp17 and GFP-gp17, and also because there is no background overlapping band at the same position. The gp17 band in the full head lane (lane 4) is faint because some of these heads released the packaged DNA during the procedure, which resulted in poor recovery of the heads during the centrifugation and washing steps.</p>", "links"=>[], "tags"=>["characterization", "phage"], "article_id"=>468501, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Purification_and_characterization_of_phage_heads_/468501", "title"=>"Purification and characterization of phage heads.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:21:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/798017"], "description"=>"<p>The major capsid protein assembles around a scaffolding core into a prehead. The core is removed by proteolysis to produce an empty unexpanded prohead (A). The unexpanded prohead normally has a round shape, but in phage T4 it has angular geometry <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592-Steven1\" target=\"_blank\">[45]</a>. The packaging motor–DNA complex docks on portal and initiates packaging. The prohead expands after about 10%–25% of the DNA is packaged (B). After headful packaging, the motor cuts the concatemeric DNA and dissociates from the DNA-full head (C). The neck proteins (gp13, gp14, and gp15) assemble on portal to seal off the DNA-full head and provide a platform for tail assembly (D). The various colors of portal represent different conformational states. In promiscuous assembly, the packaging motor assembles on a partial head produced by ejection of packaged DNA (E) or a full head (G), and refills the head with new fragments of DNA ([F] and [G]; new DNA fragments shown in red).</p>", "links"=>[], "tags"=>["schematic", "dna", "packaging", "sequential", "promiscuous"], "article_id"=>468380, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_schematic_of_DNA_packaging_by_sequential_assembly_and_promiscuous_assembly_/468380", "title"=>"A schematic of DNA packaging by sequential assembly and promiscuous assembly.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:19:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/798450"], "description"=>"<p>(A) The dual optical trap set-up for single molecule DNA packaging. The T4 head–motor complex and the 10-kb DNA substrate were tethered between two beads, each held in an optical trap and held under 5 pN tension. See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#s4\" target=\"_blank\">Materials and Methods</a> for details. (B–D) Packaging traces showing the packaging of DNA by proheads (B), partial heads (C), and full heads (DI–DIII). “n” represents the number of packaging traces qualitatively showing similar packaging behavior in that panel.</p>", "links"=>[], "tags"=>["mature-phage-head-assembled", "packaging", "machines", "refill"], "article_id"=>468812, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Single_mature_phage_head_assembled_packaging_machines_refill_the_capsid_/468812", "title"=>"Single mature-phage-head-assembled packaging machines refill the capsid.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:26:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/399237", "https://ndownloader.figshare.com/files/399275", "https://ndownloader.figshare.com/files/399306", "https://ndownloader.figshare.com/files/399338"], "description"=>"<div><p>Complex viruses are assembled from simple protein subunits by sequential and irreversible assembly. During genome packaging in bacteriophages, a powerful molecular motor assembles at the special portal vertex of an empty prohead to initiate packaging. The capsid expands after about 10%–25% of the genome is packaged. When the head is full, the motor cuts the concatemeric DNA and dissociates from the head. Conformational changes, particularly in the portal, are thought to drive these sequential transitions. We found that the phage T4 packaging machine is highly promiscuous, translocating DNA into finished phage heads as well as into proheads. Optical tweezers experiments show that single motors can force exogenous DNA into phage heads at the same rate as into proheads. Single molecule fluorescence measurements demonstrate that phage heads undergo repeated initiations, packaging multiple DNA molecules into the same head. These results suggest that the phage DNA packaging machine has unusual conformational plasticity, powering DNA into an apparently passive capsid receptacle, including the highly stable virus shell, until it is full. These features probably led to the evolution of viral genomes that fit capsid volume, a strikingly common phenomenon in double-stranded DNA viruses, and will potentially allow design of a novel class of nanocapsid delivery vehicles.</p></div>", "links"=>[], "tags"=>["promiscuous", "dna", "packaging", "bacteriophage", "t4"], "article_id"=>138866, "categories"=>["Cancer"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000592.s001", "https://dx.doi.org/10.1371/journal.pbio.1000592.s002", "https://dx.doi.org/10.1371/journal.pbio.1000592.s003", "https://dx.doi.org/10.1371/journal.pbio.1000592.s004"], "stats"=>{"downloads"=>4, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Promiscuous_DNA_Packaging_Machine_from_Bacteriophage_T4/138866", "title"=>"A Promiscuous DNA Packaging Machine from Bacteriophage T4", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-02-15 02:27:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/798350"], "description"=>"<p>(A) The phage heads were isolated from <i>10am13am</i> infected <i>E. coli</i> P301 cells (500 ml culture) by lysis in the presence of DNAse I followed by differential centrifugation (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#s4\" target=\"_blank\">Materials and Methods</a> for details). The phage head pellet containing a mixture of partial heads and full heads was resuspended in 200 µl of 50 mM Tris-HCl (pH 7.5) and 5 mM MgCl<sub>2</sub>. The sample was split into two halves, and larger scale packaging assays were conducted immediately. The 500-µl packaging reactions contained 100 µl of phage heads, 4.75 µM GFP-gp17, 43 µg of ladder DNA (50–766 bp; NEB), 5% PEG buffer, and 1 mM ATP <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000592#pbio.1000592-Kondabagil1\" target=\"_blank\">[30]</a>. gp17 and ATP were omitted in the control reaction. After 30 min of incubation at room temperature, 40 µl (1,000 units) of Benzonase nuclease (EMD Biosciences) was added to digest unpackaged DNA, and the samples were separated by CsCl density gradient centrifugation. (B) The partial and full head samples from the gradient were electrophoresed on 10% SDS polyacrylamide gel to analyze for proteins and to estimate the concentration of particles used in the packaging reactions. Since the concentration of full heads is very low compared to that of partial heads (roughly 1/10<sup>th</sup> that of partial heads), the full heads were concentrated by high-speed centrifugation such that the number of particles per lane are approximately the same for both full heads and partial heads. (C and D) The full (C) and partial (D) head bands from the gradient were treated with proteinase K (18.5 µg; Fermentas) and electrophoresed on 4%–20% polyacrylamide gel in Tris-borate buffer (pH 8) to analyze for packaged DNA.</p>", "links"=>[], "tags"=>["heads"], "article_id"=>468719, "categories"=>["Virology"], "users"=>["Zhihong Zhang", "Vishal I. Kottadiel", "Reza Vafabakhsh", "Li Dai", "Yann R. Chemla", "Taekjip Ha", "Venigalla B. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000592.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Full_heads_can_package_DNA_/468719", "title"=>"Full heads can package DNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-02-15 02:25:19"}

PMC Usage Stats | Further Information

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