Biological and Structural Characterization of a Host-Adapting Amino Acid in Influenza Virus
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{"title"=>"Biological and structural characterization of a host-adapting amino acid in influenza virus", "type"=>"journal", "authors"=>[{"first_name"=>"Yamada", "last_name"=>"Shinya", "scopus_author_id"=>"35418940500"}, {"first_name"=>"Masato", "last_name"=>"Hatta", "scopus_author_id"=>"7004521317"}, {"first_name"=>"Bart L.", "last_name"=>"Staker", "scopus_author_id"=>"35767145400"}, {"first_name"=>"Shinji", "last_name"=>"Watanabe", "scopus_author_id"=>"35371645500"}, {"first_name"=>"Masaki", "last_name"=>"Imai", "scopus_author_id"=>"56494054500"}, {"first_name"=>"Kyoko", "last_name"=>"Shinya", "scopus_author_id"=>"7004441613"}, {"first_name"=>"Yuko", "last_name"=>"Sakai-Tagawa", "scopus_author_id"=>"8683348700"}, {"first_name"=>"Mutsumi", "last_name"=>"Ito", "scopus_author_id"=>"12791429700"}, {"first_name"=>"Makoto", "last_name"=>"Ozawa", "scopus_author_id"=>"35345736600"}, {"first_name"=>"Tokiko", "last_name"=>"Watanabe", "scopus_author_id"=>"8926021900"}, {"first_name"=>"Saori", "last_name"=>"Sakabe", "scopus_author_id"=>"21834989800"}, {"first_name"=>"Chengjun", "last_name"=>"Li", "scopus_author_id"=>"35078736700"}, {"first_name"=>"Jin Hyun", "last_name"=>"Kim", "scopus_author_id"=>"57191681415"}, {"first_name"=>"Peter J.", "last_name"=>"Myler", "scopus_author_id"=>"7005974497"}, {"first_name"=>"Isabelle", "last_name"=>"Phan", "scopus_author_id"=>"6602863589"}, {"first_name"=>"Amy", "last_name"=>"Raymond", "scopus_author_id"=>"26538105800"}, {"first_name"=>"Eric", "last_name"=>"Smith", "scopus_author_id"=>"55479658600"}, {"first_name"=>"Robin", "last_name"=>"Stacy", "scopus_author_id"=>"9742599900"}, {"first_name"=>"Chairul A.", "last_name"=>"Nidom", "scopus_author_id"=>"6507930981"}, {"first_name"=>"Simon M.", "last_name"=>"Lank", "scopus_author_id"=>"26040850700"}, {"first_name"=>"Roger W.", "last_name"=>"Wiseman", "scopus_author_id"=>"20035327000"}, {"first_name"=>"Benjamin N.", "last_name"=>"Bimber", "scopus_author_id"=>"14053443700"}, {"first_name"=>"David H.", "last_name"=>"O'Connor", "scopus_author_id"=>"7401496996"}, {"first_name"=>"Gabriele", "last_name"=>"Neumann", "scopus_author_id"=>"7202631658"}, {"first_name"=>"Lance J.", "last_name"=>"Stewart", "scopus_author_id"=>"35460249000"}, {"first_name"=>"Yoshihiro", "last_name"=>"Kawaoka", "scopus_author_id"=>"26643027000"}], "year"=>2010, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-77958149212", "sgr"=>"77958149212", "pui"=>"359800982", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pmid"=>"20700447", "doi"=>"10.1371/journal.ppat.1001034"}, "id"=>"cdd087b7-2f2f-30ca-95ef-ca8c40041098", "abstract"=>"Two amino acids (lysine at position 627 or asparagine at position 701) in the polymerase subunit PB2 protein are considered critical for the adaptation of avian influenza A viruses to mammals. However, the recently emerged pandemic H1N1 viruses lack these amino acids. Here, we report that a basic amino acid at position 591 of PB2 can compensate for the lack of lysine at position 627 and confers efficient viral replication to pandemic H1N1 viruses in mammals. Moreover, a basic amino acid at position 591 of PB2 substantially increased the lethality of an avian H5N1 virus in mice. We also present the X-ray crystallographic structure of the C-terminus of a pandemic H1N1 virus PB2 protein. Arginine at position 591 fills the cleft found in H5N1 PB2 proteins in this area, resulting in differences in surface shape and charge for H1N1 PB2 proteins. These differences may affect the protein's interaction with viral and/or cellular factors, and hence its ability to support virus replication in mammals.", "link"=>"http://www.mendeley.com/research/biological-structural-characterization-hostadapting-amino-acid-influenza-virus", "reader_count"=>110, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>29, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>4, "Student > Master"=>5, "Other"=>4, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>29, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>4, "Student > Master"=>5, "Other"=>4, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Agricultural and Biological Sciences"=>65, "Business, Management and Accounting"=>2, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>3, "Computer Science"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>11, "Mathematics"=>1, "Medicine and Dentistry"=>9, "Physics and Astronomy"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>7}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>1}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>65}, "Computer Science"=>{"Computer Science"=>3}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "South Korea"=>1, "United States"=>4, "Japan"=>1, "China"=>1, "Denmark"=>1, "United Kingdom"=>1, "France"=>1}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/417034", "https://ndownloader.figshare.com/files/417061", "https://ndownloader.figshare.com/files/417075", "https://ndownloader.figshare.com/files/417091", "https://ndownloader.figshare.com/files/417109", "https://ndownloader.figshare.com/files/417138"], "description"=>"<div><p>Two amino acids (lysine at position 627 or asparagine at position 701) in the polymerase subunit PB2 protein are considered critical for the adaptation of avian influenza A viruses to mammals. However, the recently emerged pandemic H1N1 viruses lack these amino acids. Here, we report that a basic amino acid at position 591 of PB2 can compensate for the lack of lysine at position 627 and confers efficient viral replication to pandemic H1N1 viruses in mammals. Moreover, a basic amino acid at position 591 of PB2 substantially increased the lethality of an avian H5N1 virus in mice. We also present the X-ray crystallographic structure of the C-terminus of a pandemic H1N1 virus PB2 protein. Arginine at position 591 fills the cleft found in H5N1 PB2 proteins in this area, resulting in differences in surface shape and charge for H1N1 PB2 proteins. These differences may affect the protein's interaction with viral and/or cellular factors, and hence its ability to support virus replication in mammals.</p></div>", "links"=>[], "tags"=>["characterization", "host-adapting", "amino", "influenza"], "article_id"=>142329, "categories"=>["Cell Biology", "Medicine", "Cancer"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.s001", "https://dx.doi.org/10.1371/journal.ppat.1001034.s002", "https://dx.doi.org/10.1371/journal.ppat.1001034.s003", "https://dx.doi.org/10.1371/journal.ppat.1001034.s004", "https://dx.doi.org/10.1371/journal.ppat.1001034.s005", "https://dx.doi.org/10.1371/journal.ppat.1001034.s006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Biological_and_Structural_Characterization_of_a_Host_Adapting_Amino_Acid_in_Influenza_Virus/142329", "title"=>"Biological and Structural Characterization of a Host-Adapting Amino Acid in Influenza Virus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-08-05 00:38:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/837506"], "description"=>"<p><b>A</b>. We inoculated the human UT3006 virus, the avian CkUT3091 virus, or CkUT3091-based reassortant viruses possessing single genes of UT3006 (CkUT3091-UT3006PB2, -UT3006PB1, -UT3006PA, -UT3006HA, -UT3006NP, -UT3006NA, -UT3006M, and -UT3006NS) into normal human bronchioepithelial (NHBE) cells at a multiplicity of infection of 0.0005 and cultured infected cells at 37°C. The culture supernatants were harvested at the indicated times and subjected to plaque assays in NHBE cells to determine virus titers. <b>B</b>. Growth curves in NHBE cells of UT3006, CkUT3091, and CkUT3091 variants possessing UT3006-derived PB2 substitutions at position 117 (PB2-T117I), 591 (PB2-Q591K), or at all five positions indicated in the text (PB2-5aa). The CkUT3091 virus possessing the UT3006-PB2 gene (CkUT3091-UT3006PB2, see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001034#ppat-1001034-g001\" target=\"_blank\">Fig. 1A</a>) is shown again for comparison. Experiments to determine viral growth kinetics were carried out twice, with three explicates each. Shown are data from one experiment.</p>", "links"=>[], "tags"=>["pb2-591", "h5n1", "replication", "mammalian"], "article_id"=>507843, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amino_acid_PB2_591_is_important_for_H5N1_virus_replication_in_mammalian_cells_/507843", "title"=>"Amino acid PB2-591 is important for H5N1 virus replication in mammalian cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-05 02:10:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/837642"], "description"=>"<p>Mice (4 per group) were inoculated with the indicated amounts of CkUT3091 virus (blue squares) or CkUT3091 virus possessing the PB2-Q591K substitution (red circles) and observed daily for changes in body weight. Animals that lost more than 25% of their pre-infection weight were euthanized. The numbers in the graphs indicate the numbers of surviving mice per group. <b>A</b>.–<b>F</b>. Infection of mice with 10<sup>6</sup> pfu (<b>A</b>), 10<sup>5</sup> pfu (<b>B</b>), 10<sup>4</sup> pfu (<b>C</b>), 10<sup>3</sup> pfu (<b>D</b>), 10<sup>2</sup> pfu (<b>E</b>), or 10<sup>1</sup> pfu (<b>F</b>) of virus.</p>", "links"=>[], "tags"=>["pb2-591k", "increases", "virulence", "avian", "h5n1"], "article_id"=>507970, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amino_acid_PB2_591K_increases_the_virulence_of_an_avian_H5N1_virus_in_mice_/507970", "title"=>"Amino acid PB2-591K increases the virulence of an avian H5N1 virus in mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-05 02:12:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/837759"], "description"=>"<p><b>A</b>. Overview of PB2 amino acids at positions 591, 627, and 701. Shown are A/California/04/09 (H1N1; Cal04) and its mutants tested in competitive transmission studies. <b>B</b>.–<b>D</b>. The indicated pairs of viruses were mixed at a 1∶1 ratio and three ferrets (one per cage) were infected intranasally with 10<sup>6</sup> plaque-forming units of virus mix. One day later, one ferret each was placed in a cage adjacent to an infected ferret (‘contact’ ferret); that is, for each set of viruses, three pairs of infected/contact ferrets were tested. Virus populations in the nasal washes of infected and contact ferrets were assessed at the indicated time points. Grey bars; percent wild-type PB2 molecules. Colored bars; percent mutant PB2 molecules. NA, not applicable; ND, not determined (nasal wash samples with virus titers of less than 10<sup>2</sup> plaque-forming units per ml were not processed for sequence analysis). Competition studies were carried out for Cal04 (PB2-591R/<u>627E</u>/701D) and Cal04PB2-627K (PB2-591R/<u>627K</u>/701D) (<b>B</b>), Cal04 (PB2-591R/627E/<u>701D</u>) and Cal04PB2-701N (PB2-591R/627E/<u>701N</u>) (<b>C</b>), and for Cal04 (PB2-<u>591R</u>/627E/701D) and Cal04-PB2-591Q (PB2-<u>591Q</u>/627E/701D) (<b>D</b>).</p>", "links"=>[], "tags"=>["studies", "ferrets", "wild-type", "mutant", "pandemic", "h1n1"], "article_id"=>508089, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Competitive_transmission_studies_in_ferrets_for_wild_type_and_mutant_pandemic_H1N1_viruses_/508089", "title"=>"Competitive transmission studies in ferrets for wild-type and mutant pandemic H1N1 viruses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-05 02:14:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/837897"], "description"=>"<p>Shown are the X-ray crystal structures of a pandemic H1N1 (PB2-591R/627E) and an H5N1 PB2 protein encoding PB2-627K (PB2-591Q/627K). <b>A</b>. The surface of H1N1-PB2 in the region of PB2-591R and PB2-627E (PDBID:3KHW). Color of surface is mapped by qualitative vacuum electrostatics generated by PYMOL (27). Blue = relative positive charge, Red = relative negative charge. Residue S590, R591, and E627 are shown as stick representations underneath the surface contour and are identified with black arrows. The side chain of R591 intrudes into the cleft shown in Fig. 4B. <b>B</b>. The surface of H5N1-PB2 in the region of PB2-591Q and PB2-627K (PDBID:3KC6) shows a distinct cleft in comparison to the surface of H1N1 PB2-591R and PB2-627E (PDBID:3KHW). <b>C</b>. Close-up view of the interactions of H1N1 PB2-591R with neighbouring residues. H1N1-PB2 residues A587, S590, R591, and E627 are shown in sticks model, green = carbon, red = oxygen, blue = nitrogen. The conformation of H1N1 PB2-591R (PDBID:3KHW) is shown oriented away from PB2-627E making hydrogen bonding and water-mediated hydrogen bonding interactions to the carbonyl oxygen of residue PB2-587A. PB2-591R fills the cleft shown in Figure 4B. Residue S590 sits underneath E627 and blocks the conformational freedom of E627.</p>", "links"=>[], "tags"=>["structures", "pandemic", "h1n1", "avian", "h5n1", "pb2"], "article_id"=>508220, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_X_ray_crystal_structures_of_pandemic_H1N1_and_avian_H5N1_PB2_proteins_/508220", "title"=>"X-ray crystal structures of pandemic H1N1 and avian H5N1 PB2 proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-05 02:17:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/838039"], "description"=>"a<p>We intratracheally inoculated A/duck/Vietnam/5001/04 (H5N1) into a 3-week-old ostrich and isolated virus from trachea, lungs, and brain on day 3 post-infection (for more details, see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001034#ppat.1001034-Shinya1\" target=\"_blank\">[10]</a>). Viral RNA was isolated, and the PB2 gene was amplified by RT-PCR and cloned. We then sequenced the indicated numbers of PB2 clones. Results for PB2-627 and PB2-701 were already shown in Shinya <i>et al.</i><a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1001034#ppat.1001034-Shinya1\" target=\"_blank\">[10]</a>. We here expanded our analysis to include PB2-591 in this study.</p>b<p>Mammalian-type amino acids are shown in bold and italics.</p>", "links"=>[], "tags"=>["amino", "acids", "pb2", "ostrich"], "article_id"=>508372, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mammalian_type_amino_acids_in_the_PB2_protein_of_ostrich_isolates_/508372", "title"=>"Mammalian-type amino acids in the PB2 protein of ostrich isolates.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-05 02:19:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/838111"], "description"=>"(1)<p>Numbers in parenthesis represent highest resolution shell of data.</p>(2)<p><i>R</i><sub>merge</sub> = (|Σ<i>I</i><sub>hkl</sub>−<<i>I</i>>|/(Σ<i>I</i><sub>hkl</sub>), where the average intensity <<i>I</i>> is taken over all symmetry equivalent measurements and <i>I</i><sub>hkl</sub> is the measured intensity for any given reflection.</p>(3)<p><i>I/σI</i> is the mean reflection intensity divided by the estimated error.</p>(4)<p><i>R</i><sub>cryst</sub> = ∥<i>F</i><sub>o</sub>|−|<i>F</i><sub>c</sub>∥/|<i>F</i><sub>o</sub>|, where <i>F</i><sub>o</sub> and <i>F</i><sub>c</sub> are the observed and calculated structure factor amplitudes, respectively.</p>(5)<p><i>R</i><sub>free</sub> is equivalent to <i>R</i><sub>cryst</sub> but calculated for 5% of the reflections chosen at random and omitted from the refinement process.</p>", "links"=>[], "tags"=>["crystallographic", "refinement"], "article_id"=>508445, "categories"=>["Virology", "Medicine", "Infectious Diseases", "Plant Biology"], "users"=>["Shinya Yamada", "Masato Hatta", "Bart L. Staker", "Shinji Watanabe", "Masaki Imai", "Kyoko Shinya", "Yuko Sakai-Tagawa", "Mutsumi Ito", "Makoto Ozawa", "Tokiko Watanabe", "Saori Sakabe", "Chengjun Li", "Jin Hyun Kim", "Peter J. Myler", "Isabelle Phan", "Amy Raymond", "Eric Smith", "Robin Stacy", "Chairul A. Nidom", "Simon M. Lank", "Roger W. Wiseman", "Benjamin N. Bimber", "David H. O'Connor", "Gabriele Neumann", "Lance J. Stewart", "Yoshihiro Kawaoka"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1001034.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_X_ray_crystallographic_data_collection_and_refinement_statistics_/508445", "title"=>"X-ray crystallographic data collection and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-05 02:20:45"}

PMC Usage Stats | Further Information

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Relative Metric

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