Signature Patterns of MHC Diversity in Three Gombe Communities of Wild Chimpanzees Reflect Fitness in Reproduction and Immune Defense against SIVcpz
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{"title"=>"Signature Patterns of MHC Diversity in Three Gombe Communities of Wild Chimpanzees Reflect Fitness in Reproduction and Immune Defense against SIVcpz", "type"=>"journal", "authors"=>[{"first_name"=>"Emily E.", "last_name"=>"Wroblewski", "scopus_author_id"=>"8716477100"}, {"first_name"=>"Paul J.", "last_name"=>"Norman", "scopus_author_id"=>"7201826831"}, {"first_name"=>"Lisbeth A.", "last_name"=>"Guethlein", "scopus_author_id"=>"6602111757"}, {"first_name"=>"Rebecca S.", "last_name"=>"Rudicell", "scopus_author_id"=>"26027193300"}, {"first_name"=>"Miguel A.", "last_name"=>"Ramirez", "scopus_author_id"=>"13404586200"}, {"first_name"=>"Yingying", "last_name"=>"Li", "scopus_author_id"=>"35262131400"}, {"first_name"=>"Beatrice H.", "last_name"=>"Hahn", "scopus_author_id"=>"7201799232"}, {"first_name"=>"Anne E.", "last_name"=>"Pusey", "scopus_author_id"=>"6701915235"}, {"first_name"=>"Peter", "last_name"=>"Parham", "scopus_author_id"=>"35392381800"}], "year"=>2015, "source"=>"PLoS Biology", "identifiers"=>{"pui"=>"604601917", "doi"=>"10.1371/journal.pbio.1002144", "isbn"=>"1544-9173", "pmid"=>"26020813", "issn"=>"15457885", "scopus"=>"2-s2.0-84930644633", "sgr"=>"84930644633"}, "id"=>"ae7d4474-072f-3125-8ec6-c755c87b60fa", "abstract"=>"Major histocompatibility complex (MHC) class I molecules determine immune responses to viral infections. These polymorphic cell-surface glycoproteins bind peptide antigens, forming ligands for cytotoxic T and natural killer cell receptors. Under pressure from rapidly evolving viruses, hominoid MHC class I molecules also evolve rapidly, becoming diverse and species-specific. Little is known of the impact of infectious disease epidemics on MHC class I variant distributions in human populations, a context in which the chimpanzee is the superior animal model. Population dynamics of the chimpanzees inhabiting Gombe National Park, Tanzania have been studied for over 50 years. This population is infected with SIVcpz, the precursor of human HIV-1. Because HLA-B is the most polymorphic human MHC class I molecule and correlates strongly with HIV-1 progression, we determined sequences for its ortholog, Patr-B, in 125 Gombe chimpanzees. Eleven Patr-B variants were defined, as were their frequencies in Gombe's three communities, changes in frequency with time, and effect of SIVcpz infection. The growing populations of the northern and central communities, where SIVcpz is less prevalent, have stable distributions comprising a majority of low-frequency Patr-B variants and a few high-frequency variants. Driving the latter to high frequency has been the fecundity of immigrants to the northern community, whereas in the central community, it has been the fecundity of socially dominant individuals. In the declining population of the southern community, where greater SIVcpz prevalence is associated with mortality and emigration, Patr-B variant distributions have been changing. Enriched in this community are Patr-B variants that engage with natural killer cell receptors. Elevated among SIVcpz-infected chimpanzees, the Patr-B*06:03 variant has striking structural and functional similarities to HLA-B*57, the human allotype most strongly associated with delayed HIV-1 progression. Like HLA-B*57, Patr-B*06:03 correlates with reduced viral load, as assessed by detection of SIVcpz RNA in feces.", "link"=>"http://www.mendeley.com/research/signature-patterns-mhc-diversity-three-gombe-communities-wild-chimpanzees-reflect-fitness-reproducti", "reader_count"=>56, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>7, "Medicine and Dentistry"=>4, "Agricultural and Biological Sciences"=>30, "Neuroscience"=>1, "Social Sciences"=>2, "Computer Science"=>1, "Immunology and Microbiology"=>2, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>30}, "Computer Science"=>{"Computer Science"=>1}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>2}}, "reader_count_by_country"=>{"Japan"=>1, "United Kingdom"=>2, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2085810"], "description"=>"<p>(A) Contribution of the offspring of fecund individuals to the 2010 <i>Patr-B</i> allele frequencies of the northern and central communities. Partial gray shading of the frequency bars gives the allelic contribution of the offspring produced by fecund individuals. Fecund males (Male) were current or former alpha males. Fecund females (Female) in the central community produced at least twice the mean number of offspring. In the northern community, fecund females were defined as having more offspring than the mean. “Male and Female” combines the offspring produced by the fecund females for each community with either that of the top two producing fecund males for the central community, or that of the three alpha males for the northern community. <i>Patr-B</i> N is the number of alleles present within the community, while <i>P.t.s.</i> N is the number of offspring of fecund individuals in the population on the first day of the year. Frequencies are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s004\" target=\"_blank\">S4 Data</a> and <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s007\" target=\"_blank\">S7 Data</a>. (B) Shows how the matrilineal F lineage contributed substantially to the high frequency of <i>Patr-B*23:05</i> in the central community. Partial gray shading of the frequency bars gives the contribution of F lineage individuals. <i>Patr-B</i> N is the number of alleles present within the community. <i>P.t.s.</i> N is the number of F lineage individuals in the population on the first day of the year. Frequency data are included in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s004\" target=\"_blank\">S4 Data</a>.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428826, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g011", "stats"=>{"downloads"=>2, "page_views"=>40, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fecundity_of_socially_dominant_chimpanzees_is_most_influential_in_Gombe_8217_s_central_community_/1428826", "title"=>"Fecundity of socially dominant chimpanzees is most influential in Gombe’s central community.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085805"], "description"=>"<p>Shown is a neighbor-joining phylogenetic tree for the exon 2 sequences of representative <i>MHC-B</i> alleles and the four novel, nonrecombinant Gombe <i>Patr-B</i> alleles (A). An African green monkey (<i>Chlorocebus sabaeus</i>) <i>MHC-B</i> is the outgroup (<i>Chsa</i>, red) in panel A. The gray shaded box denotes the unique clade containing <i>Patr-B*06:03</i> (bold blue). This clade is maintained in trees constructed from the sequence of codons 62–74 (B), but not in trees constructed from exon 2 sequences with codons 62–74 deleted (C). This shows that codons 62–74 are the basis for the clade and the relatedness of its members. Nodal bootstrap values are based on 1,000 replications, and only values with at least 50% support are shown. Nodes that were collapsed are represented by large, black triangles. Chimpanzee alleles (<i>Patr</i>) are in blue. Also included are human (<i>HLA</i>, black), orangutan (<i>Popy</i>, pink), western gorilla (<i>Gogo</i>, green), and white-handed gibbon (<i>Hyla</i>, orange) <i>MHC-B</i>. Bonobo (<i>Papa</i>) sequences were also included in the analysis, but are within the collapsed nodes. <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s015\" target=\"_blank\">S7 Fig</a> gives the full trees with all the taxa, and the sequences are included in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s002\" target=\"_blank\">S2 Data</a>. (D) The trans-species clade containing Patr-B*06:03 (bold blue) and HLA-B*57:01 is defined by an extensive sequence motif covering residues 25–74 of the α<sub>2</sub> domain. The sequences of representative MHC-B allotypes that are in the clade, or not in the clade (Other), are compared. Only positions of difference are shown. Identity to the consensus is shown by a dash, with differences from the consensus being shown by the amino acid substitution. Black-filled boxes show residues of the B pocket that bind the anchor residue at position 2 (P2) of peptide antigens [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref053\" target=\"_blank\">53</a>,<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref054\" target=\"_blank\">54</a>]. Under “Anchor” and “P2” are listed the anchor residues at P2 that are predicted to bind to each MHC-B allotype (compiled from the SYFPEITHI database of MHC ligands and peptide motifs, <a href=\"http://www.syfpeithi.de/\" target=\"_blank\">http://www.syfpeithi.de/</a> [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref055\" target=\"_blank\">55</a>] and de Groot et al. (2010) [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref041\" target=\"_blank\">41</a>]). Patr-B P2 residues that were inferred from known ligands are in gray italics. HLA-B*08:01 is distinguished by having a P3 anchor residue [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref055\" target=\"_blank\">55</a>]. Residue positions that have been associated with control of HIV are indicated by white numbers on black background [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref046\" target=\"_blank\">46</a>,<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref056\" target=\"_blank\">56</a>].</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428821, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g008", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SIVcpz_associated_Patr_B_06_03_is_related_in_structure_and_evolution_to_HLA_B_57_01_/1428821", "title"=>"SIVcpz-associated Patr-B*06:03 is related in structure and evolution to HLA-B*57:01.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085804"], "description"=>"<p>(A) Comparison of <i>Patr-B</i> allele frequencies in SIVcpz-infected and uninfected Gombe chimpanzees. The <i>Patr-B*06:03, B*22:03,</i> and <i>B*22:05</i> alleles are at elevated frequency in the SIVcpz-infected chimpanzees. In contrast, the frequency of <i>Patr-B*22:04</i> is lowered in the SIVcpz-infected chimpanzees. Asterisks denote differences between the SIVcpz-infected (red) (N = 30) and uninfected (black) (N = 95) subpopulations (Fisher’s Exact tests, <i>p</i>-values given underneath the asterisks *<i>p</i> < 0.1 and **<i>p</i> < 0.05). The frequencies for this figure are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s003\" target=\"_blank\">S3 Data</a>. (B) Sites of amino acid difference that distinguish Patr-B*22 subtypes. “<i>P.t.s.</i>” is <i>P. t. schweinfurthii</i>; “<i>P.t.v.</i>” is <i>P. t. verus</i>. Patr-B*39:01 is included because it has structural similarities with Patr-B*22, including an α<sub>1</sub> domain that is identical to that of Patr-B*22:03 and B*22:05.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428820, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g007", "stats"=>{"downloads"=>0, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_the_Gombe_chimpanzees_SIVcpz_infection_correlates_with_increased_frequencies_for_three_Patr_B_alleles_/1428820", "title"=>"In the Gombe chimpanzees, SIVcpz infection correlates with increased frequencies for three <i>Patr-B</i> alleles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085801"], "description"=>"<p>Pairwise nucleotide differences (p-distances) in the sequences of exons 2 and 3 were calculated for each set of comparisons listed. “<i>P.t.s.</i>” is <i>P. t. schweinfurthii</i>; “<i>P.t.v.</i>” is <i>P. t. verus</i>; “<i>P.t.t.</i>” is <i>P. t. troglodytes</i>. The number of alleles in each set being compared is given in parentheses. Histogram distributions and statistics are given in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s012\" target=\"_blank\">S4 Fig</a>. The alleles used to generate the p-distances are listed in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s014\" target=\"_blank\">S6 Fig</a>, and their sequences are included in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s002\" target=\"_blank\">S2 Data</a>.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428817, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g004", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_diversity_of_the_polymorphic_exons_of_chimpanzee_and_human_MHC_B_alleles_/1428817", "title"=>"Sequence diversity of the polymorphic exons of chimpanzee and human <i>MHC-B</i> alleles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085799"], "description"=>"<p>Gombe National Park is small, covering 35 square kilometers of mountainous terrain in northwest Tanzania and has many streams that flow into Lake Tanganyika. The thick black line in the map shows the park boundary. The blue line denotes the territory in 2010 of the northern community (N), the orange line denotes the territory of the central community (C), and the dashed purple line denotes the approximate territory of the southern community (S). The inset map shows the location of the park, both within Tanzania and relative to other East African countries: Rwanda (R), Burundi (B), Democratic Republic of Congo (D), Malawi (M), and Mozambique (MZ). Within each community, the number of individuals sampled is given in parentheses, followed by the mean SIVcpz prevalence [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref016\" target=\"_blank\">16</a>]. Shown for each community are the high-frequency <i>Patr-B</i> alleles. The expanding northern and central communities maintained the same high-frequency alleles throughout the study (1995–2010), while it changed in the southern community, as shown by the arrow. Immigrant females (indicated by “I”) and their progeny were responsible for the high-frequency allele in the north, whereas in the central community, that role was played by the progeny of fecund males and females (indicated by “F”). The map was created by Steffen Foerster, The Jane Goodall Institute Research Center, Duke University.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428815, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g002", "stats"=>{"downloads"=>0, "page_views"=>36, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Territories_of_the_three_chimpanzee_communities_in_Gombe_National_Park_/1428815", "title"=>"Territories of the three chimpanzee communities in Gombe National Park.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085800"], "description"=>"<p>The upper panels give the <i>Patr-B</i> allele frequencies for the entire Gombe population (A), the northern community (B), the central community (C), and the southern community (D). The Gombe chimpanzees are of subspecies <i>P. t. schweinfurthii</i>. (B-D) Underlined are the names of alleles not present in all three communities. The lower panels show the <i>Patr-B</i> allele frequencies for the Biomedical Primate Research Centre (BPRC) chimpanzee population, subspecies <i>P. t. verus</i> [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref041\" target=\"_blank\">41</a>] (E) (further described in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s027\" target=\"_blank\">S1 Text</a>), and the <i>HLA-B</i> allele frequencies (in gray) in the Hadza [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref042\" target=\"_blank\">42</a>] (F), Tao [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref043\" target=\"_blank\">43</a>] (G), Kampala [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref043\" target=\"_blank\">43</a>,<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref044\" target=\"_blank\">44</a>] (H), and Bergamo [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref043\" target=\"_blank\">43</a>] (I) human populations. The Hadza and Tao are indigenous, tribal populations from Africa (Tanzania) and Asia (Taiwan), respectively; Kampala and Bergamo are admixed urban populations from Africa (Kampala, Uganda) and Europe (Bergamo, Italy), respectively. The wider brackets (A and C) show that the two most common alleles are significantly more frequent than all other alleles, but do not differ significantly from each other; the narrower brackets (B, E, F, and G) show that the most common allele is significantly more frequent than the second most common allele (Fisher’s Exact tests, <i>p</i>-values given below the bracket (<i>p</i> < 0.0001 applies to both higher frequency alleles in A and C)). The asterisk (E) indicates that the second most common alleles, in Gombe and BPRC, have significantly different frequencies (Fisher’s Exact test, <i>p</i> = 0.033). Overall, the <i>Patr-B</i> frequency distributions for Gombe and BPRC do not differ significantly (<i>χ<sup>2</sup></i> test) (In this analysis, the frequencies of the two rarest Gombe alleles were combined so as to give equal allele numbers for the two populations). The <i>HLA-B</i> distributions of the indigenous human populations do not differ significantly from the <i>Patr-B</i> distributions of the chimpanzee populations. The <i>HLA-B</i> distributions in urban human populations do differ significantly (<i>χ<sup>2</sup></i> tests, <i>p</i> < 0.01) from the Patr-B distributions of the chimpanzee populations (In this analysis, only the three most common alleles were included individually; all other alleles were combined to equalize the number of alleles for the different populations). N: the number of individuals analyzed. Data for this figure are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s001\" target=\"_blank\">S1 Data</a>.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428816, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g003", "stats"=>{"downloads"=>0, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Frequency_distribution_of_MHC_B_alleles_in_chimpanzee_and_human_populations_/1428816", "title"=>"Frequency distribution of <i>MHC-B</i> alleles in chimpanzee and human populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085813", "https://ndownloader.figshare.com/files/2085814", "https://ndownloader.figshare.com/files/2085815", "https://ndownloader.figshare.com/files/2085816", "https://ndownloader.figshare.com/files/2085817", "https://ndownloader.figshare.com/files/2085818", "https://ndownloader.figshare.com/files/2085819", "https://ndownloader.figshare.com/files/2085820", "https://ndownloader.figshare.com/files/2085821", "https://ndownloader.figshare.com/files/2085822", "https://ndownloader.figshare.com/files/2085823", "https://ndownloader.figshare.com/files/2085824", "https://ndownloader.figshare.com/files/2085825", "https://ndownloader.figshare.com/files/2085826", "https://ndownloader.figshare.com/files/2085827", "https://ndownloader.figshare.com/files/2085828", "https://ndownloader.figshare.com/files/2085829", "https://ndownloader.figshare.com/files/2085830", "https://ndownloader.figshare.com/files/2085831", "https://ndownloader.figshare.com/files/2085832", "https://ndownloader.figshare.com/files/2085833", "https://ndownloader.figshare.com/files/2085834", "https://ndownloader.figshare.com/files/2085835", "https://ndownloader.figshare.com/files/2085836", "https://ndownloader.figshare.com/files/2085837", "https://ndownloader.figshare.com/files/2085838", "https://ndownloader.figshare.com/files/2085839"], "description"=>"<div><p>Major histocompatibility complex (MHC) class I molecules determine immune responses to viral infections. These polymorphic cell-surface glycoproteins bind peptide antigens, forming ligands for cytotoxic T and natural killer cell receptors. Under pressure from rapidly evolving viruses, hominoid MHC class I molecules also evolve rapidly, becoming diverse and species-specific. Little is known of the impact of infectious disease epidemics on MHC class I variant distributions in human populations, a context in which the chimpanzee is the superior animal model. Population dynamics of the chimpanzees inhabiting Gombe National Park, Tanzania have been studied for over 50 years. This population is infected with SIVcpz, the precursor of human HIV-1. Because HLA-B is the most polymorphic human MHC class I molecule and correlates strongly with HIV-1 progression, we determined sequences for its ortholog, Patr-B, in 125 Gombe chimpanzees. Eleven Patr-B variants were defined, as were their frequencies in Gombe’s three communities, changes in frequency with time, and effect of SIVcpz infection. The growing populations of the northern and central communities, where SIVcpz is less prevalent, have stable distributions comprising a majority of low-frequency Patr-B variants and a few high-frequency variants. Driving the latter to high frequency has been the fecundity of immigrants to the northern community, whereas in the central community, it has been the fecundity of socially dominant individuals. In the declining population of the southern community, where greater SIVcpz prevalence is associated with mortality and emigration, Patr-B variant distributions have been changing. Enriched in this community are Patr-B variants that engage with natural killer cell receptors. Elevated among SIVcpz-infected chimpanzees, the Patr-B*06:03 variant has striking structural and functional similarities to HLA-B*57, the human allotype most strongly associated with delayed HIV-1 progression. Like HLA-B*57, Patr-B*06:03 correlates with reduced viral load, as assessed by detection of SIVcpz RNA in feces.</p></div>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428829, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1002144.s001", "https://dx.doi.org/10.1371/journal.pbio.1002144.s002", "https://dx.doi.org/10.1371/journal.pbio.1002144.s003", "https://dx.doi.org/10.1371/journal.pbio.1002144.s004", "https://dx.doi.org/10.1371/journal.pbio.1002144.s005", "https://dx.doi.org/10.1371/journal.pbio.1002144.s006", "https://dx.doi.org/10.1371/journal.pbio.1002144.s007", "https://dx.doi.org/10.1371/journal.pbio.1002144.s008", "https://dx.doi.org/10.1371/journal.pbio.1002144.s009", "https://dx.doi.org/10.1371/journal.pbio.1002144.s010", "https://dx.doi.org/10.1371/journal.pbio.1002144.s011", "https://dx.doi.org/10.1371/journal.pbio.1002144.s012", "https://dx.doi.org/10.1371/journal.pbio.1002144.s013", "https://dx.doi.org/10.1371/journal.pbio.1002144.s014", "https://dx.doi.org/10.1371/journal.pbio.1002144.s015", "https://dx.doi.org/10.1371/journal.pbio.1002144.s016", "https://dx.doi.org/10.1371/journal.pbio.1002144.s017", "https://dx.doi.org/10.1371/journal.pbio.1002144.s018", "https://dx.doi.org/10.1371/journal.pbio.1002144.s019", "https://dx.doi.org/10.1371/journal.pbio.1002144.s020", "https://dx.doi.org/10.1371/journal.pbio.1002144.s021", "https://dx.doi.org/10.1371/journal.pbio.1002144.s022", "https://dx.doi.org/10.1371/journal.pbio.1002144.s023", "https://dx.doi.org/10.1371/journal.pbio.1002144.s024", "https://dx.doi.org/10.1371/journal.pbio.1002144.s025", "https://dx.doi.org/10.1371/journal.pbio.1002144.s026", "https://dx.doi.org/10.1371/journal.pbio.1002144.s027"], "stats"=>{"downloads"=>15, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Signature_Patterns_of_MHC_Diversity_in_Three_Gombe_Communities_of_Wild_Chimpanzees_Reflect_Fitness_in_Reproduction_and_Immune_Defense_against_SIVcpz_/1428829", "title"=>"Signature Patterns of MHC Diversity in Three Gombe Communities of Wild Chimpanzees Reflect Fitness in Reproduction and Immune Defense against SIVcpz", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085798"], "description"=>"<p>Humans and chimpanzees have six orthologous MHC class I genes: <i>MHC-A, -B, -C, -E, -F,</i> and <i>-G</i>. Human genes and alleles have the prefix <i>HLA-</i> (Human Leukocyte Antigen). Chimpanzee genes and alleles have the prefix <i>Patr-</i> (<i>Pan troglodytes</i>). The gene map shows their relative organization within the MHC. Each gene encodes a cell-surface glycoprotein that is involved in activating cytotoxic T and NK cell responses against infection. <i>MHC-A, -B,</i> and -<i>C</i> (orange) are highly polymorphic; <i>MHC-E, F,</i> and <i>G</i> (gray) are conserved. Under “MHC class I” are given the number of protein variants (allotypes) so far defined for each gene. For chimpanzees, these numbers are given for the three subspecies studied: <i>P. t. schweinfurthii (P.t.s.)</i> (the number given includes the novel <i>Patr-B</i> alleles defined in this study), <i>P. t. verus (P.t.v.)</i>, and <i>P. t. troglodytes (P.t.t.)</i>. For the subspecies <i>P. t. ellioti</i>, MHC class I genes have yet to be studied. The sum of all chimpanzee allotypes identified is given under “Total.” The subspecies origin of the <i>Patr-E</i> variant sequenced is not known. Under “Nomenclature” is shown the standardized nomenclature for <i>Patr-B</i> alleles, the subject of this paper. Further information is given on the <a href=\"http://www.ebi.ac.uk/ipd/imgt/hla/\" target=\"_blank\">http://www.ebi.ac.uk/ipd/imgt/hla/</a> and <a href=\"http://www.ebi.ac.uk/ipd/mhc/\" target=\"_blank\">http://www.ebi.ac.uk/ipd/mhc/</a> websites [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.ref021\" target=\"_blank\">21</a>].</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428814, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g001", "stats"=>{"downloads"=>0, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Organization_and_polymorphism_of_human_and_chimpanzee_major_histocompatibility_complex_MHC_class_I_genes_/1428814", "title"=>"Organization and polymorphism of human and chimpanzee major histocompatibility complex (MHC) class I genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085807"], "description"=>"<p>(A) Shows changes in population size for the central (orange), northern (blue), and southern (purple) communities between the years 1995 and 2010. The earliest census year was 1998 for the southern community. The number of <i>Patr-B</i> alleles is given at each time point: diamonds for the central, rectangles for the northern, and triangles for the southern community. (B) Shows the temporal variation of <i>Patr-B</i> allele frequencies and the contribution of immigrant females and their offspring to the northern Gombe community. Partial gray shading of the frequency gives the contribution made by immigrant females who arrived during the study period and their offspring. <i>P.t.s.</i> N is the number of individuals that were genotyped for <i>Patr-B</i> out of the total number of individuals alive on the first day of the year. <i>Patr-B</i> N is the number of alleles present within the community. The brackets in 2000 and 2005 indicate a difference in the frequencies between the two most frequent alleles; the bracket between alleles in 2010 indicates that the highest frequency allele is significantly elevated compared to the third highest frequency allele (Fisher’s Exact tests, <i>p</i>-values given below the brackets). (C) Temporal variation of <i>Patr-B</i> allele frequencies and the contribution of immigrant females and their offspring to the southern community (Distributions for all three communities are provided together in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s021\" target=\"_blank\">S13 Fig</a>). Partial gray shading of the frequency bars represents the contribution of immigrant females that arrived during the study period and their offspring. <i>P.t.s.</i> N is the number of individuals that were genotyped for <i>Patr-B</i> out of the total number of individuals alive on the first day of the year. <i>Patr-B</i> N is the number of alleles present within the community. The bracket in 1998 indicates a difference in the frequencies between the two most frequent alleles; the bracket between alleles in 2000 indicates that the highest frequency allele is significantly elevated compared to the third highest frequency allele (Fisher’s Exact tests, <i>p</i>-values given below the brackets). The overall frequency distribution for the southern community is significantly different between 2000 and 2005 (<i>χ<sup>2</sup></i> = 11.343, <i>p</i> < 0.025) (all within-community frequency distributions (between time points) and comparison statistics for the total allele frequency distributions for all three communities are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s020\" target=\"_blank\">S12 Fig</a>). Community size and frequency data are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s004\" target=\"_blank\">S4 Data</a>.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428823, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g009", "stats"=>{"downloads"=>0, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Population_dynamics_of_Patr_B_in_the_three_communities_of_Gombe_chimpanzees_/1428823", "title"=>"Population dynamics of <i>Patr-B</i> in the three communities of Gombe chimpanzees.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085808"], "description"=>"<p>(A) Patr-B*23:05 is the only Gombe Patr-B allotype that carries the Bw4 epitope, a ligand for KIR receptors of NK cells. Similarly, Patr-B*28:01 is the only Gombe Patr-B allotype that carries the C1 epitope, also a ligand for KIR. Shown are the temporal changes in the frequencies of <i>Patr-B*23:05</i> (green bars) and <i>Patr-B*28:01</i> (purple bars) in the three Gombe communities. In the northern and central communities, these frequencies were relatively stable, whereas in the southern community, there was a steady increase in the frequency of Bw4-bearing Patr-B*23:05 during 2000–2010 when the southern community was declining (Fisher’s Exact test, <i>p</i> = 0.099). Although not significant, a monotonic increase in the frequency of C1-bearing Patr-B*28:01 is also seen. The earliest census year was 1995 for the central and northern communities, and 1998 for the southern community. The community frequency data for these alleles are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s004\" target=\"_blank\">S4 Data</a>. (B) This compares <i>Patr-B</i> allele frequencies for natal (black bars) and immigrant (colored bars) female chimpanzees of the northern and central communities. The <i>Patr-B*23:05</i> and <i>Patr-B*17:03</i> alleles are enriched among natal females, but not immigrant females. Significance is denoted by asterisks (Fisher’s Exact tests, <i>p</i>-values are given beneath the asterisks). The frequency data are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002144#pbio.1002144.s006\" target=\"_blank\">S6 Data</a>.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428824, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g010", "stats"=>{"downloads"=>0, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_frequency_of_the_Bw4_KIR_ligand_is_elevated_among_natal_females_and_has_increased_in_the_southern_community_/1428824", "title"=>"The frequency of the Bw4 KIR ligand is elevated among natal females and has increased in the southern community.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085803"], "description"=>"<p>Plus and minus superscripts following C1 and Bw4 indicate presence or absence of the epitope. (A) Gives the distribution of the C1 and Bw4 epitopes recognized by KIR among the known 16 <i>P. t. schweinfurthii</i> (<i>P.t.s.</i>) and 21 <i>P. t. verus</i> (<i>P.t.v.</i>) <i>Patr-B</i> allotypes. The Gombe <i>P. t. schweinfurthii</i> allotypes are considered as a separate group from the “Other” <i>P. t. schweinfurthii</i> allotypes that are not present in the Gombe population. Likewise, the BPRC <i>P. t. verus</i> allotypes are considered as a separate group from the “Other” <i>P. t. verus</i> allotypes that are not present in the BPRC population. (B) Gives the frequencies of the <i>Patr-B</i> alleles encoding C1 and Bw4 epitopes in the Gombe and BPRC chimpanzee populations. Frequencies were transformed to integers by multiplying times 10<sup>3</sup>. Statistical significance was tested using Fisher’s exact tests, and <i>p</i>-values are provided (Gombe-BPRC comparison (p)). (C) Gives the phenotype frequency of the C1 and Bw4 epitopes in the Gombe and BPRC populations. Statistical significance was tested using Fisher’s exact tests and <i>p</i>-values are provided (Gombe-BPRC comparison (p)).</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428819, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g006", "stats"=>{"downloads"=>1, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significant_differences_in_the_Gombe_and_BPRC_Patr_B_allotypes_bearing_C1_and_Bw4_KIR_ligands_/1428819", "title"=>"Significant differences in the Gombe and BPRC Patr-B allotypes bearing C1 and Bw4 KIR ligands.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2085802"], "description"=>"<p>(A) Displayed are the amino acid sequence differences that distinguish the α<sub>1</sub> and α<sub>2</sub> domains of Gombe <i>P. t. schweinfurthii</i> (upper group) and BPRC <i>P. t. verus</i> (lower group) Patr-B allotypes. Only polymorphic positions are included. Identity to the consensus is denoted by a dash. For amino acid differences from the consensus, the residue is shown. The black-filled boxes between the two sets of sequences show which residues contribute to binding sites for peptide, T cell receptor (TCR), CD8 T-cell coreceptor (CD8), KIR and the invariant β<sub>2</sub>-microglobulin subunit (β<sub>2</sub>-m) of the MHC class I molecule. In bold are the names of “novel” alleles, which were discovered in the Gombe population. Positions highlighted in gray are polymorphic in one population but not the other. (B) Histograms showing the value of the sequence variability coefficient, W, for the Gombe (upper) and BPRC (lower) Patr-B allotypes. The histograms are in vertical alignment with the sequence alignment in (A). For each population, the horizontal dashed lines mark the value for W that is twice the mean W value for all polymorphic residues in the population.</p>", "links"=>[], "tags"=>["killer cell receptors", "frequency", "Gombe National Park", "molecule", "Wild Chimpanzees Reflect Fitness", "SIVcpz Major histocompatibility", "MHC class", "rna", "125 Gombe chimpanzees", "hiv", "hominoid MHC class", "variant"], "article_id"=>1428818, "categories"=>["Biological Sciences"], "users"=>["Emily E. Wroblewski", "Paul J. Norman", "Lisbeth A. Guethlein", "Rebecca S. Rudicell", "Miguel A. Ramirez", "Yingying Li", "Beatrice H. Hahn", "Anne E. Pusey", "Peter Parham"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002144.g005", "stats"=>{"downloads"=>1, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Extensive_amino_acid_sequence_polymorphism_in_the_Patr_B_allotypes_of_the_Gombe_and_BPRC_chimpanzees_/1428818", "title"=>"Extensive amino acid sequence polymorphism in the Patr-B allotypes of the Gombe and BPRC chimpanzees.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-28 02:49:18"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
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  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"25", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"1", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"38", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
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  • {"unique-ip"=>"5", "full-text"=>"9", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"12", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}

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