Macrophage-Derived Human Resistin Is Induced in Multiple Helminth Infections and Promotes Inflammatory Monocytes and Increased Parasite Burden
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{"title"=>"Macrophage-Derived Human Resistin Is Induced in Multiple Helminth Infections and Promotes Inflammatory Monocytes and Increased Parasite Burden", "type"=>"journal", "authors"=>[{"first_name"=>"Jessica C.", "last_name"=>"Jang", "scopus_author_id"=>"56038180400"}, {"first_name"=>"Gang", "last_name"=>"Chen", "scopus_author_id"=>"57113921600"}, {"first_name"=>"Spencer H.", "last_name"=>"Wang", "scopus_author_id"=>"56532209600"}, {"first_name"=>"Mark A.", "last_name"=>"Barnes", "scopus_author_id"=>"23767014100"}, {"first_name"=>"Josiah I.", "last_name"=>"Chung", "scopus_author_id"=>"56532230300"}, {"first_name"=>"Mali", "last_name"=>"Camberis", "scopus_author_id"=>"6507035696"}, {"first_name"=>"Graham", "last_name"=>"Le Gros", "scopus_author_id"=>"7005876876"}, {"first_name"=>"Philip J.", "last_name"=>"Cooper", "scopus_author_id"=>"7402087724"}, {"first_name"=>"Cathy", "last_name"=>"Steel", "scopus_author_id"=>"7102708217"}, {"first_name"=>"Thomas B.", "last_name"=>"Nutman", "scopus_author_id"=>"7102482146"}, {"first_name"=>"Mitchell A.", "last_name"=>"Lazar", "scopus_author_id"=>"7201649830"}, {"first_name"=>"Meera G.", "last_name"=>"Nair", "scopus_author_id"=>"7202870862"}], "year"=>2015, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-84923826412", "sgr"=>"84923826412", "doi"=>"10.1371/journal.ppat.1004579", "pui"=>"602679693", "issn"=>"15537374", "isbn"=>"1553-7366", "pmid"=>"25568944"}, "id"=>"d3e5f719-390c-32ec-abd3-3d2f9c7ecf15", "abstract"=>"Parasitic helminth infections can be associated with lifelong morbidity such as immune-mediated organ failure. A better understanding of the host immune response to helminths could provide new avenues to promote parasite clearance and/or alleviate infection-associated morbidity. Murine resistin-like molecules (RELM) exhibit pleiotropic functions following helminth infection including modulating the host immune response; however, the relevance of human RELM proteins in helminth infection is unknown. To examine the function of human resistin (hResistin), we utilized transgenic mice expressing the human resistin gene (hRetnTg+). Following infection with the helminth Nippostrongylus brasiliensis (Nb), hResistin expression was significantly upregulated in infected tissue. Compared to control hRetnTg- mice, hRetnTg+ mice suffered from exacerbated Nb-induced inflammation characterized by weight loss and increased infiltration of inflammatory monocytes in the lung, along with elevated Nb egg burdens and delayed parasite expulsion. Genome-wide transcriptional profiling of the infected tissue revealed that hResistin promoted expression of proinflammatory cytokines and genes downstream of toll-like receptor signaling. Moreover, hResistin preferentially bound lung monocytes, and exogenous treatment of mice with recombinant hResistin promoted monocyte recruitment and proinflammatory cytokine expression. In human studies, increased serum resistin was associated with higher parasite load in individuals infected with soil-transmitted helminths or filarial nematode Wuchereria bancrofti, and was positively correlated with proinflammatory cytokines. Together, these studies identify human resistin as a detrimental factor induced by multiple helminth infections, where it promotes proinflammatory cytokines and impedes parasite clearance. Targeting the resistin/proinflammatory cytokine immune axis may provide new diagnostic or treatment strategies for helminth infection and associated immune-mediated pathology. Copyright © 2015.", "link"=>"http://www.mendeley.com/research/macrophagederived-human-resistin-induced-multiple-helminth-infections-promotes-inflammatory-monocyte", "reader_count"=>42, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>5, "Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. 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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1862822", "https://ndownloader.figshare.com/files/1862823", "https://ndownloader.figshare.com/files/1862824", "https://ndownloader.figshare.com/files/1862825", "https://ndownloader.figshare.com/files/1862827", "https://ndownloader.figshare.com/files/1862829"], "description"=>"<div><p>Parasitic helminth infections can be associated with lifelong morbidity such as immune-mediated organ failure. A better understanding of the host immune response to helminths could provide new avenues to promote parasite clearance and/or alleviate infection-associated morbidity. Murine resistin-like molecules (RELM) exhibit pleiotropic functions following helminth infection including modulating the host immune response; however, the relevance of human RELM proteins in helminth infection is unknown. To examine the function of human resistin (hResistin), we utilized transgenic mice expressing the human resistin gene (h<i>Retn</i>Tg<sup>+</sup>). Following infection with the helminth <i>Nippostrongylus brasiliensis</i> (<i>Nb</i>), hResistin expression was significantly upregulated in infected tissue. Compared to control h<i>Retn</i>Tg<sup>−</sup> mice, h<i>Retn</i>Tg<sup>+</sup> mice suffered from exacerbated <i>Nb</i>-induced inflammation characterized by weight loss and increased infiltration of inflammatory monocytes in the lung, along with elevated <i>Nb</i> egg burdens and delayed parasite expulsion. Genome-wide transcriptional profiling of the infected tissue revealed that hResistin promoted expression of proinflammatory cytokines and genes downstream of toll-like receptor signaling. Moreover, hResistin preferentially bound lung monocytes, and exogenous treatment of mice with recombinant hResistin promoted monocyte recruitment and proinflammatory cytokine expression. In human studies, increased serum resistin was associated with higher parasite load in individuals infected with soil-transmitted helminths or filarial nematode <i>Wuchereria bancrofti</i>, and was positively correlated with proinflammatory cytokines. Together, these studies identify human resistin as a detrimental factor induced by multiple helminth infections, where it promotes proinflammatory cytokines and impedes parasite clearance. Targeting the resistin/proinflammatory cytokine immune axis may provide new diagnostic or treatment strategies for helminth infection and associated immune-mediated pathology.</p></div>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286281, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004579.s001", "https://dx.doi.org/10.1371/journal.ppat.1004579.s002", "https://dx.doi.org/10.1371/journal.ppat.1004579.s003", "https://dx.doi.org/10.1371/journal.ppat.1004579.s004", "https://dx.doi.org/10.1371/journal.ppat.1004579.s005", "https://dx.doi.org/10.1371/journal.ppat.1004579.s006"], "stats"=>{"downloads"=>13, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Macrophage_Derived_Human_Resistin_Is_Induced_in_Multiple_Helminth_Infections_and_Promotes_Inflammatory_Monocytes_and_Increased_Parasite_Burden_/1286281", "title"=>"Macrophage-Derived Human Resistin Is Induced in Multiple Helminth Infections and Promotes Inflammatory Monocytes and Increased Parasite Burden", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862820"], "description"=>"<p>Many inflammatory factors are positively correlated with resistin in humans infected with soil-transmitted helminths or filarial nematodes.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286279, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.t001", "stats"=>{"downloads"=>2, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Many_inflammatory_factors_are_positively_correlated_with_resistin_in_humans_infected_with_soil_transmitted_helminths_or_filarial_nematodes_/1286279", "title"=>"Many inflammatory factors are positively correlated with resistin in humans infected with soil-transmitted helminths or filarial nematodes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862819"], "description"=>"<p>(A) Serum resistin from uninfected (n = 51) or STH-infected children (n = 49) was measured. (B) The fecal egg burdens in infected children was quantified as <i>A. lumbricoides</i> eggs per gram feces (alepg) and plotted against serum resistin and TNFα. (C) Proinflammatory cytokines were positively correlated with resistin in the serum of STH-infected children. (D) Serum from uninfected endemic normal individuals (n = 17) or patients infected with <i>Wuchereria bancrofti</i> (n = 44) was analyzed by ELISA for resistin. (E) In infected individuals, a positive correlation was observed between the circulating microfilariae and resistin or TNFα. (F) Proinflammatory cytokines were positively correlated with resistin levels in the serum of infected patients.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286278, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g008", "stats"=>{"downloads"=>0, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_resistin_in_human_patients_infected_with_STH_or_filarial_nematodes_/1286278", "title"=>"Expression of resistin in human patients infected with STH or filarial nematodes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862816"], "description"=>"<p>(A-B) Lung cells from <i>Nb</i>-infected mice were incubated with recombinant hResistin followed by detection with α-hRetn to determine which cells can bind hResistin compared with control PBS (A). Surface expression of the hResistin-bound cells identified monocytes as the main cell-type that bound hResistin (B). (C) Sorted lung cells from <i>Nb</i>-infected h<i>Retn</i>Tg<sup>−</sup> and h<i>Retn</i>Tg<sup>+</sup> mice were analyzed for proinflammatory gene expression by real-time PCR. Data (mean ± SEM, n = 3–4 per group) are representative of two separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286275, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g006", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Monocytes_and_neutrophils_are_the_main_cellular_targets_of_hResistin_during_Nb_infection_/1286275", "title"=>"Monocytes and neutrophils are the main cellular targets of hResistin during <i>Nb</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862809"], "description"=>"<p>(A) h<i>Retn</i>Tg<sup>−</sup> mice or h<i>Retn</i>Tg<sup>+</sup> mice were infected with <i>Nb</i> and weight loss was measured as a percentage of original weight. (B-C) Lung sections from naïve or <i>Nb</i>-infected mice were stained with H&E (B, scale bar  = 200 µm) and pathology at day 7 post-infection was assessed by blind scoring (C). (D-E) At day 7 post infection, total BAL cells were quantified (D) and dissociated lung cells were recovered for flow cytometry analysis of Ly6C<sup>+</sup> CD11b<sup>+</sup> monocytes (E). Data (mean ± SEM, n = 4–6 per group) are representative of three separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286268, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g003", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_hResistin_exacerbates_lung_inflammation_/1286268", "title"=>"Expression of hResistin exacerbates lung inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862806"], "description"=>"<p>(A) Gating strategy for sorted lung cells from <i>Nb</i>-infected mice for CD11b<sup>+</sup>Ly6C<sup>+</sup> monocytes, SiglecF<sup>+</sup>CD11c<sup>−</sup> eosinophils, CD11b<sup>+</sup>Ly6G<sup>+</sup> neutrophils, and CD11c<sup>+</sup>F4/80<sup>+</sup> alveolar macrophages and corresponding H&E stained cytospins. (B) Sorted cells were recovered for RNA and analyzed for h<i>Retn</i> by real-time PCR. Data (mean ± SEM, n = 3–4 per group) are representative of three separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286265, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g002", "stats"=>{"downloads"=>2, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Monocytes_neutrophils_and_alveolar_macrophages_express_hResistin_in_Nb_infected_lungs_/1286265", "title"=>"Monocytes, neutrophils and alveolar macrophages express hResistin in <i>Nb</i>-infected lungs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862784"], "description"=>"<p>(A-B) hResistin expression in the lung and small intestine of naïve or <i>Nb</i>-infected mice was measured by real-time PCR analysis (A) or ELISA (B). (C) Quantification of hResistin expressing cells was performed on immunofluorescent stained lung sections. (D) IF staining for <i>Griffonia simplicifolia</i> lectin (red), hResistin (green), and DAPI (blue) was performed on lung tissue sections. Data (mean ± SEM, n = 4–6 per group) are representative of four separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286263, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Detection_of_hResistin_expression_in_Nb_infected_transgenic_mice_/1286263", "title"=>"Detection of hResistin expression in <i>Nb</i>-infected transgenic mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862817"], "description"=>"<p>(A-B) h<i>Retn</i>Tg<sup>+</sup> mice (black bars) and control h<i>Retn</i>Tg<sup>−</sup> mice (white bars) were infected with 500 L3 <i>Nb</i> worms followed by parasitology analysis by fecal egg counts (A) or adult parasite numbers in the intestine at day 9 (B). Data (mean ± SEM, n = 4–6 per group) are representative of three separate experiments. (C) Serum hResistin concentration in h<i>Retn</i>Tg<sup>+</sup> mice is positively correlated with <i>Nb</i> worms at day 7 post-infection (n = 12).</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286276, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g007", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_h_Retn_Tg_mice_are_more_susceptible_to_Nb_infection_/1286276", "title"=>"h<i>Retn</i>Tg<sup>+</sup> mice are more susceptible to <i>Nb</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862814"], "description"=>"<p>(A-B) Naïve BL/6 mice were treated with recombinant human resistin (500 ng) followed by flow cytometry analysis of CD115<sup>+</sup> Ly6C<sup>+</sup> inflammatory monocytes (A) and real-time PCR analysis of PEC RNA (B). Data (mean ± SEM, n = 3 per group) are representative of two separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286273, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g005", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_hResistin_recruits_inflammatory_monocytes_/1286273", "title"=>"hResistin recruits inflammatory monocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862812"], "description"=>"<p>(A) Venn diagrams demonstrate infection-induced genes in h<i>Retn</i>Tg<sup>−</sup> and h<i>Retn</i>Tg<sup>+</sup> mice. (B-C) Enriched biological pathways induced by <i>hRetn</i> were identified by (B) Gene Ontology and (C) KEGG annotations and represented as a graph and heatmap. (D) h<i>Retn</i>-induced TLR signaling and chemokine genes were validated by real-time PCR analysis of lung tissue. (E) Serum TNFα was quantified by ELISA. Data (mean ± SEM, n = 3–4 per group) are representative of two separate experiments.</p>", "links"=>[], "tags"=>["proinflammatory cytokine expression", "hRetnTg", "resistin", "proinflammatory cytokines", "RELM", "Multiple Helminth Infections", "Helminth infection", "exhibit pleiotropic functions", "Nb egg burdens", "monocyte", "parasite clearance", "hResistin", "filarial nematode Wuchereria bancrofti", "Parasite Burden Parasitic helminth infections", "helminth Nippostrongylus brasiliensis"], "article_id"=>1286271, "categories"=>["Biological Sciences"], "users"=>["Jessica C. Jang", "Gang Chen", "Spencer H. Wang", "Mark A. Barnes", "Josiah I. Chung", "Mali Camberis", "Graham Le Gros", "Philip J. Cooper", "Cathy Steel", "Thomas B. Nutman", "Mitchell A. Lazar", "Meera G. Nair"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004579.g004", "stats"=>{"downloads"=>1, "page_views"=>80, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_hResistin_promotes_type_1_inflammation_TLR_signaling_and_chemokines_/1286271", "title"=>"hResistin promotes type 1 inflammation, TLR signaling and chemokines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:14:58"}

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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"20", "full-text"=>"22", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"20", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"9", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"27", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"10", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

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

Net::HTTPInternalServerError

Source
Counter
Time
2019-04-06 02:41:27 UTC
Target URL
http://counter-101.soma.plos.org/api/v1.0/stats/doi/10.1371%2Fjournal.ppat.1004579
Trace

/app/models/concerns/networkable.rb:21:in `get_result'
/app/models/source.rb:165:in `get_data'
/app/models/retrieval_status.rb:47:in `perform_get_data'
/app/jobs/source_job.rb:52:in `block (2 levels) in perform'
/app/jobs/source_job.rb:51:in `block in perform'
/app/jobs/source_job.rb:35:in `each'
/app/jobs/source_job.rb:35:in `perform'