HrpA, an RNA Helicase Involved in RNA Processing, Is Required for Mouse Infectivity and Tick Transmission of the Lyme Disease Spirochete
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{"title"=>"HrpA, an RNA Helicase Involved in RNA Processing, Is Required for Mouse Infectivity and Tick Transmission of the Lyme Disease Spirochete", "type"=>"journal", "authors"=>[{"first_name"=>"Aydan", "last_name"=>"Salman-Dilgimen", "scopus_author_id"=>"23010201400"}, {"first_name"=>"Pierre Olivier", "last_name"=>"Hardy", "scopus_author_id"=>"35733989500"}, {"first_name"=>"Justin D.", "last_name"=>"Radolf", "scopus_author_id"=>"7005032724"}, {"first_name"=>"Melissa J.", "last_name"=>"Caimano", "scopus_author_id"=>"6701551795"}, {"first_name"=>"George", "last_name"=>"Chaconas", "scopus_author_id"=>"7003818877"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"24367266", "doi"=>"10.1371/journal.ppat.1003841", "sgr"=>"84892878516", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "scopus"=>"2-s2.0-84892878516", "issn"=>"15537374", "pui"=>"372180085"}, "id"=>"68caae90-7927-33a2-9e1c-d059c9c06e5b", "abstract"=>"The Lyme disease spirochete Borrelia burgdorferi must differentially express genes and proteins in order to survive in and transit between its tick vector and vertebrate reservoir. The putative DEAH-box RNA helicase, HrpA, has been recently identified as an addition to the spirochete's global regulatory machinery; using proteomic methods, we demonstrated that HrpA modulates the expression of at least 180 proteins. Although most bacteria encode an HrpA helicase, RNA helicase activity has never been demonstrated for HrpAs and the literature contains little information on the contribution of this protein to bacterial physiology or pathogenicity. In this work, we report that B. burgdorferi HrpA has RNA-stimulated ATPase activity and RNA helicase activity and that this enzyme is essential for both mammalian infectivity by syringe inoculation and tick transmission. Reduced infectivity of strains carrying mutations in the ATPase and RNA binding motif mutants suggests that full virulence expression requires both ATPase and coupled helicase activity. Microarray profiling revealed changes in RNA levels of two-fold, or less in an hrpA mutant versus wild-type, suggesting that the enzyme functions largely or exclusively at the post-transcriptional level. In this regard, northern blot analysis of selected gene products highly regulated by HrpA (bb0603 [p66], bba74, bb0241 [glpK], bb0242 and bb0243 [glpA]) suggests a role for HrpA in the processing and translation of transcripts. In addition to being the first demonstration of RNA helicase activity for a bacterial HrpA, our data indicate that the post-transcriptional regulatory functions of this enzyme are essential for maintenance of the Lyme disease spirochete's enzootic cycle.", "link"=>"http://www.mendeley.com/research/hrpa-rna-helicase-involved-rna-processing-required-mouse-infectivity-tick-transmission-lyme-disease", "reader_count"=>31, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Librarian"=>1, "Student > Doctoral Student"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>2, "Philosophy"=>1, "Social Sciences"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Social Sciences"=>{"Social Sciences"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Switzerland"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1323322", "https://ndownloader.figshare.com/files/1323323", "https://ndownloader.figshare.com/files/1323324", "https://ndownloader.figshare.com/files/1323325", "https://ndownloader.figshare.com/files/1323326", "https://ndownloader.figshare.com/files/1323327", "https://ndownloader.figshare.com/files/1323328"], "description"=>"<div><p>The Lyme disease spirochete <i>Borrelia burgdorferi</i> must differentially express genes and proteins in order to survive in and transit between its tick vector and vertebrate reservoir. The putative DEAH-box RNA helicase, HrpA, has been recently identified as an addition to the spirochete's global regulatory machinery; using proteomic methods, we demonstrated that HrpA modulates the expression of at least 180 proteins. Although most bacteria encode an HrpA helicase, RNA helicase activity has never been demonstrated for HrpAs and the literature contains little information on the contribution of this protein to bacterial physiology or pathogenicity. In this work, we report that <i>B. burgdorferi</i> HrpA has RNA-stimulated ATPase activity and RNA helicase activity and that this enzyme is essential for both mammalian infectivity by syringe inoculation and tick transmission. Reduced infectivity of strains carrying mutations in the ATPase and RNA binding motif mutants suggests that full virulence expression requires both ATPase and coupled helicase activity. Microarray profiling revealed changes in RNA levels of two-fold, or less in an <i>hrpA</i> mutant versus wild-type, suggesting that the enzyme functions largely or exclusively at the post-transcriptional level. In this regard, northern blot analysis of selected gene products highly regulated by HrpA (<i>bb0603</i> [<i>p66</i>], <i>bba74</i>, <i>bb0241</i> [<i>glpK</i>], <i>bb0242</i> and <i>bb0243</i> [<i>glpA</i>]) suggests a role for HrpA in the processing and translation of transcripts. In addition to being the first demonstration of RNA helicase activity for a bacterial HrpA, our data indicate that the post-transcriptional regulatory functions of this enzyme are essential for maintenance of the Lyme disease spirochete's enzootic cycle.</p></div>", "links"=>[], "tags"=>["rna", "helicase", "infectivity", "tick", "lyme"], "article_id"=>882592, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003841.s001", "https://dx.doi.org/10.1371/journal.ppat.1003841.s002", "https://dx.doi.org/10.1371/journal.ppat.1003841.s003", "https://dx.doi.org/10.1371/journal.ppat.1003841.s004", "https://dx.doi.org/10.1371/journal.ppat.1003841.s005", "https://dx.doi.org/10.1371/journal.ppat.1003841.s006", "https://dx.doi.org/10.1371/journal.ppat.1003841.s007"], "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HrpA_an_RNA_Helicase_Involved_in_RNA_Processing_Is_Required_for_Mouse_Infectivity_and_Tick_Transmission_of_the_Lyme_Disease_Spirochete_/882592", "title"=>"HrpA, an RNA Helicase Involved in RNA Processing, Is Required for Mouse Infectivity and Tick Transmission of the Lyme Disease Spirochete", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323302"], "description"=>"<p><b>A</b>) Structure of the dsRNA substrate. Preparation of the helicase substrate is described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#s4\" target=\"_blank\">Materials and Methods</a>. The long strand was prepared by <i>in vitro</i> transcription of pGEMX-1 that had been cleaved with NheI. The short strand was chemically synthesized and labeled with [γ-<sup>32</sup>P]ATP and polynucleotide kinase at the 5′ free end. The length of the double strand portion of the substrate is given in base pairs (bp), the single stranded and the overhang portions are given in nucleotides. <b>B</b>) Autoradiograph of a polyacrylamide gel used to assay RNA helicase activity. The helicase assay was carried out for the wild-type and 5 different <i>B. burgdorferi</i> HrpA mutant proteins as described in the <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#s4\" target=\"_blank\">Materials and Methods</a>. The enzymatic reaction products were resolved by 12% native PAGE followed by autoradiography. The autoradiograph shows wild-type and the S158A mutant HrpA as an example. Lane 1, No enzyme control, lane 2, ds RNA boiled at 95°C for 5 min to generate a marker for the single-stranded (SS) product. Lanes 3–5 contain wild-type HrpA and lines 6–8, the S158A HrpA mutant, with the indicated amounts of purified proteins. <b>C</b>) Quantification of Helicase Activity. Helicase assays were performed in duplicate for three different concentrations of each purified HrpA. The results are plotted as the percentage of double strand RNA substrate converted to single stand as a function of the amount of enzyme per microliter of reaction. Errors bars represent the standard deviation.</p>", "links"=>[], "tags"=>["helicase"], "article_id"=>882572, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g003", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RNA_helicase_assay_/882572", "title"=>"RNA helicase assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323278"], "description"=>"<p>Conserved sequence motifs II, III and V of DEAH box RNA helicases are shown, along with their primary functions. The numbers below the motif sequences represent the position of the conserved motifs in <i>Borrelia burgdorferi</i> HrpA. Amino acid residues that are conserved in the mentioned motifs are shown in bold and the residues mutated in this study are indicated.</p>", "links"=>[], "tags"=>["deah-box", "rna", "helicase", "motifs", "hrpa"], "article_id"=>882569, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conserved_DEAH_box_RNA_helicase_motifs_in_the_B_burgdorferi_HrpA_protein_used_for_point_mutations_/882569", "title"=>"Conserved DEAH-box RNA helicase motifs in the <i>B. burgdorferi</i> HrpA protein used for point mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323310"], "description"=>"<p>Purified RNA samples from the <i>hrpA</i> mutant (<i>hrpA</i>) and the complemented strain (<i>hrpA<sup>+</sup></i>) were run on a 1.2% agarose-formaldehyde gel with an RNA marker shown in lane M. Each panel shows a membrane strip that contains 10 µg of RNA from the mutant and the complemented <i>hrpA</i> strain. The blot was hybridized with a <sup>32</sup>P-labelled gene probe prepared by PCR using the indicated primers. The target transcripts were <i>p66 (bb0603) for </i><b>Panel A</b>, <i>bba74</i> for <b>Panel B</b>, <i>glpK</i> (<i>bb0241</i>) for <b>Panel C</b> , <i>glpA</i> (<i>bb0243</i>) for <b>Panel D</b> and <i>bb0242</i> for <b>Panel E</b>.</p>", "links"=>[], "tags"=>["blot", "glpk", "bb0242"], "article_id"=>882580, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Northern_blot_analysis_of_p66_oms28_glpK_bb0242_and_glpA_/882580", "title"=>"Northern blot analysis of p66, <i>oms28, glpK bb0242 and glpA</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323306"], "description"=>"<p>Gene level correlation of <i>hrpA</i> versus complemented <i>hrpA</i> strains of <i>B. burgdorferi</i> is plotted as the log<sub>2</sub> of normalized hybridization intensities of the <i>hrpA</i> strain and the complemented mutant. The green line in the middle shows where both strains have the same intensity and the outer green lines show where the intensities are two-fold apart.</p>", "links"=>[], "tags"=>[], "article_id"=>882576, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g005", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microarray_analysis_/882576", "title"=>"Microarray analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323304"], "description"=>"<p><b>A</b>) Schematics of the strategy used. The <i>B. burgdorferi hrpA</i> KO strain GCB1164 was transformed with a construct carrying either wild-type or mutated <i>hrpA</i> (<i>hrpA</i>+, a red star indicates the point mutation), a <i>PflgB</i>-driven kanamycin resistance cassette (green) and 500 bp of sequence downstream from <i>hrpA</i>, to replace the disrupted <i>hrpA</i> gene. The point mutations were transferred in the complementation plasmid pPOH62-1 using PacI and AgeI restriction sites. Allelic exchange was confirmed by PCR using primers indicated by an arrow. <b>B</b>) PCR verification of the allelic exchange. Each construct was confirmed with four PCR analyses. <b>Panel 1</b>) The loss of gentamicin-resistance cassette following allelic exchange was confirmed as shown. The shuttle vector pBSV2G served as the positive control (c<sup>+</sup>) for amplification of the <i>gent</i> cassette (lane 5). <b>Panel 2</b>) The replacement of the gentamicin-resistance cassette by <i>hrpA</i> was confirmed by amplification of the segment of <i>hrpA</i> that was deleted in the KO strain GCB1164 (lane 8). <b>Panel 3</b>) The size of the <i>hrpA</i> gene was compared between wild-type (lane 14), <i>hrpA</i> KO (lane 13) and complemented clones (lanes 11 and 12). Lane 10 and 15 was a negative control containing ddH<sub>2</sub>O as template. A 100 bp and a 1 kb DNA ladder were used (M). The schematic in <b>A</b> of the figure is modified from <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841-Dresser1\" target=\"_blank\">[74]</a>.</p>", "links"=>[], "tags"=>["complementation", "insertion", "mutations", "burgdorferi"], "article_id"=>882574, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g004", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Strategy_for_complementation_and_insertion_of_point_mutations_in_B_burgdorferi_hrpA_/882574", "title"=>"Strategy for complementation and insertion of point mutations in <i>B. burgdorferi hrpA</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323282"], "description"=>"<p>ATPase activity was assayed as described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#s4\" target=\"_blank\">Materials and Methods</a>. ATPase activity of wild-type HrpA and five different point mutants was measured in the presence and absence of poly adenosine (RNA). The percentage of ATP hydrolyzed was determined by the release of <sup>32</sup>Pi from 1 mM of [γ-<sup>32</sup>P]ATP after incubation with 500 fmol purified HrpA per microliter of reaction for 1 h at 37°C with and without 1.1 nmol polyadenosine mononucleotide. Experiments were run in duplicate and the standard deviations are represented with error bars. Motifs and assigned functions are shown for the studied mutants.</p>", "links"=>[], "tags"=>["hydrolysis", "wild-type", "mutant", "hrpa"], "article_id"=>882571, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATP_Hydrolysis_by_wild_type_and_mutant_HrpA_proteins_/882571", "title"=>"ATP Hydrolysis by wild-type and mutant HrpA proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323315"], "description"=>"<p><sup>a</sup> All fractional values listed correspond to number of cultures positive/number of sites tested.</p><p><sup>b</sup> All % values listed represent the corresponding number of cultures positive/number of sites tested.</p><p><sup>c</sup> Complemented <i>hrpA</i> mutant where the mutant chromosomal gene was replaced with a wild-type gene.</p>", "links"=>[], "tags"=>["complementation", "mutations", "infectivity"], "article_id"=>882585, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_complementation_and_mutations_in_hrpA_on_B_burgdorferi_infectivity_in_C3H_HeN_mice_/882585", "title"=>"Effect of complementation and mutations in <i>hrpA</i> on <i>B. burgdorferi</i> infectivity in C3H/HeN mice.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323313"], "description"=>"<p><b>A</b>. Spirochete burdens in larvae (3 pools of 15 larvae per isolate) infected with either GCB1164 (<i>hrpA</i>) or GCB549 (Comp) by immersion and then fed to repletion on naïve C3H/HeJ mice. Genome copy numbers were assessed by qPCR using a TaqMan-based assay for <i>B. burgdorferi flaB</i> as previously described <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841-Mulay1\" target=\"_blank\">[73]</a>. Values represent the average <i>flaB</i> copy number per tick ± standard error of the mean in each pool. <b>B</b>. Spirochete burdens in flat nymphs (3 pools of 5 per isolate) and nymphs fed to repletion on naïve C3H/HeJ mice (3 pools of 8–10 nymphs per isolate). Genome copies numbers were assessed by qPCR as described for larvae. <b>C</b>. Representative micrographs of nymphs fed to repletion on naïve mice. Spirochetes were detected by immunofluorescence using FITC-conjugated α-<i>Borrelia</i> antibody as previously described <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841-Mulay1\" target=\"_blank\">[73]</a>. Scale bar, 25 µm. <b>D</b>. Viability of GCB1164 (<i>hrpA</i>) and GCB549 (Comp) in nymphs fed to repletion on naïve mice (5 mice per isolate). The average number of CFU per nymph is based on 5 pools (8–10 nymphs per pool) for each isolate (± standard deviation). Pools were serially-diluted (undiluted, 10<sup>−1</sup>, and 10<sup>−2</sup>) in BSK medium and plated in duplicate as previously described <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841-Caimano2\" target=\"_blank\">[75]</a>.</p>", "links"=>[], "tags"=>["molt", "nymphal"], "article_id"=>882583, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.g007", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HrpA_deficient_B_burgdorferi_persist_through_the_molt_and_survive_the_nymphal_blood_meal_/882583", "title"=>"HrpA-deficient <i>B. burgdorferi</i> persist through the molt and survive the nymphal blood meal.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-19 03:54:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1323314"], "description"=>"<p><sup>a</sup> 3 mice per isolate.</p><p><sup>b</sup> Based on immunoblot using whole cell lysates derived from temperature-shifted <i>B. burgdorferi</i> strain B31 5A4 NP1.</p><p><sup>c</sup> The area of skin below capsules used to contain feeding nymphs was excised within 24 hours of repletion (∼96 hour post-placement), divided into 6 equal portions for each mouse (5 mice per isolate), and cultured in BSK II medium containing the appropriate antibiotic as described previously <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841-DunhamEms1\" target=\"_blank\">[48]</a>.</p><p><sup>d</sup> One mouse in this group yielded no positive bite site cultures (0/6), most likely due to significantly lower spirochete burdens in the cohort of nymphs placed in this capsule (See <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003841#ppat.1003841.s001\" target=\"_blank\">Fig. S1</a>).</p>", "links"=>[], "tags"=>["infected", "hrpa-deficient"], "article_id"=>882584, "categories"=>["Biological Sciences"], "users"=>["Aydan Salman-Dilgimen", "Pierre-Olivier Hardy", "Justin D. Radolf", "Melissa J. Caimano", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003841.t002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nymphs_infected_with_HrpA_deficient_B_burgdorferi_are_unable_to_transmit_infection_/882584", "title"=>"Nymphs infected with HrpA-deficient <i>B. burgdorferi</i> are unable to transmit infection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-19 03:54:52"}

PMC Usage Stats | Further Information

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Relative Metric

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