Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph
Publication Date
June 09, 2011
Journal
PLOS Pathogens
Authors
Lili Zhang, Yue Zhang, Sarojini Adusumilli, Lei Liu, et al
Volume
7
Issue
6
Pages
e1002079
DOI
https://dx.plos.org/10.1371/journal.ppat.1002079
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1002079
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21695244
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3111543
Europe PMC
http://europepmc.org/abstract/MED/21695244
Web of Science
000292379600017
Scopus
79959827638
Mendeley
http://www.mendeley.com/research/molecular-interactions-enable-movement-lyme-disease-agent-tick-gut-hemolymph
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Mendeley 3327 Apr 04:09 UTC

Mendeley | Further Information

{"title"=>"Molecular interactions that enable movement of the lyme disease agent from the tick gut into the hemolymph", "type"=>"journal", "authors"=>[{"first_name"=>"Lili", "last_name"=>"Zhang", "scopus_author_id"=>"55922441900"}, {"first_name"=>"Yue", "last_name"=>"Zhang", "scopus_author_id"=>"55922463000"}, {"first_name"=>"Sarojini", "last_name"=>"Adusumilli", "scopus_author_id"=>"55315899800"}, {"first_name"=>"Lei", "last_name"=>"Liu", "scopus_author_id"=>"56456776400"}, {"first_name"=>"Sukanya", "last_name"=>"Narasimhan", "scopus_author_id"=>"7103035763"}, {"first_name"=>"Jianfeng", "last_name"=>"Dai", "scopus_author_id"=>"36722536600"}, {"first_name"=>"Yang O.", "last_name"=>"Zhao", "scopus_author_id"=>"31067583100"}, {"first_name"=>"Erol", "last_name"=>"Fikrig", "scopus_author_id"=>"7102240544"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"doi"=>"10.1371/journal.ppat.1002079", "sgr"=>"79959827638", "issn"=>"15537366", "pui"=>"362058362", "isbn"=>"1553-7374 (Electronic) 1553-7366 (Linking)", "pmid"=>"21695244", "scopus"=>"2-s2.0-79959827638"}, "id"=>"176c5289-4e98-37a0-80f3-d19071ab7c70", "abstract"=>"Borrelia burgdorferi, the causative agent of Lyme disease, is transmitted to humans by bite of Ixodes scapularis ticks. The mechanisms by which the bacterium is transmitted from vector to host are poorly understood. In this study, we show that the F(ab)(2) fragments of BBE31, a B.burgdorferi outer-surface lipoprotein, interfere with the migration of the spirochete from tick gut into the hemolymph during tick feeding. The decreased hemolymph infection results in lower salivary glands infection, and consequently attenuates mouse infection by tick-transmitted B. burgdorferi. Using a yeast surface display approach, a tick gut protein named TRE31 was identified to interact with BBE31. Silencing tre31 also decreased the B. burgdorferi burden in the tick hemolymph. Delineating the specific spirochete and arthropod ligands required for B. burgdorferi movement in the tick may lead to new strategies to interrupt the life cycle of the Lyme disease agent.", "link"=>"http://www.mendeley.com/research/molecular-interactions-enable-movement-lyme-disease-agent-tick-gut-hemolymph", "reader_count"=>32, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>16, "Medicine and Dentistry"=>6, "Philosophy"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United States"=>2, "Brazil"=>1, "Portugal"=>1}, "group_count"=>1}
Scopus 3728 Nov 23:30 UTC

Scopus | Further Information

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Figshare 3510 May 18:55 UTC

Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/767459"], "description"=>"<p>(A) <i>tre31</i> mRNA was dramatically reduced within <i>tre31 ds</i>RNA-treated tick guts. Equal volumes of <i>tre31 ds</i>RNA (tre31 ds) or Elute Buffer (Buffer) were delivered directly into the gut of N40-infected <i>Ixodes</i> nymphs via microinjection. Ticks were allowed to rest for 3 hours and feed on C3H mice for 66 hr. <i>tre31</i> expression in tick gut was measured by q-RT-PCR. (**: <i>p</i><0.01) (B) <i>B.burgdoferi</i> burden in the tick gut was not influenced by <i>tre31</i> deficiency. (C) <i>B.burgdoferi</i> burden in tick salivary glands was decreased by <i>tre31</i> deficiency (*: <i>p</i><0.05). (D) <i>B.burgdoferi</i> burden in tick hemolymph was decreased by <i>tre31</i> deficiency (*: <i>p</i><0.05). Each dot represents 2 tick gut or salivary glands, or 4 hemolymph. Experiments were repeated two times.</p>", "links"=>[], "tags"=>["interfered", "spirochete", "tick"], "article_id"=>437824, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g007", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_tre31_ds_RNA_interfered_with_the_migration_of_B_burgdorferi_within_I_scapularis_during_spirochete_transmission_from_tick_to_the_host_/437824", "title"=>"<i>tre31 ds</i>RNA interfered with the migration of <i>B.burgdorferi</i> within <i>I.scapularis</i> during spirochete transmission from tick to the host.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:10:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/385316"], "description"=>"<div><p><em>Borrelia burgdorferi</em>, the causative agent of Lyme disease, is transmitted to humans by bite of <em>Ixodes scapularis</em> ticks. The mechanisms by which the bacterium is transmitted from vector to host are poorly understood. In this study, we show that the F(ab)<sub>2</sub> fragments of BBE31, a <em>B.burgdorferi</em> outer-surface lipoprotein, interfere with the migration of the spirochete from tick gut into the hemolymph during tick feeding. The decreased hemolymph infection results in lower salivary glands infection, and consequently attenuates mouse infection by tick-transmitted <em>B. burgdorferi</em>. Using a yeast surface display approach, a tick gut protein named TRE31 was identified to interact with BBE31. Silencing <em>tre31</em> also decreased the <em>B. burgdorferi</em> burden in the tick hemolymph. Delineating the specific spirochete and arthropod ligands required for <em>B. burgdorferi</em> movement in the tick may lead to new strategies to interrupt the life cycle of the Lyme disease agent.</p> </div>", "links"=>[], "tags"=>["molecular", "interactions", "lyme", "tick", "hemolymph"], "article_id"=>136070, "categories"=>["Cancer"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Molecular_Interactions_that_Enable_Movement_of_the_Lyme_Disease_Agent_from_the_Tick_Gut_into_the_Hemolymph/136070", "title"=>"Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-09 01:41:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/767018"], "description"=>"<p>(A) <i>B.burgdorferi</i> burden in <i>I.scapularis</i> gut and salivary glands assayed by q-PCR. N40-infected nymphs fed on C3H mice, which were injected with normal rabbit serum (NRS), BBE31 antiserum (BBE31 Ab) or BBI16 antiserum (BBI16 Ab), for 66 hours. DNA was extracted from both gut and salivary glands for q-PCR analysis. Each dot represents 5 guts or pairs of salivary glands. Data were collected from 3 studies of tick-feedings. *: P<0.05. (B) <i>B.burgdorferi</i> burden in the <i>I.scapularis</i> gut and salivary glands assayed by confocal microscopy. Murine immunization and tick feeding are the same as that in part (A). The spirochetes were probed with FITC-labeled goat anti-<i>borrelia</i> antibodies (shown in green), the nucleolus were stained with TO-PRO-3 (shown in blue). Orthogonal views (<i>xz</i> and <i>yz</i> axes) revealing the distribution of spirochetes through the full thickness of the infected salivary glands are shown. The gut and salivary gland samples were examined with the magnification of 63x and 25x, respectively. Scale bar represents 20 µm.</p>", "links"=>[], "tags"=>["antibodies", "salivary"], "article_id"=>437385, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BBE31_antibodies_block_B_burgdorferi_migration_from_I_scapularis_gut_to_the_salivary_glands_/437385", "title"=>"BBE31 antibodies block <i>B.burgdorferi</i> migration from <i>I.scapularis</i> gut to the salivary glands.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:03:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/767376"], "description"=>"<p>(A) Nucleotide and predicted amino acid sequences of TRE31. The <i>tre31</i> nucleotide sequence was deduced from the alignment of sequenced tick gut genes, which were expressed by yeast cells enriched through biotinylated BBE31, with several databases (BLAST search, GenBank and EMBL nonredundant databases). Two <i>I.scapularis</i> contigs <u>IscW_ISCW017272</u> and <u>IscW_ISCW017271</u> (arrows) were identified from the databases, which showed 100% and 98% nucleotide identity with <i>tre31</i> N-terminal and C-terminal sequences, respectively. The predicted peptide sequences of both contigs are in-frame with each other and constitute a protein of 302 amino acids. Among the 16 sequenced <i>tre31</i> copies expressed by enriched yeast cells, 4 different N-terminals were found (shading). The longest TRE31 copy is from amino acid 31 to 302. Protein sequence analysis through SignalP 3.0 revealed a signal peptide in the N-terminal (underlining) with the cleavage site between amino acid 23 (A) and 24 (K). (B) BBE31specifically interacts with yeast cells expressing TRE31. Plasmid containing <i>tre31</i> or the empty vector pYD1 was introduced into yeast competent cell EYB100, respectively. Both kinds of yeast cells were grown in SDCAA, induced in SGCAA, enriched through biotinylated BBE31 or OspC, and enriched cells eluted from the MACS column for quantification. Protein interaction was assessed by the elution percentage. (C) <i>tre31</i> expression in tick. <i>tre31</i> expression in unfed clean nymphal gut (Unfed Clean), N40-infected unfed nymphal gut (Unfed Gut), guts and salivary glands of N40-nymphs fed on C3H mice for 66 hours (Fed Gut and Fed SG), was measure by q-RT-PCR. Mean and SD were calculated from 6 mRNA samples.</p>", "links"=>[], "tags"=>["bbe31", "tre31"], "article_id"=>437746, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Confirmation_of_the_interaction_between_BBE31_and_TRE31_in_vitr_o_/437746", "title"=>"Confirmation of the interaction between BBE31 and TRE31 <i>in vitr</i>o.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:09:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/766928"], "description"=>"<p>(A) Protease digestion assay. Intact <i>B. burgdorferi</i> N40 cells were incubated with Protease K in the absence (-) or presence (+) of 0.05% Triton X-100. After digestion, cells were lysed and proteins were fractionated by SDS-PAGE. Immunoblots were developed with anti-BBE31 or anti-BB0365 (an inner membrane protein). 0, 20, 200: Protease K concentration is 0, 20 or 200 µg/ml. (B) Indirect immunofluorescence staining. Intact unfixed or methanol-fixed <i>B. burgdorferi</i> N40 were incubated with primary rabbit anti-BBE31 (right panels) or rabbit anti-BB0365 (left panels) antibodies, then incubated with the secondary antibodies Alexa 488-labelled goat anti-rabbit. Magnification, x63. Scale bar represents 20 µm.</p>", "links"=>[], "tags"=>["localization"], "article_id"=>437294, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Subcellular_localization_of_BBE31_/437294", "title"=>"Subcellular localization of BBE31.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:01:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/766830"], "description"=>"<p><i>bbe31</i> is preferentially expressed in fed tick. It is induced from the 2<sup>nd</sup> day, expressed in all the tested tissues including gut, hemolymph and salivary glands, and showed the highest expression level in the fed gut. Both mean and SD were calculated from 2 independent experiments, with 3 mRNA samples each experiment. <i>In vitro</i>, <i>B.burgdorferi</i> N40 grown in BSK medium with a concentration of 1×10<sup>7</sup>/ml; Larva, <i>I.scapularis</i> larva fed on N40-infected mouse till engorged; day4, larva 4-day after feeding; day 21; larva 21-day after feeding; day1 Gut, day2 Gut and day3 Gut, guts of N40-nymphs feeding on C3H mice for 24, 48 and 72 hours; SG, salivary glands; HL, hemolymph; Injection, mouse inoculated with 1*10<sup>6 </sup><i>B.burgdorferi</i> N40; day1, day2 and day3, mouse localized skin 24, 48 or 72 hours after <i>B.burgdorferi</i> N40 infection through needle inoculation; skin, heart, bladder and joint, mouse tissues collected 21 days after N40-infected nymphs feeding on C3H mice.</p>", "links"=>[], "tags"=>["stages", "spirochete"], "article_id"=>437200, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_bbe3_1_expression_profile_throughout_representative_stages_of_the_natural_spirochete_life_cycle_/437200", "title"=>"<i>bbe3</i>1 expression profile throughout representative stages of the natural spirochete life cycle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/767127"], "description"=>"<p>(A) BBE31 antibodies protect mouse from infection by tick-transmitted <i>B. burgdorferi</i>. Six of N40-infected nymphs were placed on 1 mouse, which has been injected with normal rabbit serum (NRS), BBE31 antiserum (E31) or BBI16 antiserum (I16), allowing to feed till exhausted. Twenty-one days later, the <i>B. burgdorferi</i> burden in mouse skin, bladder, heart and joints tissues were measured by q-PCR. Each dot represents 1 mouse. *: <i>p</i><0.05, **: <i>p</i><0.01. (B) BBE31 antibodies can't protect mice from infection by needle-inoculated <i>B. burgdorferi</i>. Mice were injected with rabbit normal serum (NRS) or BBE31 antiserum (E31). Twenty-four hours later, 10<sup>2</sup> of cultured <i>B.burgdorferi</i> N40 were intraperitoneally inoculated into the mice. <i>B.burgdorferi</i> burden in murine tissues were measured 21 days after <i>Borrelia</i> inoculation. Each dot represents 1 mouse. (C) Mice protection by BBE31 antiserum determined by <i>in vitro</i> culture of skin, bladder, heart and joints. Mice tissues used for culture were the same as those described above (4A and 4B). 10<sup>2</sup> Bb inoculation and 10<sup>3</sup> Bb inoculation: 10<sup>2</sup> or 10<sup>3</sup> of <i>B.burgdorferi</i> N40 in BSK medium were needle-inoculated into each C3H mouse. NA: not assayed.</p>", "links"=>[], "tags"=>["bbe31", "antibodies", "infectivity"], "article_id"=>437490, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Influence_of_BBE31_antibodies_on_B_burgdorferi_infectivity_in_mice_/437490", "title"=>"Influence of BBE31 antibodies on <i>B.burgdorferi</i> infectivity in mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:04:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/767263"], "description"=>"<p>(A) <i>Borreliacidal</i> activity of BBE31 F(ab)<sub>2</sub> fragments against <i>B. burgdorferi</i>. <i>B.burgdorferi</i> N40 were incubated in BSK medium in the absence (Control) or presence of F(ab)<sub>2</sub> fragments prepared from normal rabbit serum [NRS F(ab)<sub>2</sub>] or BBE31 antiserum [BBE31 F(ab)<sub>2</sub>]. A borreliacidal serum from a patient with diagnosed Lyme Disease (<i>B.burgdorferi</i> antisera) was used as a positive control. The number of spirochetes was assessed by dark-field microscopy after 24 and 48 hours of incubation. Data are presented relative to controls without treatment. Data represent the number of spirochetes remaining viable after treatment (mean ± SD, n = 4). Difference between control and NRS F(ab)<sub>2</sub>- as well as BBE31 F(ab)<sub>2</sub>-treated samples were not statistically significant. (B) <i>B.burgdorferi</i> burden in <i>I.scapularis</i> hemolymph assayed by q-PCR. N40-infected nymphs fed on C3H mice, which had been injected with F(ab)<sub>2</sub> fragments of either normal rabbit IgG (NRS-F(ab)<sub>2</sub>) or anti-BBE31 IgG (BBE31-F(ab)<sub>2</sub>), for 66 hours. DNA was extracted from the hemolymph for q-PCR analysis. Each dot represents hemolymph from 5 ticks. Data were collected from 2 times of tick-feedings. *: <i>p</i><0.05. (C) <i>B.burgdorferi</i> burden in <i>I.scapularis</i> hemolymph assayed by confocal microscope. Tick feeding is the same as that described in part (A). The spirochetes in tick hemolymph were probed with FITC-labeled goat anti-<i>borrelia</i> antibodies (shown in green), the hemocyte nucleolus were stained with TO-PRO-3 (shown in blue). The FITC and TO-PRO-3 images were examined at ×25 magnifications and are presented as merged images. Scale bar represents 20 µm. (D) Spirochetes lacking <i>bbe31</i> can survive in tick hemolymph and invade the salivary glands. <i>B.burgdorferi</i> wild-type strain MSK5 and the lp25-lacking isolate ML23 were grown in BSK medium, resuspended in PBS and microinjected into partially-fed clean nymphal hemocoel (clean nymphs fed on C3H mice for 48 hours before microinjection). Six hours later, both hemolymph (HL) and salivary glands (SG) were collected for <i>B.burgdorferi</i> quantification by q-PCR. Mean and SD were calculated from 5 mRNA samples and 5 ticks were grouped for 1 mRNA sample.</p>", "links"=>[], "tags"=>["fragments", "anti-bbe31", "igg"], "article_id"=>437627, "categories"=>["Infectious Diseases"], "users"=>["Lili Zhang", "Yue Zhang", "Sarojini Adusumilli", "Lei Liu", "Sukanya Narasimhan", "Jianfeng Dai", "Yang O. Zhao", "Erol Fikrig"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002079.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_F_ab_2_fragments_of_anti_BBE31_IgG_interfere_with_B_burgdorferi_migration_from_I_scapularis_gut_into_hemolymph_/437627", "title"=>"F(ab)<sub>2</sub> fragments of anti-BBE31 IgG interfere with <i>B.burgdorferi</i> migration from <i>I.scapularis</i> gut into hemolymph.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-09 02:07:07"}
PMC Usage Stats 150317 Nov 19:27 UTC

PMC Usage Stats | Further Information

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Relative Metric 75344710 May 17:15 UTC

Relative Metric

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F1000Prime 111 Dec 12:35 UTC

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