Inheritance of DNA Transferred from American Trypanosomes to Human Hosts
Publication Date
February 12, 2010
Journal
PLOS ONE
Authors
Mariana M. Hecht, Nadjar Nitz, Perla F. Araujo, Alessandro O. Sousa, et al
Volume
5
Issue
2
Pages
e9181
DOI
https://dx.plos.org/10.1371/journal.pone.0009181
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0009181
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20169193
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2820539
Europe PMC
http://europepmc.org/abstract/MED/20169193
Web of Science
000274474600004
Scopus
77949438260
Mendeley
http://www.mendeley.com/research/inheritance-dna-transferred-american-trypanosomes-human-hosts
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CiteULike | Further Information

Mendeley | Further Information

{"title"=>"Inheritance of DNA transferred from American trypanosomes to human hosts", "type"=>"journal", "authors"=>[{"first_name"=>"Mariana M.", "last_name"=>"Hecht", "scopus_author_id"=>"23496492000"}, {"first_name"=>"Nadjar", "last_name"=>"Nitz", "scopus_author_id"=>"6602292970"}, {"first_name"=>"Perla F.", "last_name"=>"Araujo", "scopus_author_id"=>"36092445200"}, {"first_name"=>"Alessandro O.", "last_name"=>"Sousa", "scopus_author_id"=>"36093247700"}, {"first_name"=>"Ana De Cássia", "last_name"=>"Rosa", "scopus_author_id"=>"15823172300"}, {"first_name"=>"Dawidson A.", "last_name"=>"Gomes", "scopus_author_id"=>"9839298200"}, {"first_name"=>"Eduardo", "last_name"=>"Leonardecz", "scopus_author_id"=>"23061013200"}, {"first_name"=>"Antonio R L", "last_name"=>"Teixeira", "scopus_author_id"=>"35552540300"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77949438260", "sgr"=>"77949438260", "pui"=>"358460787", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"20169193", "doi"=>"10.1371/journal.pone.0009181"}, "id"=>"deb667e0-32b7-33ad-9b86-720101d72934", "abstract"=>"Interspecies DNA transfer is a major biological process leading to the accumulation of mutations inherited by sexual reproduction among eukaryotes. Lateral DNA transfer events and their inheritance has been challenging to document. In this study we modified a thermal asymmetric interlaced PCR by using additional targeted primers, along with Southern blots, fluorescence techniques, and bioinformatics, to identify lateral DNA transfer events from parasite to host. Instances of naturally occurring human infections by Trypanosoma cruzi are documented, where mitochondrial minicircles integrated mainly into retrotransposable LINE-1 of various chromosomes. The founders of five families show minicircle integrations that were transferred vertically to their progeny. Microhomology end-joining of 6 to 22 AC-rich nucleotide repeats in the minicircles and host DNA mediates foreign DNA integration. Heterogeneous minicircle sequences were distributed randomly among families, with diversity increasing due to subsequent rearrangement of inserted fragments. Mosaic recombination and hitchhiking on retrotransposition events to different loci were more prevalent in germ line as compared to somatic cells. Potential new genes, pseudogenes, and knockouts were identified. A pathway of minicircle integration and maintenance in the host genome is suggested. Thus, infection by T. cruzi has the unexpected consequence of increasing human genetic diversity, and Chagas disease may be a fortuitous share of negative selection. This demonstration of contemporary transfer of eukaryotic DNA to the human genome and its subsequent inheritance by descendants introduces a significant change in the scientific concept of evolutionary biology and medicine.", "link"=>"http://www.mendeley.com/research/inheritance-dna-transferred-american-trypanosomes-human-hosts", "reader_count"=>93, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>12, "Researcher"=>23, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>5, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>10}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>12, "Researcher"=>23, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>5, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>57, "Medicine and Dentistry"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>1, "Chemistry"=>3, "Psychology"=>1, "Social Sciences"=>2, "Computer Science"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>3}, "Social Sciences"=>{"Social Sciences"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>57}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>2, "Brazil"=>1, "United Kingdom"=>2, "Italy"=>1, "France"=>1, "Spain"=>1, "Russia"=>1}, "group_count"=>6}

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Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/863057"], "description"=>"<p>kDNA integrations were co-localized in metaphase plates of nine patients from families <b>a</b>, <b>b</b>, and <b>c</b> with the 350-bp probe resulting from <i>Nsi</i>I digest of wild-type kDNA, and with the LINE-1 clone 198 probe. (A) <i>T. cruzi</i> epimastigote fluorescein-labeled antibody (green) from Chagas patient serum (left) and control non-chagasic serum (right). The parasite silhouette is seen by digital image of contrast. B) <i>T. cruzi</i> DNA (Hoechst in blue), nDNA (Cy3 in red) and kDNA (FITC in green). The merged panel showed the parasite DNAs positioned with the digital image of contrast. C) <i>Leishmania (viannia) braziliensis</i> Hoechst stained DNA (blue); in absence of staining red (Cy3-LINE) and green (fluorescein-kDNA), respectively, with the 350-bp kDNA and with the LINE clone 180 probes. The merge was not positioned with the digital image of contrast. D) Metaphase chromosomes (blue), LINE-1 (red) and kDNA (green). The merge positioned with the digital image of contrast. Scale bars  = 5 µm.</p>", "links"=>[], "tags"=>["kdna", "metaphase", "chromosomes", "mononuclear"], "article_id"=>533504, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_localizing_Trypanosoma_cruzi_kDNA_sequence_in_metaphase_plate_chromosomes_from_human_blood_mononuclear_cells_/533504", "title"=>"Co-localizing <i>Trypanosoma cruzi</i> kDNA sequence in metaphase plate chromosomes from human blood mononuclear cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 00:58:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/862844"], "description"=>"<p>(A) Representative PCR amplifications of <i>T. cruzi</i> kDNA and nDNA. kDNA and nDNA signatures indicate active infections and LkDTs, while only kDNA indicates LkDT. Amplification products obtained with kDNA (S35/S36) and nDNA (Tcz1/Tcz2) primer sets hybridized with specific internal probes S67 and Tcz3, respectively, on blots of 1% agarose gels. The numbers above each lane indicates the study case. Tc, <i>T. cruzi</i>. Patients 10, 34, 51, 61 and 71, showing nDNA and kDNA signatures, harbor active <i>T. cruzi</i> infections. Patients 9, 36, 50 and 60, with only the kDNA signature, may carry inherited integration events. (B) Southern hybridization of integrated kDNA revealed by a minicircle (kCR) probe. A 0.8% agarose gel was used to analize <i>Eco</i>RI-digested DNA from Chagas patient blood mononuclear cells. Top numbers indicate family founders who had the kDNA integrations in LINE-1 on chromosome X (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009181#pone.0009181.s009\" target=\"_blank\">Table S3</a>). DNA from uninfected human donors (C2 to C5) and from <i>T. cruzi</i> were included as controls. (C) Schematic representation of microhomology-mediated end-joining kDNA minicircle integration into retrotransposon LINE-1. Patients 71 (top) and 24 (bottom) show AC-rich intermediates involved in recombination. Each patient showing nDNA and/or kDNA footprints yielded at least one chimeric sequence.</p>", "links"=>[], "tags"=>["somatic", "cells", "suggests", "kdna", "homologous"], "article_id"=>533289, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g003", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LkDT_in_somatic_cells_suggests_mechanism_of_kDNA_integration_by_homologous_recombination_/533289", "title"=>"LkDT in somatic cells suggests mechanism of kDNA integration by homologous recombination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 00:54:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/863299"], "description"=>"<p>(A) Infection-induced host DNA (green) double strand-break (DSB) and integration of kDNA minicircle sequence (blue) mediated by microhomology end-joining. (B) Replication of the kDNA-LINE sequence by target-primed reverse-transcription using the autonomous recombination machinery of the LINE-1. The kDNA sequence repeat received a specific cut, and free-end pairing with a first strand transcript (green). A complementary second strand transcript is made, which can transpose to different chromosomes.</p>", "links"=>[], "tags"=>["minicircle", "replication"], "article_id"=>533749, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g007", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_Trypanosoma_cruzi_minicircle_integration_and_replication_in_the_human_genome_/533749", "title"=>"Model of <i>Trypanosoma cruzi</i> minicircle integration and replication in the human genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 01:02:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/863200"], "description"=>"<p>Donors of diploid peripheral blood mononuclear cell DNA: Male, open square; female, open circle. Donors of haploid sperm cell DNA are indicated by yellow-edged square. Patients showing <i>T. cruzi</i> nDNA and kDNA are represented by red square or circle. Patients having integrated kDNA alone are identified by blue square or circle. Absence of a serial number means no biological sampling. A case deceased is indicated by crossed square. Volunteer samples were challenged by nDNA and kDNA amplifications withTcz1/Tcz2 and with S34/S67 primer sets, and blot hybridization with nDNA and kDNA probes. Each family member having nDNA and/or kDNA footprints yielded at least one chimeric sequence.</p>", "links"=>[], "tags"=>["patchwork", "resulting", "lkdt"], "article_id"=>533648, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_patchwork_resulting_from_LkDT_and_VkDT_/533648", "title"=>"Phylogenetic patchwork resulting from LkDT and VkDT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 01:00:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/429387", "https://ndownloader.figshare.com/files/429443", "https://ndownloader.figshare.com/files/429480", "https://ndownloader.figshare.com/files/429532", "https://ndownloader.figshare.com/files/429559", "https://ndownloader.figshare.com/files/429604", "https://ndownloader.figshare.com/files/429654", "https://ndownloader.figshare.com/files/429693", "https://ndownloader.figshare.com/files/429730", "https://ndownloader.figshare.com/files/429860", "https://ndownloader.figshare.com/files/429979", "https://ndownloader.figshare.com/files/430027"], "description"=>"<div><p>Interspecies DNA transfer is a major biological process leading to the accumulation of mutations inherited by sexual reproduction among eukaryotes. Lateral DNA transfer events and their inheritance has been challenging to document. In this study we modified a thermal asymmetric interlaced PCR by using additional targeted primers, along with Southern blots, fluorescence techniques, and bioinformatics, to identify lateral DNA transfer events from parasite to host. Instances of naturally occurring human infections by <em>Trypanosoma cruzi</em> are documented, where mitochondrial minicircles integrated mainly into retrotransposable LINE-1 of various chromosomes. The founders of five families show minicircle integrations that were transferred vertically to their progeny. Microhomology end-joining of 6 to 22 AC-rich nucleotide repeats in the minicircles and host DNA mediates foreign DNA integration. Heterogeneous minicircle sequences were distributed randomly among families, with diversity increasing due to subsequent rearrangement of inserted fragments. Mosaic recombination and hitchhiking on retrotransposition events to different loci were more prevalent in germ line as compared to somatic cells. Potential new genes, pseudogenes, and knockouts were identified. A pathway of minicircle integration and maintenance in the host genome is suggested. Thus, infection by <em>T. cruzi</em> has the unexpected consequence of increasing human genetic diversity, and Chagas disease may be a fortuitous share of negative selection. This demonstration of contemporary transfer of eukaryotic DNA to the human genome and its subsequent inheritance by descendants introduces a significant change in the scientific concept of evolutionary biology and medicine.</p></div>", "links"=>[], "tags"=>["inheritance", "dna", "transferred", "american", "trypanosomes", "hosts"], "article_id"=>144765, "categories"=>["Immunology", "Biological Sciences", "Physics", "Microbiology", "Cancer", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0009181.s001", "https://dx.doi.org/10.1371/journal.pone.0009181.s002", "https://dx.doi.org/10.1371/journal.pone.0009181.s003", "https://dx.doi.org/10.1371/journal.pone.0009181.s004", "https://dx.doi.org/10.1371/journal.pone.0009181.s005", "https://dx.doi.org/10.1371/journal.pone.0009181.s006", "https://dx.doi.org/10.1371/journal.pone.0009181.s007", "https://dx.doi.org/10.1371/journal.pone.0009181.s008", "https://dx.doi.org/10.1371/journal.pone.0009181.s009", "https://dx.doi.org/10.1371/journal.pone.0009181.s010", "https://dx.doi.org/10.1371/journal.pone.0009181.s011", "https://dx.doi.org/10.1371/journal.pone.0009181.s012"], "stats"=>{"downloads"=>9, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Inheritance_of_DNA_Transferred_from_American_Trypanosomes_to_Human_Hosts/144765", "title"=>"Inheritance of DNA Transferred from American Trypanosomes to Human Hosts", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-02-12 01:19:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/862645"], "description"=>"<p>Map showing five main ecosystems in Brazil: light gray, Cerrado, savannah-like; intermediate gray, Inland Atlantic forest; gray, Coastal Atlantic forest; dark gray, Caatinga, dry shrubs; black, Amazon-Tocantins rain-forest. Family pedigrees <b>a-</b>to<b>-e</b> showing intermingling of human populations from the five main ecosystems. Based on their epidemiological histories, families <b>a</b>, <b>b</b>, and <b>c</b> live in the urban Federal District of Brazil, where individuals are not exposed to the insect transmitters of <i>T. cruzi</i> infection. By contrast, country families <b>d</b> and <b>e</b> live in houses infested with the cone-nosed kissing bugs, vectors of <i>T. cruzi</i> infection. The red asterisks indicate family members with chronic <i>T. cruzi</i> infection as detected by ELISA, hemagglutination, and immunofluorescence exams, and by the parasite DNA signature. The red disks indicate individuals showing the parasite DNA signature in absence of anti-<i>T. cruzi</i> antibodies.</p>", "links"=>[], "tags"=>["members"], "article_id"=>533098, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Origin_of_family_members_in_this_study_/533098", "title"=>"Origin of family members in this study.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 00:51:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/862942"], "description"=>"<p>(A) Representative PCR amplifications of <i>T. cruzi</i> kDNA and nDNA from male gametes, obtained with kDNA S35/S36 and nDNA Tcz1/Tcz2 primers, and hybridization to a blot of a 1% agarose gels with the kCR probe. Top numbers indicate study cases. nDNA and kDNA signatures indicate active infections and LkDTs, while kDNA indicate VkDT. (B) Southern blot hybridizations of <i>Eco</i>RI digestions of human DNA with a kDNA-specific probe on blots of 0.8% agarose gels. Top numbers indicate family <b>c</b> F1 progeny (patient 50) married to Chagas case patient (51) showing kDNA integrations in LINE-1 on chromosome X. The DNA from the parents and from two progeny (patients 55 and 56) formed 3.2-kb bands, whereas DNA from progeny 57 and from uninfected patients (C1 and C2) did not. Tc, <i>T. cruzi</i>. (C) Frequency of kDNA integrations in chromosomes of somatic (dark blue) and of germ-line (light blue) cells.</p>", "links"=>[], "tags"=>["kdna", "germ", "somatic", "germline", "cells", "integrations"], "article_id"=>533395, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tracking_kDNA_into_germ_line_cells_and_distribution_of_somatic_and_germline_cells_integrations_into_chromosomes_/533395", "title"=>"Tracking kDNA into germ line cells, and distribution of somatic and germline cells integrations into chromosomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 00:56:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/862737"], "description"=>"<p>(A) Truncated fragments of minicircles found in the LINE-1 copy at chromosome Y <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009181#pone.0009181-SimesBarbosa1\" target=\"_blank\">[20]</a>; clone C showing conserved region annealed primer S36 (dark blue) at both ends followed by minicircle variable regions (light blue) and the LINE-1 sequence (green). (B) Targeted LINE-1 primers were used in combination with kDNA primer sets shown on top of the gel. The nested PCR reactions performed sequentially amplified target kDNA-host DNA sequences. The tertiary cycling products hybridizing with kDNA kCR probe on blots of 1% agarose gels were cloned and sequenced.</p>", "links"=>[], "tags"=>["modified", "minicircle", "integrations"], "article_id"=>533188, "categories"=>["Immunology", "Computational Biology", "Physics", "Microbiology", "Infectious Diseases", "Molecular Biology", "Evolutionary Biology", "Genetics", "Medicine"], "users"=>["Mariana M. Hecht", "Nadjar Nitz", "Perla F. Araujo", "Alessandro O. Sousa", "Ana de Cássia Rosa", "Dawidson A. Gomes", "Eduardo Leonardecz", "Antonio R. L. Teixeira"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009181.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_modified_tp_TAIL_PCR_used_to_detect_Trypanosoma_cruzi_minicircle_integrations_into_the_human_genome_/533188", "title"=>"The modified <i>tp</i>TAIL-PCR used to detect <i>Trypanosoma cruzi</i> minicircle integrations into the human genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-12 00:53:08"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"18", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
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Relative Metric

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