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n2:pmcid: PMC0
bibo:doi: 10.1371%2Fjournal.pone.0007251
n4:contains: _:vb6142676 _:vb6142680 _:vb6142666 _:vb6142649

Subject Item: _:vb6142649
rdf:type: n4:Section
dc:title: introduction
n4:contains: _:vb6142650 _:vb6142651 _:vb6142652 _:vb6142653 _:vb6142654 _:vb6142655 _:vb6142656 _:vb6142657 _:vb6142658 _:vb6142659 _:vb6142660 _:vb6142661 _:vb6142662 _:vb6142663 _:vb6142664 _:vb6142665

Subject Item: _:vb6142650
rdf:type: n2:Context
rdf:value: Of the flaviviruses, DENV have the most significant impact on morbidity and mortality worldwide with over 100 million infections estimated annually [>>1<<]. In most cases, infection is either minimally symptomatic or results in an uncomplicated, though sometimes severe, acute febrile illness (dengue fever, DF). In a small percentage of cases, however, individuals develop a severe capillary
n2:mentions: n3:9665979

Subject Item: _:vb6142651
rdf:type: n2:Context
rdf:value: In a small percentage of cases, however, individuals develop a severe capillary leakage syndrome, dengue hemorrhagic fever (DHF), which can be life-threatening [>>2<<].
n2:mentions: n3:8903160

Subject Item: _:vb6142652
rdf:type: n2:Context
rdf:value: DHF is strongly associated with a secondary DENV infection, i.e. infection in individuals with pre-existing DENV-specific antibodies and memory T cells from an earlier infection with a different DENV serotype [>>3<<]–[5]. Therefore, experimental manipulation of in vivo immune responses to DENV would be a desirable approach to explore the role of prior immunity on subsequent DENV infection and to test the potential for candidate vaccines and
n2:mentions: n3:3341519

Subject Item: _:vb6142653
rdf:type: n2:Context
rdf:value: DHF is strongly associated with a secondary DENV infection, i.e. infection in individuals with pre-existing DENV-specific antibodies and memory T cells from an earlier infection with a different DENV serotype [3]–[>>5<<]. Therefore, experimental manipulation of in vivo immune responses to DENV would be a desirable approach to explore the role of prior immunity on subsequent DENV infection and to test the potential for candidate vaccines and therapeutics.
n2:mentions: n3:8032282

Subject Item: _:vb6142654
rdf:type: n2:Context
rdf:value: Subcutaneous injection of DENV into non-human primates results in productive infection with animals developing DENV-specific antibody and memory T cell responses [>>6<<], [7] but no clinical disease. Several murine models for DENV-induced disease have been reported that have been useful in dissecting some key aspects of disease pathogenesis [8]–[14].
n2:mentions: n3:4198027

Subject Item: _:vb6142655
rdf:type: n2:Context
rdf:value: Subcutaneous injection of DENV into non-human primates results in productive infection with animals developing DENV-specific antibody and memory T cell responses [6], [>>7<<] but no clinical disease. Several murine models for DENV-induced disease have been reported that have been useful in dissecting some key aspects of disease pathogenesis [8]–[14].
n2:mentions: n3:8166355

Subject Item: _:vb6142656
rdf:type: n2:Context
rdf:value: Several murine models for DENV-induced disease have been reported that have been useful in dissecting some key aspects of disease pathogenesis [>>8<<]–[14]. However, major limitations of these models include the use of very high input doses of virus, routes of inoculation that do not mimic natural infection and the use of mouse-adapted strains of virus.
n2:mentions: n3:10544083

Subject Item: _:vb6142657
rdf:type: n2:Context
rdf:value: Several murine models for DENV-induced disease have been reported that have been useful in dissecting some key aspects of disease pathogenesis [8]–[>>14<<]. However, major limitations of these models include the use of very high input doses of virus, routes of inoculation that do not mimic natural infection and the use of mouse-adapted strains of virus.
n2:mentions: n3:17360740

Subject Item: _:vb6142658
rdf:type: n2:Context
rdf:value: Previous attempts at engrafting immunodeficient mice with human cells as targets for DENV infection have yielded limited success partly because of low levels of human engraftment [>>15<<]. Bente and Moto et al immunized engrafted NOD-scid mice with clinical strains of DENV-2 [16], [17]. Infected engrafted mice developed clinical signs of dengue disease including thrombocytopenia and erythema compared to infected
n2:mentions: n3:7771614

Subject Item: _:vb6142659
rdf:type: n2:Context
rdf:value: Bente and Moto et al immunized engrafted NOD-scid mice with clinical strains of DENV-2 [16], [>>17<<]. Infected engrafted mice developed clinical signs of dengue disease including thrombocytopenia and erythema compared to infected non-engrafted mice and uninfected engrafted mice. Kuruvilla et al used humanized BALB/c-RAG2−/−γc −/− mice
n2:mentions: n3:16227299

Subject Item: _:vb6142660
rdf:type: n2:Context
rdf:value: Kuruvilla et al used humanized BALB/c-RAG2−/−γc −/− mice (RAG hu) and demonstrated that these mice developed dengue-specific IgM and IgG antibodies several weeks after infection [>>18<<]. The data by these two groups are promising, however human T cell responses in engrafted mice were not examined in either of these studies.
n2:mentions: n3:17707071

Subject Item: _:vb6142661
rdf:type: n2:Context
rdf:value: Novel mouse models have recently been described that permit long term multi-lineage human hematopoiesis and immune response [>>19<<]–[21]. We utilized NOD-scid IL2rγnull mice, considered the “gold standard” strain for human hematolymphoid development to determine whether humanized mice will support productive infection with DENV [20], [22]–[24].
n2:mentions: n3:15879151

Subject Item: _:vb6142662
rdf:type: n2:Context
rdf:value: Novel mouse models have recently been described that permit long term multi-lineage human hematopoiesis and immune response [19]–[>>21<<]. We utilized NOD-scid IL2rγnull mice, considered the “gold standard” strain for human hematolymphoid development to determine whether humanized mice will support productive infection with DENV [20], [22]–[24].
n2:mentions: n3:16954502

Subject Item: _:vb6142663
rdf:type: n2:Context
rdf:value: We utilized NOD-scid IL2rγnull mice, considered the “gold standard” strain for human hematolymphoid development to determine whether humanized mice will support productive infection with DENV [>>20<<], [22]–[24].
n2:mentions: n3:17259968

Subject Item: _:vb6142664
rdf:type: n2:Context
rdf:value: We utilized NOD-scid IL2rγnull mice, considered the “gold standard” strain for human hematolymphoid development to determine whether humanized mice will support productive infection with DENV [20], [>>22<<]–[24]. We identified human cells that were targets of in vitro and in vivo infection with DENV. Human T cells from infected engrafted mice produced IFN-γ, TNF-α and IL-2 in response to stimulation with three HLA A2 restricted dengue
n2:mentions: n3:9617892

Subject Item: _:vb6142665
rdf:type: n2:Context
rdf:value: We utilized NOD-scid IL2rγnull mice, considered the “gold standard” strain for human hematolymphoid development to determine whether humanized mice will support productive infection with DENV [20], [22]–[>>24<<]. We identified human cells that were targets of in vitro and in vivo infection with DENV. Human T cells from infected engrafted mice produced IFN-γ, TNF-α and IL-2 in response to stimulation with three HLA A2 restricted dengue
n2:mentions: n3:15920010

Subject Item: _:vb6142666
rdf:type: n4:Section
dc:title: materials and methods
n4:contains: _:vb6142672 _:vb6142673 _:vb6142674 _:vb6142675 _:vb6142668 _:vb6142669 _:vb6142670 _:vb6142671 _:vb6142667

Subject Item: _:vb6142667
rdf:type: n2:Context
rdf:value: Tg(HLA-A2/H2-D/β2M)1Dvs/Sz (hereafter termed NOD-scid IL2rγnull Tg(HLA-A2/Huβ2M) mice were bred at the Jackson Laboratory and subsequently maintained in the animal facilities at the University of Massachusetts Medical School [>>20<<]. The HLA-A2/Huβ2M transgene encodes a human β2-microglubulin (β2M) covalently linked to the MHC class 1, alpha1 and alpha2 binding domains of the human HLA-A2.1 gene and the alpha3, cytoplasmic and transmembrane domains of the murine
n2:mentions: n3:17259968

Subject Item: _:vb6142668
rdf:type: n2:Context
rdf:value: HLA-A2/Huβ2M transgene encodes a human β2-microglubulin (β2M) covalently linked to the MHC class 1, alpha1 and alpha2 binding domains of the human HLA-A2.1 gene and the alpha3, cytoplasmic and transmembrane domains of the murine H2-Db [>>40<<], [41].
n2:mentions: n3:17620420

Subject Item: _:vb6142669
rdf:type: n2:Context
rdf:value: transgene encodes a human β2-microglubulin (β2M) covalently linked to the MHC class 1, alpha1 and alpha2 binding domains of the human HLA-A2.1 gene and the alpha3, cytoplasmic and transmembrane domains of the murine H2-Db [40], [>>41<<].
n2:mentions: n3:16493087

Subject Item: _:vb6142670
rdf:type: n2:Context
rdf:value: (DENV-2-16681) and a low passage DENV-2 Thai isolate were propagated in C6/36 cells cultured in RPMI 1640 (Invitrogen, Grand Island, NY) containing 5% heat-inactivated fetal calf serum (FCS; Gibco) at 28°C as previously described [>>42<<]. The low passage clinical strain was isolated from the sera of a patient on Study Day 1 (strain K0005/94, passage 2) with a diagnosis of DHF-grade 2 in a prospective study of dengue infections in Thailand [43], [44].
n2:mentions: n3:9454689

Subject Item: _:vb6142671
rdf:type: n2:Context
rdf:value: The low passage clinical strain was isolated from the sera of a patient on Study Day 1 (strain K0005/94, passage 2) with a diagnosis of DHF-grade 2 in a prospective study of dengue infections in Thailand [>>43<<], [44]. Virus titers were determined by plaque-forming assay on Vero cells.
n2:mentions: n3:9237695

Subject Item: _:vb6142672
rdf:type: n2:Context
rdf:value: The low passage clinical strain was isolated from the sera of a patient on Study Day 1 (strain K0005/94, passage 2) with a diagnosis of DHF-grade 2 in a prospective study of dengue infections in Thailand [43], [>>44<<]. Virus titers were determined by plaque-forming assay on Vero cells.
n2:mentions: n3:9237696

Subject Item: _:vb6142673
rdf:type: n2:Context
rdf:value: RNA from different organs was subjected to reverse-transcription and amplification using a Qiagen One-Step RT-PCR Kit (Qiagen) with DENV-2-specific primers D1 and TS2 as described by Lanciotti et al [>>45<<].
n2:mentions: n3:1372617

Subject Item: _:vb6142674
rdf:type: n2:Context
rdf:value: Viral RNA copy numbers in different organs were measured by using quantitative real-time RT-PCR based TaqMan system (Applied Biosystems, Foster City, CA) [>>46<<]. The RNA was subjected to reverse-transcription and amplification using a TaqMan One-Step RT-PCR Master Mix Reagents Kit (PE Biosystems) with DENV-2 consensus primers (forward, 5′-CAGATCTCTGATGAATAACCAACG-3′, and reverse,
n2:mentions: n3:12812340

Subject Item: _:vb6142675
rdf:type: n2:Context
rdf:value: Vero cell lysates were prepared as previously described [>>42<<]. Golgi plug (BD Biosciences) was added to each of the above samples and incubated at 37°C.
n2:mentions: n3:9454689

Subject Item: _:vb6142676
rdf:type: n4:Section
dc:title: results
n4:contains: _:vb6142677 _:vb6142678 _:vb6142679

Subject Item: _:vb6142677
rdf:type: n2:Context
rdf:value: In accordance with published data [>>24<<], we obtained high levels of human hematolymphoid cell engraftment in these mice:
n2:mentions: n3:15920010

Subject Item: _:vb6142678
rdf:type: n2:Context
rdf:value: Human T cell responses were not analyzed in humanized BALB/c-RAG2−/−γc −/− and NOD-scid-humanized mouse models used previously to study DENV infection [16]–[>>18<<]. We assessed DENV-specific T cell immune responses to an inactivated DENV-2 antigen used routinely in our laboratory to assess DENV-specific human CD4+ T cell responses by intracellular IFN-γ staining using the gating strategy shown in
n2:mentions: n3:17707071

Subject Item: _:vb6142679
rdf:type: n2:Context
rdf:value: Splenocytes obtained from mice 7 days after infection with DENV-2 were stimulated with 3 HLA-A2 restricted peptides NS4b 2353(111–119), NS4b 2423(181–189), and NS4a 2148(56–64) identified in our laboratory [>>25<<]. We detected significant frequencies of antigen-specific T cells that responded to ex vivo stimulation with all three peptides by secreting IFN-γ, TNF-α and IL-2 (Figure 7A). A summary of CD3+ CD8+ IFN-γ T cell responses obtained from
n2:mentions: n3:16493038

Subject Item: _:vb6142680
rdf:type: n4:Section
dc:title: discussion
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Subject Item: _:vb6142681
rdf:type: n2:Context
rdf:value: We and others have observed varying degrees of infectivity following in vitro infection of human primary cells and cell lines with clinical and laboratory passaged strains of DENV-2 [>>26<<], [27]. The vast majority of infected cells detected were human CD45+CD19− cells and preliminary data suggest that CD11c+ dendritic cell precursors in the bone marrow of NOD-scid IL2rγnull mice may harbor DENV antigen (data not shown).
n2:mentions: n3:2178591

Subject Item: _:vb6142682
rdf:type: n2:Context
rdf:value: We and others have observed varying degrees of infectivity following in vitro infection of human primary cells and cell lines with clinical and laboratory passaged strains of DENV-2 [26], [>>27<<]. The vast majority of infected cells detected were human CD45+CD19− cells and preliminary data suggest that CD11c+ dendritic cell precursors in the bone marrow of NOD-scid IL2rγnull mice may harbor DENV antigen (data not shown). Although
n2:mentions: n3:15613313

Subject Item: _:vb6142683
rdf:type: n2:Context
rdf:value: Although some studies have identified B cells as an important target for DENV infection in humans, most data have pointed to infection of monocytes and possibly dendritic cells in vivo [>>15<<], [28]–[30].
n2:mentions: n3:7771614

Subject Item: _:vb6142684
rdf:type: n2:Context
rdf:value: Although some studies have identified B cells as an important target for DENV infection in humans, most data have pointed to infection of monocytes and possibly dendritic cells in vivo [15], [>>28<<]–[30]. Further studies using different serotypes and strains of DENV are required to identify predominant targets of infection after in vitro infection.
n2:mentions: n3:12414963

Subject Item: _:vb6142685
rdf:type: n2:Context
rdf:value: Although some studies have identified B cells as an important target for DENV infection in humans, most data have pointed to infection of monocytes and possibly dendritic cells in vivo [15], [28]–[>>30<<]. Further studies using different serotypes and strains of DENV are required to identify predominant targets of infection after in vitro infection.
n2:mentions: n3:12682107

Subject Item: _:vb6142686
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rdf:value: Bente and Mota et al recently reported that NOD-scid mice engrafted with human CD34+ stem cells were susceptible to infection with a low passage clinical isolate of DENV [16], [>>17<<]. Infected mice showed typical signs of dengue infection, including fever, rash, weight loss and thrombocytopenia.
n2:mentions: n3:16227299

Subject Item: _:vb6142687
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rdf:value: The NGC strain of DENV was originally serially passaged in mouse brains and later extensively passaged in cell culture for use by many laboratories [>>31<<]. We have not detected any neurological symptoms in engrafted mice after infection with DENV-2 NGC. Additionally, no virus was detected in any organs of infected non-engrafted mice suggesting that the engrafted human cells were necessary
n2:mentions: n3:9445071

Subject Item: _:vb6142688
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rdf:value: However, as reported by others [>>21<<], we detected little or no DENV-specific IgG (data not shown) suggesting that very low levels of class switching occurred in these mice.
n2:mentions: n3:16954502

Subject Item: _:vb6142689
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rdf:value: Variable and low IgG responses in these mice might be due to a lack of species cross-reactive cytokines in the xenogenic environment [>>32<<], [33]. We treated a small group of mice with B Lymphocyte Stimulatory Factor (BLyS), a factor known to promote human B cell survival [34], [35] and B cell engraftment in NOD-scid IL2rγnull mice (unpublished observations). Sera from
n2:mentions: n3:16301740

Subject Item: _:vb6142690
rdf:type: n2:Context
rdf:value: Variable and low IgG responses in these mice might be due to a lack of species cross-reactive cytokines in the xenogenic environment [32], [>>33<<]. We treated a small group of mice with B Lymphocyte Stimulatory Factor (BLyS), a factor known to promote human B cell survival [34], [35] and B cell engraftment in NOD-scid IL2rγnull mice (unpublished observations). Sera from BLyS-treated
n2:mentions: n3:15064419

Subject Item: _:vb6142691
rdf:type: n2:Context
rdf:value: We treated a small group of mice with B Lymphocyte Stimulatory Factor (BLyS), a factor known to promote human B cell survival [34], [>>35<<] and B cell engraftment in NOD-scid IL2rγnull mice (unpublished observations).
n2:mentions: n3:16931037

Subject Item: _:vb6142692
rdf:type: n2:Context
rdf:value: Kuruvilla et al demonstrated high levels of DENV-specific IgM and IgG in stem cell engrafted RAG-hu mice several weeks post infection [>>18<<]. However, only RAG-hu mice that were immunized with a pool of four different strains of DENV-2 generated a strong antibody response while mice infected with individual strains of DENV-2 had very low levels of dengue-specific antibodies.
n2:mentions: n3:17707071

Subject Item: _:vb6142693
rdf:type: n2:Context
rdf:value: Several studies have reported the important role of IFN-γ in the clearance of DENV infection [>>13<<], [36], [37].
n2:mentions: n3:9847388

Subject Item: _:vb6142694
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rdf:value: Several studies have reported the important role of IFN-γ in the clearance of DENV infection [13], [>>36<<], [37]. It remains unclear how the human T cells generated in NOD-scid IL2rγnull mice are effectively educated. While mature human T cells could develop by extrathymic education and selection [24], [33], presumably most of their education
n2:mentions: n3:10799569

Subject Item: _:vb6142695
rdf:type: n2:Context
rdf:value: Several studies have reported the important role of IFN-γ in the clearance of DENV infection [13], [36], [>>37<<]. It remains unclear how the human T cells generated in NOD-scid IL2rγnull mice are effectively educated. While mature human T cells could develop by extrathymic education and selection [24], [33], presumably most of their education occurs
n2:mentions: n3:11689052

Subject Item: _:vb6142696
rdf:type: n2:Context
rdf:value: While mature human T cells could develop by extrathymic education and selection [>>24<<], [33], presumably most of their education occurs in the murine thymus.
n2:mentions: n3:15920010

Subject Item: _:vb6142697
rdf:type: n2:Context
rdf:value: While mature human T cells could develop by extrathymic education and selection [24], [>>33<<], presumably most of their education occurs in the murine thymus.
n2:mentions: n3:15064419

Subject Item: _:vb6142698
rdf:type: n2:Context
rdf:value: Melkus et al were able to overcome this problem by using NOD-scid mice implanted with human fetal liver and thymic tissues to measure human EBV-specific immune responses [>>38<<].
n2:mentions: n3:17057712

Subject Item: _:vb6142699
rdf:type: n2:Context
rdf:value: to the 3 A2 restricted peptides by secreting IFN-γ in splenocytes of humanized mice (0.1–2.8% of total CD3+CD8+ T cells) is in line with frequencies detected in human PBMC of DENV immune donors (0.1–0.68% of total CD3+CD8+ T cells) [>>25<<]. These preliminary studies suggest that NOD-scid IL2rγnull Tg(HLA-A2/Huβ2M)mice can be used effectively to assess T cell responses to virus-specific peptides identified in humans.
n2:mentions: n3:16493038

Subject Item: _:vb6142700
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rdf:value: humanized mouse models including the requirement of human specific molecules for optimal function of the human immune system and issues of remaining innate immunity that present obstacles to human hematopoietic stem cell engraftment [>>39<<]. In addition, optimal conditions to ensure reliable human T and B cell engraftment will likely involve for example the use of neonatal rather than adult mice for engraftment and transgenic expression of select cytokines.
n2:mentions: n3:18481451

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